Plant polyploidy and insect/plant interactions

We used flow cytometry and extensive geographic surveys of herbivore attack to test whether repeated evolution of autotetraploidy in the perennial herb Heuchera grossulariifolia Rydb. (Saxifragaceae) has created evolutionary barriers to attack by the specialist moth herbivore Greya politella (Prodoxidae). We found that the moth has colonized tetraploid as well as diploid populations, has colonized tetraploids of separate evolutionary origin, and, at least under some conditions, is more likely to attack tetraploids than diploids. Plant polyploidy therefore provides a potential route out of specialization as an evolutionary dead end in phytophagous insect taxa as well as a potentially important route to subsequent phylogenetic and geographic diversification of plant/insect interactions.     

Use of an exotic host plant affects mate choice in an insect herbivore

The colonization of exotic plants by herbivorous insects has provided opportunities for investigating causes and consequences of the evolution of niche breadth. The butterfly Lycaeides melissa utilizes exotic alfalfa, Medicago sativa, which is a relatively poor larval resource, and previous studies have found that caterpillars that consume M. sativa develop into smaller and less fecund adults. Here we investigate the effect of smaller female body size on male mate preference, a previously unexplored consequence of novel host use. Smaller females, which developed on the exotic host, were less likely to be visited by males. This result was confirmed with a second set of choice tests involving females reared on a single plant species, thus ruling out host-specific confounding factors. We suggest that an effect on mate choice be considered part of the complex suite of factors determining persistence of herbivorous insects following colonization of new habitats or resources.     

Response of an insect herbivore to host plants grown in carbon dioxide enriched atmospheres

Rising atmospheric carbon dioxide concentration is expected to increase plant productivity, but little evidence is available regarding effects on insect feeding or growth. Larvae of the soybean looper, a noctuid moth, were fed leaves of soybean plants grown under three carbon dioxide regimes (350, 500 and 650 l·l^-1). Larvae fed at increasingly higher rates on plants from elevated carbon dioxide atmospheres: 30% greater on leaves from the 650 l·l^-1 treatment than on leaves from the 350 l·l^-1 treatment. When variation in larval feeding was related to the leaf content of nitrogen and water, there was no significant remaining effect of carbon dioxide treatment. The principal effect on herbivores of increasing the carbon supply of leaves appeared to be reduction of leaf nutrient concentration. This study suggests that feeding by herbivores on the leaves of C₃ plants may increase as the level of atmospheric carbon dioxide rises.     

A recently acquired host plant provides an oligophagous insect herbivore with enemy-free space

Enemy-free space (EFS) is a potentially important factor affecting host plant use by phytophagous insects. Yet only a few field studies have demonstrated that natural enemy activity is the sole mechanism underlying use of novel host plants by herbivorous insects. This may be due to the fact that in earlier studies, both herbivores and natural enemies had the opportunity to adapt to the new host plant. Here we studied the possibility that EFS underlies the recently recorded increase in Phthorimaea operculella densities on tomato plants in a few areas within its geographical range. Through field experiments in Ethiopia, we show that all three conditions proposed by Berdegue et al. to demonstrate EFS are fulfilled. First, a significantly higher proportion of larvae survive on caged than on exposed potato plants, showing that natural enemies are an important mortality factor on the original host, potato. Second, larval survival was significantly higher on exposed tomato than potato plants, implying greater protection for the herbivore from its natural enemies on tomato than on potato plants. Thus tomato plants provide P. operculella with an EFS. Finally, larval survival was significantly higher on caged potato than on caged tomato plants at the preblossom stage, indicating that, in the absence of natural enemies, there is a fitness cost when larvae feed on the sub-optimal tomato plants. Fulfillment of this third condition points to the importance of natural enemy activity relative to that of other unidentified factors, such as food quality and competition. An intensive field survey provides further support for this conclusion.     

Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores

Benzoxazinoids are a class of indole-derived plant chemical defenses comprising compounds with a 2-hydroxy-2H-1,4-benzoxazin-3(4H)-one skeleton and their derivatives. These phytochemicals are widespread in grasses, including important cereal crops such as maize, wheat and rye, as well as a few dicot species, and display a wide range of antifeedant, insecticidal, antimicrobial, and allelopathic activities. Although their overall effects against insect herbivores are frequently reported, much less is known about how their modes of action specifically influence insect physiology. The present review summarizes the biological activities of benzoxazinoids on chewing, piercing-sucking, and root insect herbivores. We show how within-plant distribution modulates the exposure of different herbivore feeding guilds to these defenses, and how benzoxazinoids may act as toxins, feeding deterrents and digestibility-reducing compounds under different conditions. In addition, recent results on the metabolism of benzoxazinoids by insects and their consequences for plant-herbivore interactions are addressed, as well as directions for future research.     

