Leaf traits of congeneric host plants explain differences in performance of a specialist herbivore

1. Within the host range of herbivorous insects, performance hierarchies are often correlated with relatedness to a primary host plant, as plant traits are phylogenetically conserved. Therefore, it was hypothesised that differences in herbivore performance on closely related plant species are due to resistance traits that vary in magnitude, rather than in the nature of the traits. 2. This hypothesis was tested by manipulating putative resistance traits of three congeneric thistle species (Cirsium arvense, Cirsium palustre, and Cirsium vulgare) and assessing the performance of the oligophagous, leaf‐feeding beetle, Cassida rubiginosa. Measurements were done of survival, weight gain, and development time of the beetle on its primary host, C. arvense, and two alternative hosts under low and high nutrient availability, and on shaved and unshaved leaves. 3. Survival of C. rubiginosa was strongly dependent on plant species with final mean survival rates of 47%, 16%, and 8% on C. arvense, C. palustre, and C. vulgare, respectively. Survival was primarily explained by leaf trichome densities, and to a lesser extent by specific leaf area. Leaf flavonoid concentrations did not explain differences in beetle survival, and there were no differences in beetle weight gain or development time of individuals that survived to adulthood. 4. No beetles survived on unshaved (hairy) C. vulgare plants, but manipulating leaf trichome densities of the thistle species by shaving the leaves moderated the plant‐specific resistance, and equalised the survival rates. Survival of C. rubiginosa on alternative congeneric hosts was explained by a common physical resistance trait that varied in magnitude.     

Effects of competition and litter on a carnivorous plant, Drosera capillaris (Droseraceae)

Although carnivorous plants are widely recognized as being generally restricted to open habitats, tests of the effects of competition on individual performance are extremely rare. In this study, I examined the effects of the removal of herbaceous and shrub canopies on seedling density and growth, survival, and reproduction of phytometers of a small insectivorous plant, Drosera capillaris (pink sundew). I also examined the distribution of this species in relation to the occurrence of woody species in a frequently burned wet savanna in southeastern Mississippi. Killing plants and removing dead biomass increased seedling density in both open areas and shrub thickets. The removal of dead biomass following herbicide application was critical to increasing densities of seedlings. Killing plants with herbicide without also clearing residual litter and standing dead was not sufficient to increase seedling densities in shrub thickets. Although the removal of the groundcover canopy strongly influenced the density of seedlings, it had very little effect on survival, growth, and reproduction of small phytometers during a single growing season. Survival of phytometers was greater in open areas than in shrub thickets, regardless of whether the groundcover canopy was removed. Densities of both seedlings and adults were greater in open areas away from shrub thickets than beneath the woody canopies of thickets and were negatively correlated with the leaf area index of groundcover vegetation. Results of this study show that the establishment of this carnivorous plant species is limited in part by the effects of litter on seedling density in both open areas and shrub thickets.     

Soil nutrient effects on oviposition preference,larval performance,and chemical defense of a specialist insect herbivore

This study examined the effects of increased leaf nitrogen in natural host-plants (Plantago spp.) on female oviposition preference, larval performance, and larval chemical defense of the butterfly Junonia coenia. Increased availability of soil nutrients caused the host-plant’s foliar nitrogen to increase and its chemical defense to decrease. Larval performance did not correlate with increases in foliar nitrogen. Larval growth rate and survival were equivalent across host-plant treatments. However, larvae raised on fertilized host-plants showed concomitant decreases in chemical defense as compared to larvae reared on unfertilized host-plants. Since most butterfly larvae cannot move long distances during their first few instars and are forced to feed upon the plant on which they hatched, J. coenia larval chemical defense is determined, in large part, by female oviposition choice. Female butterflies preferred host-plants with high nitrogen over host-plants with low nitrogen; however, this preference was also mediated by plant chemical defense. Female butterflies preferred more chemically defended host-plants when foliar nitrogen was equivalent between host-plants. J. coenia larvae experience intense predation in the field, especially when larvae are not chemically well defended. Any qualitative or quantitative variation in plant allelochemical defense has fitness consequences on these larvae. Thus, these results indicate that females may be making sub-optimal oviposition decisions under a nutrient-enriched regime, when predators are present. Given the recent increase in fertilizer application and nitrogen deposition on the terrestrial landscape, these interactions between female preference, larval performance, and larval chemical defense may result in long-term changes in population dynamics and persistence of specialist insects.     

