Warren G. Abrahamson

Effects of Resource Availability on Tolerance of Herbivory: A Review and Assessment of Three Opposing Models

Although it is widely acknowledged that a plant’s tolerance of herbivore damage depends on resource availability in the plant’s environment, there is no consensus on whether higher resource levels lead to greater or to lower tolerance. The prevailing model, the compensatory continuum hypothesis (CCH), predicts that tolerance of herbivory should be greater in high‐resource or low‐competition conditions. The main rival hypothesis, the growth rate model (GRM), makes the opposite prediction: tolerance of herbivory should be greater in more stressful conditions. The tolerance predictions of a recently introduced model, the limiting resource model (LRM), are more flexible and depend on the type of resource and herbivore under consideration. We reviewed 48 studies (from 40 published articles) of plant tolerance of leaf damage in conditions differing in levels of light, inorganic nutrients, water stress, or competition. The results of 31%, 48%, and 95% of the studies were consistent with the predictions of the CCH, GRM, and LRM, respectively. Thus, by considering which resource is primarily affected by herbivory and which resource is limiting a plant’s fitness, the LRM offers a substantial advance in predicting how tolerance will be affected by environmental differences in resource availability.

Growth Form and Reproductive Effort in Goldenrods (Solidago, Compositae)

Based on Gadgil and Solbrigs (1972) ideas concerning the distribution of resources between the reproductive and vegetative tissues, it is predicted that the ratio of reproductive biomass/total biomass (reproductive effort) will decline with the increasing successional maturity of the community. This prediction was confirmed in field studies utilizing four species of goldenrods. The distribution of resources among the various vegetative tissues should depend on the nature of the limiting factor and the growth form of the dominant plants competing for this limiting factor. Thus, it is predicted that the ratio of stem biomass/total biomass will decline and that of leaf biomass/total biomass will increase for light-limited plant populations as the growth form of competitors changes from being one of the same stature (herbs with herbs) to being one of greater stature (herbs with trees). These two predictions are likewise confirmed in goldenrods. The problem of how these differences in the distribution of resources among tissues are maintained in closely growing populations of a single species was examined. It was found that populations of a given species bloomed at different times, thus reducing the gene flow between these populations. This indicates some degree of isolation which could allow for the maintenance of ecotypic variation.

REPRODUCTIVE STRATEGIES IN DEWBERRIES

Two predictions are made. (1) In a stable, predictable habitat when popula- tion density is low and clonal expansion is possible, vegetative reproduction should be favored. When population density is high because of crowding, plants should put a greater proportion of their resources into seed reproduction, resulting in dispersal. (2) In a temporally unstable habitat, this reproductive density response will not exist. Field studies utilizing Rubus hispidus and Rubus trivialis confirm the first prediction but not the second. In addition, cattle grazing and precipitation had a marked effect on mode of reproduction.

The Effects of Stem Gall Insects on Life History Patterns in Solidago Canadensis

Populations of goldenrods (Solidago canadensis) were sampled to determine the effects of three stem gall insects, Gnorimoshema gallaesolidaginis (Gelechiidae), Eurosta solidaginis (Tephritidae), and Rhopalomyia solidaginis (Cecidomyiidae) on resource allocation patterns in the plants. Gall infestations were as high as 38.5% and the dominant gall insect differed from site to site. The gall insects caused significant and highly specific effects on the plants. Each of the three gall types increased stem production, decreased current rhizome production, and lowered seed reproductive allocation as measured both by inflorescence production and propagule production. Vegetative reproductive allocation (the proportion of biomass allocated to new rhizome) was unaffected. With the exception of ball gall—beaing ramets, the number of new rhizomes produced was unaffected by the presence of galls. Growth of the elliptical gall significantly reduced shoot height and significantly increased lateral branching and propagule weight. Formation of the ball significantly reduced propagule weight and the number of new rhizomes produced. Thus gall insect—plant interactions may play an important role in the evolution of plant life history patterns in certain taxa. Future studies are needed to determine the effects of galls on entire clones (genets) and the implications of gall infestation on future growth, survivorship, and reproduction.