Condition-dependent tolerance of monoterpenes in an insect herbivore

The ability of a herbivore to tolerate plant defensive chemicals may vary with the herbivore’s energetic state. We investigated the effect of body condition on the survivorship of individual mountain pine beetles, Dendroctonus ponderosae, exposed to host monoterpenes at concentrations comparable to constitutive and induced levels of defence using fumigant exposure. Body condition index was calculated as the residual mass after fitting the relationship between fresh weight and body size. Differences in survivorship among the four monoterpenes tested (α-pinene, myrcene, terpinolene and limonene) were small. Beetles with a higher body condition index survived high monoterpene concentrations better than those in poorer condition. There was no direct effect of sex, but positive effects of body size and fat content on survivorship favoured females, the sex that pioneers attacks on live trees. Higher body condition index corresponded to both higher fat content and fat-free body mass; the same conclusions about monoterpene identity and size-dependent or energy-dependent tolerance of high monoterpene concentrations held if fat or fat-free body mass were used in place of body condition index. This study highlights the need to consider insect body condition in understanding insect–plant interactions.     

A plant pathogen reduces the enemy-free space of an insect herbivore on a shared host plant

An important mechanism in stabilizing tightly linked host-parasitoid and prey-predator interactions is the presence of refuges that protect organisms from their natural enemies. However, the presence and quality of refuges can be strongly affected by the environment. We show that infection of the host plant Silene latifolia by its specialist fungal plant pathogen Microbotryum violaceum dramatically alters the enemy-free space of a herbivore, the specialist noctuid seed predator Hadena bicruris, on their shared host plant. The pathogen arrests the development of seed capsules that serve as refuges for the herbivore's offspring against the specialist parasitoid Microplitis tristis, a major source of mortality of H. bicruris in the field. Pathogen infection resulted both in lower host-plant food quality, causing reduced adult emergence, and in twofold higher rates of parasitism of the herbivore. We interpret the strong oviposition preference of H. bicruris for uninfected plants in the field as an adaptive response, positioning offspring on refuge-rich, high-quality hosts. To our knowledge, this is the first demonstration that plant-inhabiting micro-organisms can affect higher trophic interactions through alteration of host refuge quality. We speculate that such interference can potentially destabilize tightly linked multitrophic interactions.     

Scale-dependent mechanisms in the population dynamics of an insect herbivore

A multiscale approach has lead to significant advances in the understanding of species population dynamics. The scale-dependent nature of population processes has been particularly clearly illustrated for insect herbivores. However, one of the most well-studied insect herbivores, the galling sawfly Euura lasiolepis, has to date been examined almost exclusively at fine spatial scales. The preference-performance, plant vigour and larval survival hypotheses are well supported by this species. Here, we test these hypotheses at a spatial scale larger than that previously considered, i.e. across a landscape in northern Arizona represented by an altitudinal gradient encompassing a series of drainages. We also develop a qualitative model for understanding the population dynamics of E. lasiolepis based on patterns of survival and mortality found in this study and previous ones. Gall density was highly variable across the altitudinal gradient, not explained by host plant variables, and thus a poor surrogate fot population abundance. These findings for the first time fail to support the plant vigour and preference hierarchy hypotheses for E. lasiolepis. Dispersal limitation most likely explains the lack of support for these hypotheses at this scale. By contrast, sawfly survival, gall abortion, parasitism and larval mortality were well explained by host plant quality variables and altitude. The larval survival hypothesis was well supported and is thus comparatively scale-invariant. A qualitative model developed here highlighted the importance of both willow water status and disturbance in determining host plant quality, as well as an apparent trade off between shoot length and plant moisture status in determining vital rates across the altitudinal gradient. This study thus demonstrated for the first time the scale-dependent nature of mechanisms underlying the population dynamics E. lasiolepis, and identified the interaction between parasitism and altitude as a novel mechanism underlying spatial patterns in the survival and mortality patterns of this species.     