The nutritional landscape of host plants for a specialist insect herbivore

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Effect of the specialist herbivore Luehdorfia puziloi on the performance of a woodland herbaceous plant, Asarum heterotropoides

Plants show many responses to herbivore damage caused by insects. We investigated the effect of the specialist leaf herbivore Luehdorfia puziloi on the performance of a deciduous forest understory perennial herb Asarum heterotropoides . We conducted artificial defoliation experiments with different levels of damage (0, 50 or 100% clipping) in the early growing period (flowering time: early May) and in the late growing period (when natural herbivory by L. puziloi larvae occurs: early June) in a natural population. Effects of the defoliation treatments on reproduction (seed-set ratio) of A. heterotropoides in the treated year and on survival and development of the plant in the subsequent year were investigated. Severe defoliation conducted in the early period resulted in less current-year seed production and increased regression to a dormant or non-reproductive stage in the following year, which would reduce the probability of future flowering. In contrast, defoliation conducted in the late period had no effect on the reproduction, survival and development of A. heterotropoides . Similarly, we found no obvious correlation between the damaged leaf area during the later period and seed set. Our results show that the specialist herbivore L. puziloi did not influence the performance of A. heterotropoides by damaging the plant later in the season when it was tolerant of damage.     

Preference for outbred host plants and positive effects of inbreeding on egg survival in a specialist herbivore

Inbreeding can profoundly affect the interactions of plants with herbivores as well as with the natural enemies of the herbivores. We studied how plant inbreeding affects herbivore oviposition preference, and whether inbreeding of both plants and herbivores alters the probability of predation or parasitism of herbivore eggs. In a laboratory preference test with the specialist herbivore moth Abrostola asclepiadis and inbred and outbred Vincetoxicum hirundinaria plants, we discovered that herbivores preferred to oviposit on outbred plants. A field experiment with inbred and outbred plants that bore inbred or outbred herbivore eggs revealed that the eggs of the outbred herbivores were more likely to be lost by predation, parasitism or plant hypersensitive responses than inbred eggs. This difference did not lead to differences in the realized fecundity as the number of hatched larvae did not differ between inbred and outbred herbivores. Thus, the strength of inbreeding depression in herbivores decreases when their natural enemies are involved. Plant inbreeding did not alter the attraction of natural enemies of the eggs. We conclude that inbreeding can significantly alter the interactions of plants and herbivores at different life-history stages, and that some of these alterations are mediated by the natural enemies of the herbivores.     

Variation in phenology and nutritional quality between host plants and its effect on larval performance in a specialist butterfly,Zerynthia rumina

The main host plants of the butterfly Zerynthia rumina L. (Lepidoptera: Papilionidae) in southern Spain occur in different habitats and in general do not grow sympatrically. Therefore, each single local butterfly population uses the particular host available within its range. Aristolochia longa L. is a tuberous perennial herb available only in the spring, while A. baetica L. is an evergreen perennial vine with indeterminate growth. However, because of the toughness of older leaves, newly hatched larvae feed only on new leaves of A. baetica, and most of these leaves are produced well before the larvae hatch. In laboratory experiments, caterpillars feeding on either new or mature A. longa leaves grew faster and converted food into biomass more efficiently than those feeding on new A. baetica leaves. These differences are related to variation in nutritional quality among the host plants. Estimates of butterfly abundance were lower in sites where Z. rumina uses A. baetica, compared with those where the host is A. longa. The potential differential effect of these two food plants on the densities of local butterfly populations relying on them is discussed here.     

