What kills the virtually immortal palms of the Florida scrub?

PREMISE: Life span varies greatly across plants, with some species being capable of extreme longevity. Yet even long-lived individuals are susceptible to climatic events, fire, and other challenges. We examined rare mortality events and their causes in two long-lived palmettos over four decades. METHODS: We monitored the survival of the clonal Serenoa repens and non-clonal, Florida-endemic Sabal etonia from 1981 to 2022 in four habitats along an elevational gradient within the globally imperiled Florida scrub ecosystem. We considered several challenges to palmetto survival, including extreme fires, shading due to lack of fire, droughts, periods of high precipitation, and possible pathogens. RESULTS: Survival of palmettos was remarkably high, and mortality was infrequent (Serenoa: cumulative, 5.7%; annualized, 0%-0.68%; Sabal: cumulative, 3.5%; annualized, 0%-0.43%). Mortality was highest in higher-elevation habitats with greater soil drainage, and smaller palmettos were more likely to die. When subjected to extreme fire, Serenoa suffered greater mortality than Sabal. Mortality in long-unburned habitats with increased shading rivaled that which occurred with extreme fire. There was no evidence of mortality due to lethal bronzing palm disease. CONCLUSIONS: Both palmettos had exceptionally low mortality rates, which, coupled with earlier work showing slow rates of transition from seedling to adult and remarkable adult longevity, suggest notably low rates of population turnover. Observed mortality in long-unburned habitats suggests the importance of fire-management planning with prescription burning. Lengthy age to reproduction and/or dependency on clonal propagation limits migration or genetic adaptation to altered conditions caused by climate change.

New species of Nearctic oak gall wasps (Hymenoptera: Cynipidae, Cynipini).

Twenty nine new species of cynipid oak gall wasps from the Nearctic region (America north of Mexico) are described: Andricus archboldi Melika Abrahamson, sp. nov., A. catalinensis Melika, Nicholls Stone, sp. nov., A. chapmanii Melika Abrahamson, sp. nov., A. chiricahuensis Melika, Nicholls Stone, sp. nov., A. coconinoensis Melika, Nicholls Stone, sp. nov., A. columbiensis Melika, Nicholls Stone, sp. nov., A. cooki Melika, Nicholls Stone, sp. nov., A. fitzpatricki Melika Abrahamson, sp. nov., A. highlandensis Melika, Nicholls Stone, sp. nov., A. mellificus Nicholls, Stone Melika, sp. nov., A. menkei Melika Abrahamson, sp. nov., A. mogollonensis Melika, Nicholls Stone, sp. nov., A. nichollsi Melika Stone, sp. nov., A. schickae Nicholls, Melika Stone, sp. nov., A. torreyaensis Melika Abrahamson, sp. nov., A. williami Melika, Nicholls Stone, sp. nov., Antron lovellae Melika, Nicholls Stone, sp. nov., A.tomkursari Melika, Nicholls Stone, sp. nov., Dryocosmus archboldi Melika Abrahamson, sp. nov., Loxaulus virginianae Melika Buss, sp. nov., Neuroterus alexandrae Nicholls Melika, sp. nov., N. aliceae Melika, Nicholls Stone, sp. nov., N. bussae Melika Nicholls, sp. nov., N. oblongifoliae Nicholls, Stone Melika, sp. nov., N. quaili Melika, Nicholls Stone, sp. nov., N. rosieae Melika, Nicholls Stone, sp. nov., N. stonei Melika Nicholls, sp. nov., Zapatella abrahamsoni Melika, sp. nov., Z. brooksvillei Melika Abrahamson, sp. nov.. Alternate asexual and sexual generations are described for four species, Andricus archboldi Melika Abrahamson, sp. nov., A. fitzpatricki Melika Abrahamson, sp. nov., A. schickae Nicholls, Melika Stone, sp. nov., Neuroterus aliceae Melika, Nicholls Stone, sp. nov.. Descriptions, diagnoses, plus information on biology and host associations are given for all new species. All taxa are supported by morphological data; matching of generations is established using DNA sequence data. We also demonstrate that Neuroterus niger var. alimas Kinsey should be considered as a nomen dubium.

Constraints on the evolution of resistance to gall flies in Solidago altissima: resistance sometimes costs more than it is worth.

