Nutrition as a facilitator of host‐race formation: the shift of a stem‐boring beetle to a gall host

1. The importance of host‐race formation to herbivorous insect diversity depends on the likelihood that successful populations can be established on a new plant host. A previously unexplored ecological aid to success on a novel host is better nutritional quality. The role of nutrition was examined in the shift of the stem‐boring beetle Mordellistena convicta to fly‐induced galls on goldenrod and the establishment there of a genetically distinct gall host race. 2. First, larvae of the host race inhabiting stems of Solidago gigantea were transplanted into stems and galls of greenhouse‐grown S. gigantea plants. At the end of larval development, the mean mass of larvae transplanted to galls was significantly greater than the mass of larvae transplanted to stems, indicating a likely nutritional benefit during the shift. This advantage was slightly but significantly diminished when the gall‐inducing fly feeding at the centre of the gall died early in the season. Additionally, there was a suggestion of a trade‐off in the increased mortality of smaller beetle larvae transplanted into galls. 3. In a companion experiment, S. gigantea gall‐race beetle larvae were likewise transplanted to S. gigantea stems and galls. Besides the expected greater mass in galls, the larvae also exhibited adaptations to the gall nutritional environment: larger inherent size, altered tunnelling behaviour, and no diminution of mass pursuant to gall‐inducer mortality. 4. In a third line of inquiry, chemical analyses of field‐collected S. gigantea plants revealed higher levels of mineral elements important to insect nutrition in galls as compared with stems.     

The distribution of risk and density-dependent mortality in the galls of Eurosta solidaginis, the goldenrod gall fly

ABSTRACT.

• 1 This paper explores the net effect of a suite of mortality factors on a sedentary prey, the larvae of the goldenrod gall fly, Eurosta solidaginis Fitch (Diptera: Tephritidae).
• 2 Mortality is caused by unknown factors early in larval development, two species of parasitoid wasp (Hymenoptera: Eurytomidae), an inquiline beetle larva (Coleoptera: Mordellidae), and during the winter months downy woodpeckers Picoides pubescens (L.).
• 3 Distribution of mortality among galls relative to prey (gall) distribution was measured and discussed with respect to the distribution of relative risk of predation.
• 4 Galls are by and large contagiously distributed among quadrats, and mortality is distributed in a comparable pattern to that of galls.
• 5 The pattern of mortality on Eurosta larvae is neither density-dependent nor aggregated independently of gall distribution. Persistence in the system is probably a result of a combination of other factors such as adult mortality and early larval death which may have intergenerational density-dependent effects, and the linkage of locally unstable sub-populations via migration.

     

Temperature acclimation and seasonal responses by enzymes in cold-hardy gall insects

Changes in the activity of over 20 enzymes of intermediary metabolism in 15°C or ?4°C acclimated goldenrod gall moth (Epiblema scudderiana) and gall fly (Eurosta solidaginis) larvae were measured. Increased activities of glyco-genolytic and hexose monophosphate shunt enzymes in cold-acclimated Epiblema scudderiana suggest a role for coarse control in the conversion of glycogen reserves into glycerol cryoprotectant synthesis. In Eurosta solidaginis, high glycogen phosphorylase activity with decreased activities of glycolytic enzymes may account in part for the temperature-dependent switch from glycerol to sorbitol synthesis in these larvae upon cold acclimation. Isoelectric focusing analyses of five enzymes in overwintering Epiblema scudderiana revealed transient mid-winter changes in the isoelectric points of phosphofructokinase and pyruvate kinase, suggesting seasonal changes in the phosphorylation state of these enzymes. A distinct developmental pattern of aldolase isozymes suggests a role for a new isozyme during overwintering or upon spring emergence. Regulation of metabolism by changes in enzyme activities is indicated for both larvae. © 1995 Wiley-Liss, Inc.     

Variation in selection pressures on the goldenrod gall fly and the competitive interactions of its natural enemies

Summary Larvae of the tephritid fly Eurosta solidaginis induce ball-shaped galls on the stem of tall goldenrod, Solidago altissima. Survival probability depends on gall size; in small galls the larva is vulnerable to parasitoid oviposition, whereas larvae in large galls are more frequently eaten by avian predators. Fly populations from 20 natural old fields in central Pennsylvania were monitored in 1983 and 1984 to examine the distribution of the selection intensity imposed by natural enemies, the parasitoids Eurytoma gigantea and E. obtusiventris, the inquiline Mordellistena unicolor, and the predatory birds Dendrocopus pubescens and Parus atricapillus. Mordellistena and E. obtusiventris are able to attack galls of all diameters while E. gigantea and the predatory birds preferentially assaulted small and large diameter galls, respectively. Eurosta in intermediate sized galls had the highest survivorship, hence selection had a stabilizing component. However, parasitoid attack was more frequent than bird attack, and the two did not exactly balance, thus there was also a directional component. The mean directional selection intensity on gall size was 0.21 standard deviations of the mean, indicating that larger gall size was favored. Interactions among the insect members of the Eurosta natural enemy guild are complex and frequent.     

Evidence for a novel cryoprotective protein from freeze-tolerant larvae of the goldenrod gall fly Eurosta solidaginis

Third-instar larvae of the goldenrod gall fly Eurosta solidaginis (Diptera: Tephritidae) from populations in northern North America transition from freeze-susceptible to freeze-tolerant just prior to the onset of winter. While studies have documented the accumulation of carbohydrate cryoprotectants during this transition, protein cryoprotectants common to other freeze-tolerant species have not been reported in the gall fly. Using larvae collected from a population in Madison County, NY, which changes from freeze-susceptible to freeze-tolerant in early October, we assayed for the presence of factors that could preserve the catalytic activity of the cold-labile enzyme, rabbit muscle lactate dehydrogenase. Freezing this enzyme with a heat-stable, hydrophilic fraction derived from homogenates of both freeze-tolerant larvae and those in the process of becoming freeze-tolerant preserved between 70% and 80% of this enzyme's activity. Neither a comparable solution of bovine serum albumin nor the naturally-occurring carbohydrates (glycerol, sorbitol, or trehalose) conferred this level of cryoprotection. The putative cryoprotective protein from gall fly larvae did not bind to a weak anion exchanger, implying that its character may be cationic.     