EVOLUTION OF HOST-PLANT MANIPULATION BY GALL MAKERS: ECOLOGICAL AND GENETIC FACTORS IN THE SOLIDAGO-EUROSTA SYSTEM

Plant galls are growth deformities that feed and house the larvae of specialized insect species and other organisms (nematodes, bacteria, fungi, etc.). The benefits derived by the insect from its interaction with the host plant suggest that gall-making ability is an adaptive trait of the insect subject to modification by natural selection. Our findings, that variation in gall phenotype influences insect fitness and that gall phenotypic variation is affected by genetic variation in the insect population, support this interpretation. Our study of the goldenrod gall fly, Eurosta solidaginis, shows that gall size variation results from genetic variation among flies despite selective pressures by natural enemies. Eurosta larvae that produce small galls are vulnerable to the attack of parasitoid wasps, whereas those producing large galls are more prone to attack by avian predators. In this study population, parasitoid attack was more intense; hence, a net upward selective pressure was exerted. Quantitative-genetic methods were used in a greenhouse experiment to evaluate the contribution of insect genetic variance to phenotypic variation in gall size. Significant differences in gall diameter were found among full-sib families of gall makers. Gall dimensions were genetically correlated with one another at most developmental stages. Observations of galls growing on goldenrod clones in both the field and the greenhouse suggest that plant genotype also influences gall phenotype, and thus affects gall-maker vulnerability to natural enemies.

The role of natural-enemy escape in a gallmaker host-plant shift

The successful colonization of novel host-plant species by herbivorous insects may be facilitated by a reduction in natural-enemy attack on insect populations associated with the novel (derived) host plant. This is particularly true if natural enemies use host-plant or habitat cues in searching for their herbivore prey. In order to test whether the acquisition of enemy-free space could have influenced the host shift in the goldenrod ball gallmaker, Eurosta solidaginis, we estimated levels of natural-enemy attack in 25 host-race populations associated with Solidago altissima and S. gigantea (Compositae) spanning the zone of sympatry between S. altissima and S. gigantea host races in New England. Mortality due to attack by the parasitoid wasp Eurytoma obtusiventris was significantly higher for the ancestral than for the derived host race (30.5% versus 0.4%) across the transect, which is consistent with the enemy escape hypothesis. Contrary to this hypothesis, mordellid beetles caused significantly higher mortality on the derived than ancestral host race (17.1% versus 2.6%). Mortality by a second parasitoid wasp and birds showed no significant differences between the two host races. Overall, the derived host race had significantly higher survivorship across the transect (36.6% versus 20.8%). An analysis of survivorship and parasitoid mortality levels from sympatric sites in this study and previous studies showed a highly significant correlation between the levels of Eurytoma obtusiventris attack and the survivorship advantage of the derived host race. Observations of this parasitoids searching behavior confirmed that it preferentially searches the ancestral host for fly larvae. Current patterns of host-race mortality and naturalenemy behavior and abundance are consistent with the facilitation of the host shift by escape from a specialist parasitoid.

POTENTIAL SELECTIVE PRESSURES BY PARASITOIDS ON A PLANT-HERBIVORE INTERACTION'

The potential role of the third trophic level in the evolution of plant-herbivore rela- tionships was examined in the case of the goldenrod Solidago altissima, and the fly Eurosta solidaginis, which forms a round stem gall. Previous observation had shown that galls attacked by parasites are significantly smaller than those in which the gall maker survives. Two different mechanisms could cause such a pattern: parasite attack could occur before galls reach full size and the attacks could cause early cessation of growth, or attack could occur after galls reach their mature size, but with inherently small galls being more prone to attack. In the first instance, parasite attack would diminish the cost of the gall to the plant, and thus favor plant genotypes that facilitate parasites. In the second instance, parasites would exert selection pressure on the gall maker to induce larger galls. Monitoring of marked plants in the field, and field experiments in which parasites were excluded from gall-bearing plants except during controlled periods, showed that parasite attack does not stop gall growth. The parasitoid wasp Eurytoma gigantea is limited to attacking small galls because of the limited reach of its ovipositor. This created a selection intensity of 0.50, favoring Eurosta that induce larger galls. Evolutionary response to selection could be realized directly through change in the gall makers stimulus ability, or less directly through phenological changes. Plant reactivity to the gall maker declined with plant age, so that late-starting galls were more vulnerable to parasite attack.