Plant populations frequently maintain submaximal levels of resistance to natural enemies, even in the presence of substantial genetic variation for resistance. Identifying constraints on the evolution of increased resistance has been a major goal of researchers of plant-herbivore interactions. In a glasshouse study, we measured relative costs and benefits of resistance of tall goldenrod (Solidago altissima) to the gall-inducing tephritid Eurosta solidaginis. We exposed multiple ramets of 26 goldenrod genets to nutrient or shade stress and to oviposition by E. solidaginis. The presence of a gall cost a ramet an average of 1743 seeds, but the cost differed 10-fold across environments. Plant genets varied widely for an induced 'hypersensitive' response in which meristem cells become necrotic and kill E. solidaginis hatchlings before gall induction. There was no evidence that this highly effective resistance trait carried an allocation cost. However, the response carried a risk of autotoxicity, as necrosis killed the apex of 37% of the ungalled ramets. On average, a damaged apex cost each ramet 5015 seeds. Autotoxicity may constrain the resistance of S. altissima to an intermediate level, and variation in environmental conditions may alter the relative costs and benefits of resistance and tolerance, thus maintaining genetic variation within goldenrod populations.

Extensive clonal spread and extreme longevity in saw palmetto, a foundation clonal plant.

The lack of effective tools has hampered out ability to assess the size, growth and ages of clonal plants. With Serenoa repens (saw palmetto) as a model, we introduce a novel analytical framework that integrates DNA fingerprinting and mathematical modelling to simulate growth and estimate ages of clonal plants. We also demonstrate the application of such life-history information of clonal plants to provide insight into management plans. Serenoa is an ecologically important foundation species in many Southeastern United States ecosystems; yet, many land managers consider Serenoa a troublesome invasive plant. Accordingly, management plans have been developed to reduce or eliminate Serenoa with little understanding of its life history. Using Amplified Fragment Length Polymorphisms, we genotyped 263 Serenoa and 134 Sabal etonia (a sympatric non-clonal palmetto) samples collected from a 20 × 20 m study plot in Florida scrub. Sabal samples were used to assign small field-unidentifiable palmettos to Serenoa or Sabal and also as a negative control for clone detection. We then mathematically modelled clonal networks to estimate genet ages. Our results suggest that Serenoa predominantly propagate via vegetative sprouts and 10,000-year-old genets may be common, while showing no evidence of clone formation by Sabal. The results of this and our previous studies suggest that: (i) Serenoa has been part of scrub associations for thousands of years, (ii) Serenoa invasion are unlikely and (ii) once Serenoa is eliminated from local communities, its restoration will be difficult. Reevaluation of the current management tools and plans is an urgent task.

The role of nodding stems in the goldenrod-gall-fly interaction: A test of the "ducking" hypothesis.

Herbivores are among the most pervasive selective forces acting on plants, and the number of plant chemicals that presumably evolved for defense against herbivory is immense. In contrast, biologists are only beginning to appreciate the important roles that architectural traits can play in antiherbivore defense. One putative architectural-resistance trait is the nodding stem apex of some goldenrods (Solidago; Asteraceae). Individuals of S. altissima genets that undergo temporary nodding in the late spring (i.e., "candy-cane" ramets) have been shown to be more resistant than individuals of erect-stemmed genets to certain apex-attacking herbivores. We tested the hypothesis that the greater resistance of candy-cane ramets is accomplished by the ramets' "ducking" from the herbivores. In a greenhouse experiment, nodding candy-cane ramets were significantly more resistant to oviposition by the gall-inducing fly Eurosta solidaginis than were ramets of the same genets that had been experimentally straightened. The straightened candy-cane stems were just as susceptible to ovipositions as were ramets of erect-stemmed genets. Thus, ducking indeed appears to confer a resistance advantage to candy-cane genets of S. altissima.

Applying the limiting resource model to plant tolerance of apical meristem damage.

Apical meristem damage (AMD) is a common result of herbivory. AMD can have dramatically variable effects on plant architecture and fitness, ranging from a total loss of reproductive capacity to overcompensation. We explored the influence of environmental stresses and meristem limitation on tolerance of AMD by applying the limiting resource model (LRM) of plant tolerance to 17 previously published studies and a new empirical study on Solidago altissima. In the S. altissima experiment, AMD released axillary meristems from apical dominance, and fertilizer addition enabled plants to take full advantage of the lateral branches. AMD caused a 58% reduction in seed production in nutrient-stressed plants but only a 6% reduction in seed production in fertilized plants. In 12 of the 18 studies reviewed, tolerance was greater in the high-resource (or low-competition) treatment; in two, tolerance was greater in the low-resource treatment; and in four, resource level did not affect tolerance of AMD. The results of 15 studies (83%) were consistent with LRM predictions. Overcompensation was observed in six studies, and it occurred only in the high-resource treatments in five of these studies, as would be expected from applying the LRM.