Effects of light availability on host plant chemistry and the consequences for behavior and growth of an insect herbivore

We examined how light availability influenced the defensive chemistry of tomato (Lycopersicon esculentum: Solanaceae). Tomato plants were grown either in full sunlight or under shade cloth rated at 73%. Leaves from plants grown in full sunlight were tougher, had higher concentrations of allelochemicals (chlorogenic acid, rutin and tomatine), and had less protein than leaves from plants grown in shade. We determined how these differences in host plant quality due to light availability affected the behavior and growth of a Solanaceae specialist, Manduca sexta. Both in the greenhouse and in the field, caterpillars on shade-grown plants grew heavier in a shorter amount of time than those on plants that had previously been grown in full sunlight. In contrast, the effects of previous light availability to plants on caterpillar behavior appeared to be minor.To further investigate how light availability to plants influenced herbivore growth, we examined the effects of leaf-powder diets made from tomato leaves of different ages (new, intermediate, or mature) grown in full sunlight or shade on caterpillar performance. Caterpillars fed diets made from plants grown in shade consumed less but grew faster than larvae fed diets made from tomato plants grown in full sunlight. Caterpillars fed diets made from new leaves grew larger in less time than caterpillars fed diets made from intermediate aged leaves. Caterpillars did not survive on the mature leaf powder diets. There were plant-light treatment by larval thermal regime interactions. For example, at 26:15 °C , plant-light treatment had no effect on stadium duration, but at 21:10 °C, stadium duration was prolonged with the full sunlight-new leaf diet compared with the shaded-new leaf diet. In a second diet experiment, we examined the interactive effects of protein and some tomato allelochemicals (rutin, chlorogenic acid and tomatine) on the performance of caterpillars. There were food quality by thermal regime interactions. For instance, at 26:15 °C , neither protein nor allelochemical concentration influenced stadium duration, whereas at 21:10 °C, stadium duration was prolonged with the low protein-high allelochemical diet, which simulated full sunlight leaves. In sum, light availability to plants affected defensive chemistry and protein concentration. The difference in food quality was great enough to influence the growth of a specialist insect herbivore, but the effects were temperature-dependent.     

Fungal endophytes of grasses and their effects on an insect herbivore

Summary The effects of endophytic fungi (Tribe Balansiae, Clavicipitaceae, Ascomycetes) of grasses on an insect herbivore were studied by feeding paired groups of larvae of the fall armyworm (Spodoptera frugiperda, Noctuidae, Lepidoptera) leaves from either infected or uninfected individuals. Perennial ryegrass infected by the Lolium endophyte, tall fescue infected by Epichloe typhina, dallisgrass infected by Myriogenospora atramentosa, Texas wintergrass infected by Atkinsonella hypoxylon, and sandbur infected by Balansia obtecta were utilized. The endophytes of ryegrass and fescue previously have been shown to be toxic to mammalian herbivores and to deter feeding of some insect herbivores. In this study we extend the antiherbivore properties of those endophytes to the fall armyworm and demonstrate that fungal endophytes in three other genera have similar antiherbivore properties. For most grasses, survival and weights of fall armyworm larvae fed infected leaves were significantly lower and larval duration was significantly longer compared to larvae fed uninfected leaves. Resistance to herbivores may provide a selective advantage to endophyte-infected grasses in natural populations.     

Plant virus and parasitoid interactions in a shared insect vector/host

Interactions between barley yellow dwarf luteovirus (BYDV) and the aphid parasitoid, Aphidius ervi Haliday (Hymenoptera: Aphidiidae), were investigated while sharing the vector/host, Sitobion avenae (F.) (Homoptera: Aphididae). Aphids, which were parasitized during their second larval stadium, had access to virus-infected plants before, immediately after, or several days after parasitoid attack. The larval development of A. ervi in S. avenae was significantly delayed when virus acquisition took place before or shortly after the parasitoid had hatched, but not when the parasitoid was at the second larval stage during virus acquisition. Similarly, the presence of BYDV led to a significantly higher aphid mortality when they acquired virus up to and including the time that A. ervi was at the first larval stage. Adult female parasitoids deposited fewer eggs in viruliferous aphids. Virus transmission was not reduced by parasitization, and in some experiments aphids which were subjected to parasitoid attack transmitted BYDV more efficiently than unattacked insects.     