Herbivore and pathogen damage on grassland and woodland plants: a test of the herbivore uncertainty principle

Researchers can alter the behaviour and ecology of their study organisms by conducting such seemingly benign activities as non-destructive measurements and observations. In plant communities, researcher visitation and measurement of plants may increase herbivore damage in some plant species while decreasing it in others. Simply measuring plants could change their competitive ability by altering the amount of herbivore damage that they suffer. Currently, however, there is only limited empirical evidence to support this `herbivore uncertainty principle' (HUP). We tested the HUP by quantifying the amount of herbivore and pathogen damage in 13 plant species (> 1400 individuals) at four different visitation intensities at Cedar Creek Natural History Area, Minnesota, USA. Altogether, we found very little evidence to support the HUP at any intensity of visitation. Researcher visitation did not alter overall plant herbivore damage or survival and we did not detect a significant visitation effect in any of the 13 species. Pathogen damage also did not significantly vary among visitation treatments, although there was some evidence that high visitation caused slightly higher pathogen damage. Based on our results, we question whether this phenomenon should be considered a `principle' of plant ecology.     

Interactions between a specialist herbivore,Crocidosema plebejana,and its host plants Malva parviflora and cotton,Gossypium hirsutum: Oviposition preference

Ovipositional responses of gravid female Crocidosema plebejana Zeller (Lepidoptera: Tortricidae) to all stages of development of its host plants Malva parviflora L. and cotton, Gossypium hirsutum L., were studied in no-choice and choice experiments. In no-choice experiments the site of oviposition and the number of eggs laid reflected the suitability of the host plant for larval survival and development. The same was true of choice experiments although conclusions drawn from these are more tentative due to high levels of heterogeneity. Results from a natural (unplanned) choice experiment in the field, suggested flowering cotton was rejected as a site for oviposition by gravid females. Results from this paper and a previous paper by the authors are combined to explain the failure of tipworm populations to persist on cotton crops after flowering.     

Bryophytes as food: comparative consumption and utilization of mosses by a generalist insect herbivore

Compared with angiosperms, bryophytes are seldom fed upon by insects, despite being commonly used for shelter. Bryophytes are assumed to be unpalatable, and three classes of mechanisms have been suggested as possible barriers to bryophagy: chemical defenses, low digestibility, and low nutrient content. However, very few studies have tested these hypotheses. The present study examines pre‐ and post‐ingestive defenses of mosses. The acceptability and quality of four species of moss –Bryum argenteum Hedw. (Bryales: Bryaceae), Climacium americanum Brid. (Leucodontales: Climaciaceae), Leucobryum glaucum (Hedw.) (Dicranales: Leucobryaceae), and Sphagnum warnstorfii Russ. (Sphagnales: Sphagnaceae) – were compared with two control diets using the generalist caterpillar, Trichoplusia ni Hübner (Lepidoptera: Noctuidae: Plusiinae). In no‐choice trials, caterpillars consumed much less of any of the mosses than lettuce or wheat germ. The only moss consumed in sufficient quantities to evaluate post‐ingestive responses was C. americanum. Digestibility, assimilation, and overall utilization efficiency of C. americanum did not differ from that of lettuce, although C. americanum and lettuce were both less digestible than artificial diet. Choice assays using leaf discs showed that ethanol extract of L. glaucum, the least consumed moss, was deterrent, implying that chemical defenses play a major role in deterring feeding on L. glaucum. This study suggested that pre‐ingestive mechanisms are more important than post‐ingestive mechanisms in discouraging herbivory on mosses, and offered evidence that mosses are not simply nutrient poor.     