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.

Ducking as a means of resistance to herbivory in tall goldenrod, Solidago altissima.

Many populations of goldenrod show a peculiar, genetically controlled stem dimorphism. In Solidago altissima, for instance, while most stems are erect, a sizable minority (the "candy-cane" stems) nod at the apex during growth. We used data from three studies to test the hypothesis that this candy-cane growth form confers resistance to herbivory. In a controlled growth trial, we showed that nodding is a temporary phenomenon that coincides with the oviposition period of at least two common apex-attacking herbivores: the tephritid galler Eurosta solidaginis and the gall midge Rhopalomyia solidaginis. In a large field survey, stems of candy-cane genets were only half as likely to be ovipunctured by E. solidaginis. In a common-garden study, candy-cane stems were less likely to be ovipunctured by E. solidaginis, and they were galled only half as often by R. solidaginis as erect stems. These results suggest that the candy-cane stems of goldenrod possess a resistance strategy that allows them to essentially duck and hide from certain herbivores.

Nutrient stress and gall flies interact to affect floral-sex ratio in gynomonoecious Solidago altissima (Asteraceae).

A main tenet of sex-allocation theory is that environmental stress should lead to increased maleness because reproducing through pollen is generally cheaper than producing fruits and seeds. Though this prediction has held for many species, it has been little tested for gynomonoecious plants, in which individuals produce both female and perfect flowers. We exposed eight ramets of each of 22 genets of a gynomonoecious goldenrod, Solidago altissima (Asteraceae), to a factorial combination of nutrient stress and herbivory by the gall-inducer Eurosta solidaginis (Tephritidae). Nutrient stress alone increased relative femaleness: Stressed ramets produced fewer flowers total and a higher ratio of ray (female) flowers to disk (perfect) flowers. Galling caused no change in fertilized ramets, but the combination of nutrient stress and galling caused an increase in relative maleness: Nutrient-stressed, galled ramets produced fewer flowers total and had a higher disk to ray ratio. In addition to being phenotypically plastic, floral-sex ratio had a great deal of genetic variation, with a broad-sense heritability of 0.68. While the floral-sex ratio responses of gynomonoecious plants may be more complicated than for plants of other breeding systems, they offer the potential to test and refine the already rich body of sex-allocation theory.

Good mothers, bad mothers, and the nature of resistance to herbivory in Solidago altissima.

Evidence of poor correspondence between an insect herbivore's oviposition preferences and the performance of its offspring has generally been attributed either to maladaptive behavior of the insect mother or inadequate measurement by the researcher. In contrast, we hypothesize that many cases of "bad mothers" in herbivores may be a byproduct of the hierarchical way natural selection works on resistance in host plants. Epistatic selection on the components of resistance (i.e., antixenosis and antibiosis) may generate negative genetic correlations between the resistance components, which could counteract the efforts of herbivores to oviposit on the best hosts for the performance of their offspring. In common garden and greenhouse experiments, we measured aspects of antixenosis and antibiosis resistance in 26 genets of tall goldenrod, Solidago altissima, against two common herbivores: the gall-inducing fly Eurosta solidaginis and the spittlebug Philaenus spumarius. Goldenrod antixenosis and antibiosis were positively correlated against E. solidaginis and negatively correlated against P. spumarius. Analogously, population-wide preference-performance correlations were positive for the gall flies and negative for the spittlebugs. Several natural history differences between the two insects could make gall flies better mothers, including better synchrony of the phenologies of the flies and the host plant, the much narrower host range of the gall flies than the spittlebugs, and the more sedentary lifestyle of the gall fly larvae than the spittlebug nymphs. If these results are typical in nature, then negative genetic correlations in antixenosis and antibiosis in plants may often result in zero or negative population-wide correlations between preference and performance in herbivores, and thus may be an important reason why herbivorous insects often appear to be bad mothers.

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.

Leaf traits and leaf life spans of two xeric-adapted palmettos.