Simultaneous effects of night-time temperature and an allelochemical on performance of an insect herbivore

One effect of global warming may be an increase in night-time temperatures with daytime temperatures remaining largely unchanged. We examined this potential effect of global warming on the performance of tobacco hornworm larvae, Manduca sexta (Sphingidae), by manipulating night-time temperature and dietary rutin levels simultaneously under a 12 light:12 dark photoregime. All four thermal regimes (26:14, 26:18, 26:22, and 26:26° C) had a daytime temperature of 26° C, with the night-time temperature increased from 14 to 26° C by increments of 4° C. Dietary rutin levels (0, 10 and 20 moles g^–1 fresh weight of diet) reflected those occurring naturally in the leaves of tomato, a preferred host plant of M. sexta. With low night-time temperatures (14 and 18° C), rutin had a negative linear effect on developmental rate, relative growth rate and relative consumption rate of the caterpillars. However, at a night-time temperature of 22° C, rutin had a negative non-linear effect. At a night-time temperature of 26° C, rutin had a negative linear impact but less so than at the other nightime temperatures. Likewise, the negative effect of rutin on molting duration was mitigated as night-time temperature increased. Final larval weight decreased linearly with increased dietary rutin concentrations. Total amount of food ingested was not affected by either rutin or thermal regime. As expected, the caterpillars developed faster under an alternating 26:14° C regime than a constant 20° C regime (the average temperature for the alternating regime), but the effect of rutin depended on the thermal regime. Switching daytime and night-time temperatures had no statistically significant effect on caterpillar performance. Overall, the effect of rutin on rates of larval performance was greater at some levels of warmer nights but damped at another level. These results indicate that the potential effect of warmer nights on insect performance is not a simple function of temperature because there can be interactions between night-time temperature and dietary allelochemicals.     

A fungal root symbiont modifies plant resistance to an insect herbivore

Vesicular-arbuscular mycorrhizal (VAM) fungi are common root-colonizing symbionts that affect nutrient uptake by plants and can alter plant susceptibility to herbivores. I conducted a factorial experiment to test the hypotheses that colonization by VAM fungi (1) improves soybean (Glycine max) tolerance to grazing by folivorous Mexican bean beetle (Epilachna varivestis), and (2) indirectly affects herbivores by increasing host resistance. Soybean seedlings were inoculated with the VAM fungus Glomus etunicatum or VAM-free filtrate and fertilized with high-[P] or low-[P] fertilizer. After plants had grown for 7 weeks first-instar beetle larvae were placed on bagged leaves. Growth of soybean was little affected by grazing larvae, and no effects of treatments on tolerance of soybeans to herbivores were evident. Colonization by VAM fungus doubled the size of phosphorus-stressed plants but these plants were still half the size of plants given adequate phosphorus. High-[P] fertilizer increased levels of phosphorus and soluble carbohydrates, and decreased levels of soluble proteins in leaves of grazed plants. Colonization of grazed plants by VAM fungus had no significant effect on plant soluble carbohydrates, but increased concentration of phosphorus and decreased levels of proteins in phosphorus-stressed plants to concentrations similar to those of plants given adequate phosphorus. Mexican bean beetle mass at pupation, pupation rate, and survival to eclosion were greatest for beetles reared on phosphorus-stressed, VAM-colonized plants, refuting the hypothesis that VAM colonization improves host plant resistance. VAM colonization indirectly affected performance of Mexician bean beetle larvae by improving growth and nutrition of the host plant. Received: 28 February 1997 / Accepted: 23 June 1997     

Effects of potassium levels over the range occurring in host plants on the growth of an insect herbivore (Manduca sexta)

Third instar tobacco hornworms (Manduca sexta L.: Sphingidae) on low dietary potassium had a lower relative growth rate than individuals on diets with potassium concentrations reflecting those in host-plants, due to decreased consumption rate, lower efficiencies of conversion of ingested and digested food (ECI and ECD), and a prolonged growth/feeding phase. Furthermore, these larvae, when placed on a diet with a moderate potassium concentration through the fourth stadium, ended up being smaller due to lower ECI and less biomass gained, and had a prolonged growth phase, which suggest an irreversible cost of the previous low potassium diet. Third instar hornworms on high potassium diets had lower ECI and ECD, and they had a prolonged growth phase. These individuals, when placed on a moderate potassium diet in the fourth stadium, gained less biomass, than those previously offered hostplant-like-potassium diets. Body potassium concentrations (% dw) at the end of the third stadium were similar among treatment groups. With increasing potassium concentrations in the diet, utilization efficiencies of potassium decreased and potassium concentrations in the frass increased. Correspondingly, water content (% fw) of the newly-molted fourth instar larvae declined with increasing potassium, indicating a passive loss of water during potassium excretion. Low and high dietary potassium reduced survivorship of third instar larvae; fourth instar caterpillars previously fed the low potassium diet also had poor survivorship. We conclude that, within the normal range of potassium concentrations in the hostplants, caterpillar performance is largely unaffected by potassium concentration, but that potassium-poor and potassium-rich diets, such as those hornworms may sometimes experience, can reduce growth and survivorship.     