Use of an exotic host plant shifts immunity,chemical defense,and viral burden in wild populations of a specialist insect herbivore

Defense against natural enemies constitutes an important driver of herbivore host range evolution in the wild. Populations of the Baltimore checkerspot butterfly, Euphydryas phaeton (Nymphalidae), have recently incorporated an exotic plant, Plantago lanceolata (Plantaginaceae), into their dietary range. To understand the tritrophic consequences of utilizing this exotic host plant, we examined immune performance, chemical defense, and interactions with a natural entomopathogen (Junonia coenia densovirus, Parvoviridae) across wild populations of this specialist herbivore. We measured three immune parameters, sequestration of defensive iridoid glycosides (IGs), and viral infection load in field‐collected caterpillars using either P. lanceolata or a native plant, Chelone glabra (Plantaginaceae). We found that larvae using the exotic plant exhibited reduced immunocompetence, compositional differences in IG sequestration, and higher in situ viral burdens compared to those using the native plant. On both host plants, high IG sequestration was associated with reduced hemocyte concentration in the larval hemolymph, providing the first evidence of incompatibility between sequestered chemical defenses and the immune response (i.e., the “vulnerable host” hypothesis) from a field‐based study. However, despite this negative relationship between IG sequestration and cellular immunity, caterpillars with greater sequestration harbored lower viral loads. While survival of virus‐infected individuals decreased with increasing viral burden, it ultimately did not differ between the exotic and native plants. These results provide evidence that: (1) phytochemical sequestration may contribute to defense against pathogens even when immunity is compromised and (2) herbivore persistence on exotic plant species may be facilitated by sequestration and its role in defense against natural enemies.     

Specificity of constitutive and induced resistance: pigment glands influence mites and caterpillars on cotton plants

Cotton plants contain suites of phytochemicals thought to be important in defense against herbivores, some of which are localized in pigment glands which contain gossypol and other terpenoid aldehydes. The simple genetic basis for the expression of these glands has led to the development of near-isogenic glanded and glandless genotypes. Glands may also be phenotypically induced by herbivory. We determined the consequences of constitutive and induced gland expression on two types of herbivores, spider mites (cell content feeders) and noctuid caterpillars (leaf chewers).Induction of glands was strongly dependent on the density of attackers. Spider mite herbivory on cotyledons (1) increased the density (but not total number) of glands on cotyledons linearly, (2) increased the density and total number of glands on the first true leaf linearly, and (3) affected the density and total number of glands on the second true leaf non-linearly, compared to controls. Neither constitutive nor induced expression of glands affected mite population growth. An equal reduction of mite population size on induced glanded and glandless plants (50%) relative to uninduced controls indicated that factors other than glands were associated with induced resistance to mites. Constitutive gland expression had a strong negative impact on caterpillar performance, reducing growth by 45%. Induced resistance to caterpillars was three times stronger in glanded genotypes than in glandless genotypes, indicating that factors associated with induced resistance to caterpillars are strongly associated with glands. Three cotton varieties were highly variable in their constitutive and induced resistance to mites and caterpillars.Thus, defense of cotton plants against herbivores can be roughly categorized as constitutive and inducible factors associated with terpenoid aldehyde containing pigment glands that are effective against caterpillars, and factors not associated with glands that are effective against mites.     

Lack of correlation between constitutive and induced resistance to a herbivore in crucifer plants: real or flawed by experimental methods?

The correlation between constitutive and induced resistance to herbivores in plants has long been of interest to evolutionary biologists, and various approaches to determining levels of resistance have been used in this field of research. In this study, we examined the relationship between constitutive and induced resistance to the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), in 11 closely related species of wild crucifers. We assessed the survival, development, and reproduction of the test insects and calculated their intrinsic rate of increase as an indicator of constitutive and induced resistance for the plants. We used larvae of P. xylostella and jasmonic acid as elicitors of the induced response. We failed to find a correlation between constitutive and induced resistance in these crucifer plants when the induction of resistance was initiated by either herbivory or jasmonic acid application. Analysis of the results suggests that the failure to detect a relationship between the two types of resistance could be caused by flaws in measuring constitutive resistance, which was apparently confounded with induced resistance. We discuss the difficulties and pitfalls in measuring constitutive resistance and ways to improve the methodology in investigating the relationships between constitutive and induced resistance in plants.     