Plants of nutrient-poor, arid environments often have leaf traits that include small size, sclerophylly, long life span, low nutrient concentration, and low photosynthetic rate. Hence, the success of two large-leaved palmettos in peninsular Florida's seasonally xeric, nutrient-impoverished uplands seems anomalous, given that their leaves are orders of magnitude larger than the leaves of sympatric species. An examination of a 16-yr data set of leaf traits and leaf life spans across four vegetative associations differing in available light showed that Serenoa repens and Sabal etonia had low rates of leaf production coupled with long leaf life spans reaching 3.5 yr in heavily shaded plants. The adaptation of these palmettos to xeric, nutrient-poor habitats has generated dwarf statures, diminished leaf sizes and numbers, increased leaf life spans, and reduced rates of leaf production relative to other palms and congeners of more mesic sites. Leaf and petiole size, plant leaf canopy area, and leaf life span increased in both palmettos with decreasing available light, helping to compensate for reduced photosynthetic rates under shaded conditions and for the high leaf construction costs of the large, thick palmetto leaves. Large leaf size in these palmettos, likely due to phylogenetic conservatism, is compensated by other leaf traits (e.g., heavily cutinized epidermises, thick laminas) that increase survival in seasonally xeric, nutrient-impoverished environments.

Cryptic speciation and host-race formation in a purportedly generalist tumbling flower beetle.

Host-race formation remains controversial as a source of herbivorous insect diversity, and examples of host races are still fairly scarce. In this study, analysis of five enzyme loci in the ostensibly generalist tumbling flower beetle Mordellistena convicta (Coleoptera: Mordellidae) revealed hidden host-plant and plant-organ related genetic differentiation. Mordellistena convicta turned out to be a complex of cryptomorphic species, each with fewer hosts than the nominal species. These cryptic species, in turn, were divided into taxa that showed host-race characteristics: samples from different host plants and organs exhibited (1) genetic indications of partial reproductive isolation, (2) differences in size and emergence timing that suggested divergent host-related selection, and (3) among-host selective differences in mortality from parasitoids. Host-race formation in M. convicta, which has a somewhat different life history from the well-studied host races, enlarges the group of insects considered likely to undergo this process. The widespread sympatry of the M. convicta species complex, along with its spectrum of host-correlated genetic differentiation, suggests that these host specialist taxa developed in sympatry.

Long-term trends in annual reproductive output of the scrub hickory: factors influencing variation in size of nut crop.

Reproductive output by the Florida-endemic scrub hickory (Carya floridana Sargent) was studied over a 28-yr period in three south-central Florida vegetation associations: southern ridge sandhill, sand pine scrub, and scrubby flatwoods. The objectives were to describe multi-annual patterns of variation in nut production, identify factors involved in this variation, and investigate differences in patterns among associations. Peaks (higher values bracketed by lower values) in nut production occurred in 7 yr in sandhill and scrub and 8 yr in scrubby flatwoods during the 22-yr period for which we had continuous data. Of the total of 22 peaks in the three associations combined, 17 occurred at intervals of 2 or 3 yr, and peaks occurred in the same years in 18 of the 22 cases. Periodicities of nut production generated by spectral analyses (Fourier transforms) generally agreed with the observed peaks. Numbers of nuts per bearing ramet, proportion of ramets bearing nuts, ramet height, and light availability were positively correlated with nut production. Weather variables, specifically winter rainfall and minimum spring temperatures, accounted for a total of about one-quarter to one-half of the variance in nut production depending on the vegetation association. Following a prescribed fire in a sandhill plot, scrub hickory quickly regained fruit production, but over a 5-yr period following the fire nut production by ramets in the largest size class was reduced compared with the unburned control plot.

Cynipid gall-wasp communities correlate with oak chemistry.

Host-plant association data, gathered from field surveys conducted throughout Florida and from the literature, were used to identify the specificity of cynipid gall inducers to one or more of six Quercus species that occur at Archbold Biological Station, Lake Placid, Florida, USA, including the red oaks Q. laevis, Q. myrtifolia, and Q. inopina, and the white oaks Q. chapmanii, Q. geminata, and Q. minima. Quercus myrtifolia had the highest cynipid richness and diversity (37 cynipid species, Shannon H' = 3.61, Simpson's D = 0.97), followed by Q. chapmanii, Q. laevis, Q. inopina, Q. geminata, and finally Q. minima (10 species, H' = 2.30, D = 0.90). All cynipid species showed strong fidelity to a particular host plant or a restricted set of host plants. An ordination of gall-wasp host associations indicated that the cynipid communities of each oak species were distinct and specific to a given oak species. Leaf samples taken from each oak species were analyzed for condensed and hydrolyzable tannins, total phenolics, lignin, cellulose and hemicellulose, nitrogen, and carbon. All of these chemical traits, with the exception of carbon, differed by oak species, and the differences were strongly correlated with the axes of the cynipid-species ordination. These results suggest that gall-wasp occurrence is influenced by oak chemistry and imply that experimental studies of cynipid gall inducers that examine host-plant chemistry and female oviposition choice and larval performance will yield useful insights.