Consequences of host plant chemical and physical variability to an associated herbivore

The effects of watering and fertilizer treatments on the vigor and biochemistry of the willow,Salix lasiolepis, and subsequent colonization and survivorship of its gallforming herbivore,Euura lasiolepsis, were investigated in two field experiments. Some plants received low (LW), intermediate (MW) or high (HW) levels of water as treatments, while others received no (OF), low (LF) or high (HF) fertilizer levels. In the watering experiment, plant protein concentrations decreased, while growth rate and number of galls per plant increased with increased water treatments. Plant growth proved to be the best correlate of sawfly attack. Sawfly survivorship increased slightly with greater watering, and phenol concentrations showed no pattern among treatments. In the fertilization experiment, leaf protein increased with fertilization, although shoot length, number of galls and survivorship ofE. lasiolepis survivorship were greatest in intermediate treatment plants. In both experiments, plant growth, rather than protein or phenol levels, was the best predictor of sawfly attack and survivorship. In a natural experiment with galls on wild plants, galled tissue had significantly greater protein concentrations and lower phenol concentrations than did ungalled tissue. We suggest that gallformers modify host plant biochemistry within willow galls, which may explain why the chemical parameters of ambient plant quality we tested were less predictive than plant growth.     

Plant-mediated vulnerability of an insect herbivore to Bacillus thuringiensis in a plant-herbivore-pathogen system

Laboratory studies were performed to explore the effects of host-plant quality on the vulnerability of Plutella xylostella to Bacillus thuringiensis. P. xylostella were kept on different host plants, including Brassica pekinensis (Chinese cabbage) cv. Hero, Brassica oleracea var. botrytis (cauliflower) cv. Royal, and B. oleracea var. capitata (common cabbage) cv. Globe Master (white cabbage) and cv. Red Dynasty (red cabbage) for at least two generations. These host plants are considered as the high (Chinese cabbage), intermediate (cauliflower and white cabbage) and low-quality (red cabbage) hosts for P. xylostella. The vulnerability of the pest larvae was then tested using two formulation of B. thuringiensis var. kurstaki, including Biolarv^® and Biolep^®. The results demonstrated that the susceptibility of P. xylostella to B. thuringiensis was influenced by host-plant quality. Indeed, B. thuringiensis acted better on the pest fed on the low-quality host plant compared with that on the high-quality host plant. The interaction between the pathogen and plant quality/resistance resulted in more mortality of the pest larvae, implying a synergistic effect. From a pest management viewpoint, these findings may be promising for the integration of the pathogen and the low-quality/partially resistant host plants against P. xylostella in field studies.     

Growth and development of a generalist insect herbivore, Operophtera brumata, on original and alternative host plants

A generalist feeding strategy is common among eruptive insect herbivores but the ultimate reasons for a generalist strategy are not clear. Although generalist insect herbivores are able to complete their life cycle on several species of host plants, there is wide variation in the performance of individuals grown on different hosts. We examined whether different populations of Operophtera brumata are adapted to use the host species which is locally most abundant, and how the host plant affects growth and development of the insect. We reared two allopatric populations (eastern Finland, Prunus padus; south-west Finland, Quercus robur) on four species of host plants (Pr. padus, Populus tremula, Q. robur, Salix phylicifolia) from neonate larvae to the adult stage and measured the growth and development of individuals and the timing of adult hatching. The performance of both populations was best on Pr. padus, and the south-western population, originally on Q. robur, was well adapted to this host. The host affected the growth of females more than that of males. The host plant had an unexpected effect on hatching times of the adults. Individuals grown on the original host hatched in normal synchrony, i.e. males 6–7 days before females; but on alternative hosts this synchrony was disturbed. As is common in eruptive, capital-breeding generalist moths where female fecundity is linked to weight, host quality is critical for the flightless females of O. brumata. We suggest that in a heterogeneous environment the disturbing effect of alternative host plants on adult emergence may decrease the population density and growth rate compared to the potential maximum in a homogeneous environment. Received: 8 July 1999 / Accepted: 29 October 1999