Demographic models reveal the shape of density dependence for a specialist insect herbivore on variable host plants

1. It is widely accepted that density-dependent processes play an important role in most natural populations. However, persistent challenges in our understanding of density-dependent population dynamics include evaluating the shape of the relationship between density and demographic rates (linear, concave, convex), and identifying extrinsic factors that can mediate this relationship. 2. I studied the population dynamics of the cactus bug Narnia pallidicornis on host plants (Opuntia imbricata) that varied naturally in relative reproductive effort (RRE, the proportion of meristems allocated to reproduction), an important plant quality trait. I manipulated per-plant cactus bug densities, quantified subsequent dynamics, and fit stage-structured models to the experimental data to ask if and how density influences demographic parameters. 3. In the field experiment, I found that populations with variable starting densities quickly converged upon similar growth trajectories. In the model-fitting analyses, the data strongly supported a model that defined the juvenile cactus bug retention parameter (joint probability of surviving and not dispersing) as a nonlinear decreasing function of density. The estimated shape of this relationship shifted from concave to convex with increasing host-plant RRE. 4. The results demonstrate that host-plant traits are critical sources of variation in the strength and shape of density dependence in insects, and highlight the utility of integrated experimental-theoretical approaches for identifying processes underlying patterns of change in natural populations.     

The effect of direct and indirect defenses in two wild brassicaceous plant species on a specialist herbivore and its gregarious endoparasitoid

Most studies on plant defenses against insect herbivores investigate direct and indirect plant defenses independently. However, these defenses are not necessarily mutually exclusive. Plant metabolites can be transmitted through the food chain and can also affect the herbivore's natural enemies. A conflict may arise when a natural enemy is attracted to a plant that is suboptimal in terms of its own fitness. In addition, plant defenses are often studied in cultivated plant species in which artificial selection may have resulted in reduced resistance against insect herbivores. In this study, we investigated both direct and indirect plant defenses in two closely related wild brassicaceous plant species, Brassica nigra L. and Sinapis arvensis L. The herbivore Pieris brassicae L. (Lepidoptera: Pieridae), which is specialized on brassicaceous plant species, developed faster and attained higher pupal mass when reared on B. nigra than on S. arvensis. In contrast, Cotesia glomerata L. (Hymenoptera: Braconidae), which is a gregarious endoparasitoid of P. brassicae caterpillars, developed equally well on P. brassicae irrespective of the food plant on which its host had been reared. The feeding strategy of the parasitoid larvae, that is, selectively feeding on hemolymph and fat body, is likely to allow for a much wider host‐size range without affecting the size or development time of the emerging parasitoids. In flight chamber experiments, C. glomerata, which had an oviposition experience in a host that fed on Brussels sprout, exhibited significant preference for host‐damaged B. nigra over host‐damaged S. arvensis plants. Headspace analysis revealed quantitative and qualitative differences in volatile emissions between the two plant species. This parasitoid species may use a range of cues associated with the host and the host's food plant in order to recognize the different plant species on which the host can feed. These results show that there is no conflict between direct and indirect plant defenses for this plant–host–parasitoid complex.     

Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities

BACKGROUND: Carnivorous pitcher plants (CPPs) use cone-shaped leaves to trap animals for nutrient supply but are not able to kill all intruders of their traps. Numerous species, ranging from bacteria to vertrebrates, survive and propagate in the otherwise deadly traps. This paper reviews the literature on phytotelmata of CPPs. PITCHER: Fluid as a Habitat The volumes of pitchers range from 0·2 mL to 1·5 L. In Nepenthes and Cephalotus, the fluid is secreted by the trap; the other genera collect rain water. The fluid is usually acidic, rich in O(2) and contains digestive enzymes. In some taxa, toxins or detergents are found, or the fluid is extremely viscous. In Heliamphora or Sarracenia, the fluid differs little from pure water. INQUILINE: Diversity Pitcher inquilines comprise bacteria, protozoa, algae, fungi, rotifers, crustaceans, arachnids, insects and amphibia. The dominant groups are protists and Dipteran larvae. The various species of CPPs host different sets of inquilines. Sarracenia purpurea hosts up to 165 species of inquilines, followed by Nepenthes ampullaria with 59 species, compared with only three species from Brocchinia reducta. Reasons for these differences include size, the life span of the pitcher as well as its fluid. MUTUALISTIC: Activities Inquilines closely interact with their host. Some live as parasites, but the vast majority are mutualists. Beneficial activities include secretion of enzymes, feeding on the plant's prey and successive excretion of inorganic nutrients, mechanical break up of the prey, removal of excessive prey and assimilation of atmospheric N(2). CONCLUSIONS: There is strong evidence that CPPs influence their phytotelm. Two strategies can be distinguished: (1) Nepenthes and Cephalotus produce acidic, toxic or digestive fluids and host a limited diversity of inquilines. (2) Genera without efficient enzymes such as Sarracenia or Heliamphora host diverse organisms and depend to a large extent on their symbionts for prey utilization.     