Gall insects can avoid and alter indirect plant defenses

Parasitic species can dramatically alter host traits. Some of these parasite-induced changes can be considered adaptive manipulations that benefit the parasites. Gall-inducing insects are parasites well known for their ability to alter host-plant morphology and physiology, including the distribution of plant defensive compounds. Here it was investigated whether gall-inducing species alter indirect plant defenses, involving the release of volatile compounds that are attractive to foraging natural enemies. Using field and factorial laboratory experiments, volatile production by goldenrod (Solidago altissima) plants was examined in response to attack by two gall-inducing species, the tephritid fly Eurosta solidaginis and the gelechiid moth Gnorimoschema gallaesolidaginis, as well as the meadow spittlebug, Philaenus spumarius, and the generalist caterpillar Heliothis virescens. Heliothis virescens elicited strong indirect defensive responses from S. altissima, but the gall-inducing species and spittlebugs did not. More significantly, infestation by E. solidaginis appeared to suppress volatile responses to subsequent attack by the generalist caterpillar. The extensive control that E. solidaginis apparently exerts over host-plant defense responses may reduce the predation risk for the gall inducer and the subsequent herbivore, and could influence community-level dynamics, including the distribution of herbivorous insect species associated with S. altissima parasitized by E. solidaginis.

Goldenrod Ball Gall Effects on Solidago altissima: 14C Translocation and Growth

The purpose of this investigation was to determine whether the effects of the goldenrod ball gall on carbon translocation and growth in ramets of Solidago altissima can account for changes in biomass allocation and total biomass observed in galled ramets. To do this, individual leaves of S. altissima were labeled with carbon—14 introduced as CO2. The 14C was introduced into ramets that had ball galls caused by the fly Eurosta solidaginis and into ungalled control ramets; gall size (large vs. small) and point of introduction of the label (above vs. below the gall) were experimental factors. After 5 d the ramets were harvested and their component organs were assayed for 14C using liquid scintillation. In addition, a field cohort of 359 galled and ungalled was followed during the period of gall growth to determine the effect of the gal on stem height growth. Gall size and labeling position had no effect on the percent of 14C translocated out of the labeled leaf but did affect the distribution of translocated 14C. Translocation to underground organs was reduced when the label was introduced above the gall, the reduction being related to gall size. Large galls reduced translocation to the apical bud when the label was introduced below the gall, but small galls did not. Translocation to underground organs was not affected by the gall when the label was introduced below the gall and translocation to the apical bud was not affected by the gall when the label was introduced above the gall; these results indicate that the goldenrod ball gall is a nonmobilizing gall. The presence of a gall did not significantly affect final stem height but did slow the growth of ramets during the period of most rapid gall growth. The observed effects of the gall probably explain changes in resource allocation shown by other studies but do not account for the overall decrease in biomass of galled ramets.

Host Genotype Choice by the Ball Gallmaker Eurosta Solidaginis (Diptera: Tephritidae)

We examined Eurosta solidaginis host choice among 38 naturally occurring clones of tall goldenrod, Solidago altissima. Significant variation was found in the per- centages of (1) ramets ovipunctured, (2) punctured ramets with eggs, (3) ramets galled, and (4) punctured ramets that formed galls. These findings indicate that all genotypes of S. altissima are not equally suitable (capable of supporting larval development) and/or ac- ceptable (having the proper cues to stimulate oviposition). The two most resistant and two of the most susceptible of 38 clones were monitored for ovipuncturing the following season. A total of 244 apical buds on ramets were dissected at intervals of 1, 2, and 3 wk after oviposition. Significantly more larval mortality occurred in the meristems of resistant clones than in the meristems of susceptible clones. Further, 73% of the dead Eurosta larvae were surrounded by necrotic plant tissue, apparently due to a hypersensitive response by the plant to the gallmakers stimulus. Finally, a common garden experiment using replicates of 30 clones of known resistance showed that susceptible clones were growing faster at the time of oviposition.