Effects of manipulation of plant carbon nutrient balance on tall goldenrod resistance to a gallmaking herbivore

Summary Ramets from six Solidago altissima clones of known resistance to the stem gallmaker Eurosta solidaginis were grown with and without supplemental nutrients. In a greenhouse experiment, mated female Eurosta were allowed to oviposit in ramets that were subsequently grown through flowering and then harvested to determine biomass allocation. Supplemental nutrients increased plant biomass but did not affect resistance to this gallmaking herbivore. This result does not conform to the plant carbon/nutrient balance hypothesis which predicts that enhanced mineral nutrition will indirectly cause a reduction in carbon-based defensive chemistry. Our results indicate a strong genetic basis to ball gallmaker resistance since modification of host phenotype did not influence susceptibility. We suggest that evaluating the degree of genotypic or environmental control of plant resistance will be especially helpful in clarifying the patterns of defensive chemical responses.     

The effects of temperature and season on the O2 consumption of third-instar larvae of the goldenrod gall fly (Eurosta solidaginis)

Abstract. Third-instar larvae of the goldenrod gall fly ( Eurosta solidaginis Fitch) live inside ball galls on goldenrod plants from summer to the following spring.Because galls are highly exposed to the weather, larvae experience substantial variations in body temperature.This study documents the oxygen consumption of gall fly larvae with regard to the effects of ambient temperature, seasonal conditioning, and prior exposure to subzero temperature.The body mass of larvae doubles between the late summer and the autumn; it subsequently undergoes a modest decline by early winter.The O₂, consumption of field-acclimatized larvae increases with ambient temperature, especially between 0 and 10°C (Q₁₀= 2.6-3.4).The thermal sensitivity of metabolism declines at higher ambient temperatures, most notably during the autumn/early winter.After exposure to 15°C for 1 week, autumn and early winter larvae maintain much lower rates of O₂ consumption than do late summer specimens.Prior exposure to -5°C for 24 h did not influence the O₂ consumption of larvae.Low thermal sensitivity of O₂ consumption, especially at higher ambient temperatures, is an energy-sparing mechanism during seasonal inactivity.Indeed, the persistence of this metabolic pattern in larvae exposed to 15°C suggests that they have entered a state of diapause.     

The role of phenolics in goldenrod ball gall resistance and formation

Some genotypes of Solidago altissima have been shown to exhibit a hypersensitive response to the tephritid ball gallmaker Eurosta solidaginis. When the gallmaker attempts to stimulate gall formation in these genotypes, necrotic tissue surrounds the larva and apparently causes larval death [Anderson, S. S., et al. (1989) Ecology 70, 1048]. Other genotypes have varying degrees of resistance or susceptibility [McCrea, K. D. and Abrahamson, W. G. (1987) Ecology 68, 822]. Studies of other host plants have shown that phenolic compounds can play an important role in this defensive reaction. To determine the role of phenolics in the resistance of S. altissima to ball gallmakers, weekly tissue samples were collected from two resistant and two susceptible clones, both with and without Eurosta attack. These samples were analysed for total phenolics using the Folin-Ciocalteau procedure. Phenolic content increased over time in all clones. In unattacked ramets, phenolic levels were higher in susceptible clones than in resistant clones. No evidence of an increase in phenolics was seen with a hypersensitive response, but a significantly higher concentration was found in plants that had initiated normal gall development. A second study of rapidly growing galls in three additional susceptible clones confirmed this increase in phenolics, demontrated that the higher phenolic concentrations were restricted to gall tissue, and showed that phenolic levels increase as much as five-fold in galls near their peak growth period. Increases in total phenolic levels were clearly not responsible for the hypersensitive reaction for resistance, but phenols could potentially play a role in gall formation by influencing the hormonal control of growth and/or in protection of the gallmaker from its natural enemies.     

The influence of host plant variation and intraspecific competition on oviposition preference and offspring performance in the host races of Eurosta solidaginis

1. A series of experiments was conducted to measure the impact of plant genotype, plant growth rate, and intraspecific competition on the oviposition preference and offspring performance of the host races of Eurosta solidaginis (Diptera: Tephritidae), a fly that forms galls on Solidago altissima and Solidago gigantea (Asteraceae). Previous research has shown that both host races prefer to oviposit on their own host plant where survival is much higher than on the alternate host plant. In this study, neither host race showed any relationship between oviposition preference and offspring performance in choosing among plants of their natal host species. 2. The larval survival of both host races differed among plant genotypes when each host race oviposited on its natal host species. In one experiment, altissima host race females showed a preference among plant genotypes that was not correlated with offspring performance on those genotypes. In all other experiments, neither the altissima nor gigantea host race demonstrated a preference for specific host plant genotypes. 3. Eurosta solidaginis had a preference for ovipositing on rapidly growing ramets in all experiments, however larval survival was not correlated with ramet growth rate at the time of oviposition. 4. Eurosta solidaginis suffered high mortality from intraspecific competition in the early larval stage. There was little evidence, however, that females avoided ovipositing on ramets that had been attacked previously. This led to an aggregated distribution of eggs among ramets and strong intraspecific competition. 5. There was no interaction among plant genotype, plant growth rate, or intraspecific competition in determining oviposition preference or offspring performance.