Interspecific hybridization of plants and resistance to herbivores: hypotheses,genetics, and variable responses in a diverse herbivore community

We studied the morphology, molecular genetics, and hebivory of two species of willows (Salix sericea and S. eriocephala) and their interspecific hybrids to test four alternative hypotheses concerning the effects of hybridization on plant resistance. Individually marked plants were identified using morphological traits in the field and measurements of stipule and leaf pubescence were made and compared using Canonical Discriminant Function Analysis. DNA was extracted from the leaves of a sample of the marked plants and RAPD-PCR analysis was performed to establish the genetic status of parental and hybrid plants. RAPD band analysis generally verified the genetic status of parental plants. Hybrid plants were usually correctly identified in the field with a few exceptions. However, the hybrid plants were a heterogeneous group of plants made up of most plants that appear to be F₁s and a few plants that appear to be backcrosses to S. sericea. Morphological variables were useful for distinguishing S. sericea from S. eriocephala and hybrids, but were not as dependable in distinguishing between S. eriocephala and hybrids. We compared the densities of 11 herbivore species and the infection by a leaf rust pathogen (Melampsora sp.) on the leaves and stems of two parents and the hybrids in the field. We found support for the Additive hypothesis (3 species), the Dominance hypothesis (2 species) and the Hybrid Susceptibility hypothesis (7 species, 6 herbivores and the Melampsora rust). We found no evidence for the Hybrid Resistance hypothesis. Guild membership was not a good predictor of similar responses of species to hybrid versus parental plants. A Canonical Discriminant Function Analysis showed discrete separation of the taxa based on herbivore densities, illustrating different community structures on hybrid and parental plants. This study demonstrates the diversity of responses of phytophages in response to interspecific hybridization.     

The nocturnal larvae of a specialist folivore perform better on Chromolaena odorata leaves from a shaded environment

Increasing evidence suggests that individuals of the same plant species occurring in different microhabitats often show a degree of phenotypic and phytochemical variation. Consequently, insect herbivores associated with such plant species must deal with environment‐mediated changes or variability in the traits of their host plants. In this study, we examined the effects of habitat condition (shaded vs. full‐sun habitats) on plant traits and leaf characteristics of the invasive alien plant, Chromolaena odorata (L.) King & Robinson (Asteraceae). In addition, the performance was evaluated in two generations of a specialist folivore, Pareuchaetes insulata (Walker) (Lepidoptera: Erebidae: Arctiinae), on leaves obtained from both shaded and full‐sun habitats. The study was done in an area where the insect was introduced as a biological control agent. Leaves growing in shade were less tough, had higher water and nitrogen content, and lower total non‐structural carbohydrate, compared with leaves growing in full sun. Plants growing in shade had longer leaves and were taller, but above‐ground biomass was significantly reduced compared with plants growing in full sun. In both generations (parents and offspring), P. insulata developed faster and had larger pupal mass, increased growth rate, and higher fecundity when reared on shaded foliage compared with full‐sun foliage. Although immature survival and adult longevity did not differ between habitats, Maw's host suitability index indicated that shaded leaves were more suitable for the growth and reproduction of P. insulata. We suggest that the benefits obtained by P. insulata feeding on shaded foliage are associated with reduced toughness and enhanced nitrogen and water content of leaves. These results demonstrate that light‐mediated changes in plant traits and leaf characteristics can affect insect folivore performance.