One host shift leads to another? Evidence of host-race formation in a predaceous gall-boring beetle.

We show that a predator, the tumbling flower beetle Mordellistena convicta (Coleoptera: Mordellidae), has formed host races in response to a host-plant shift and subsequent host-race formation by its prey, the gall-inducing fly Eurosta solidaginis (Diptera: Tephritidae). This fly has formed two host races, one that induces stem galls on the ancestral host plant, Solidago altissima (Compositae), and another that induces stem galls on the closely related S. gigantea. We found that subpopulations of M. convicta that attack E. solidaginis galls on the different host plants have significantly different emergence times and, although slight, these allochronic differences are consistent across a range of temperatures. More importantly, we found that beetles assortatively mate according to their natal host plants, and female M. convicta preferentially attack and/or their offspring have higher survival in galls on natal host plants. Our data suggest that subpopulations of M. convicta that attack E. solidaginis galls on S. altissima and S. gigantea have formed host races. This is one of the first studies to demonstrate that a host shift and subsequent host-race formation by an herbivorous insect may have resulted in subsequent diversification by one of its natural enemies.

Post-fire recovery of acorn production by four oak species in southern ridge sandhill association in south-central Florida.

We examined post-fire recovery of two components of acorn production (percentage of bearing ramets [stems] and number of acorns per bearing ramet) for four species of oaks in southern ridge sandhill vegetation in south-central peninsular Florida. Annual counts of acorns on two white oaks (Quercus chapmanii and Q. geminata) and two red oaks (Q. laevis and Q. myrtifolia) were conducted annually (except in 1991) on two 2.7-ha grids from 1969 to 1998. A prescribed burn was conducted on one of the grids in May 1993. Newly sprouted ramets of both white oaks produced acorns during the first year following the fire, whereas red oaks required 3 yr (Q. myrtifolia) or 4 yr (Q. laevis) to produce acorns. The difference in the timing of post-fire acorn production between the white and red oak species reflected the difference in the number of years from flower bud initiation to mature acorns in the two groups, with the additional year-long lag in Q. laevis probably attributable to the fact that it is typically a tree rather than a shrub species. The data suggested that percentage of bearing ramets in the smallest size class of the two white oak species was markedly lower in the burned than unburned grid in the first year of post-fire acorn production and higher in the fifth year, but these trends were not evident for the red oaks. Among all four species, differences between mean number of acorns in burned and unburned grids were significant in only two cases (the largest size class of both white oak species in the fifth year). There was no evidence of recruitment from acorns on the burned grid, possibly due to the rapid redevelopment of the shrub layer because of low mortality of the extensive clonal root systems. Rapid post-fire recovery of acorn production in xeric fire-prone habitats is presumably the result of selection to increase the probability of recovery and persistence following sufficiently intense fires that result in high oak mortality. The timing and magnitude of post-fire acorn production in sandhill and other xeric Florida associations has a potential impact on a wide variety of insects, birds, and mammals that feed on acorns, as well as on the species with which they interact.

Relation of ramet size to acorn production in five oak species of xeric upland habitats in south-central Florida.

This study examined variation in two components of acorn production. Percentage of bearing ramets (stems) and number of acorns per bearing ramet were examined in five clonal oaks in three xeric habitats of south-central peninsular Florida in relation to ramet size within and between species and vegetative associations. Counts of acorns on two white oaks (Quercus chapmanii and Q. geminata) and three red oaks (Q. inopina, Q. laevis, and Q. myrtifolia) were conducted annually from 1969 to 1996 (except in 1991) on permanent grids in southern ridge sandhill, sand pine scrub, and scrubby flatwoods associations at the Archbold Biological Station, Florida, USA. Percentage of bearing individuals and mean number of acorns per bearing individual increased with increasing ramet size for all species across all vegetation associations. However, in Q. geminata and Q. myrtifolia, acorn production declined in the largest size class (>3.2 m), implying that larger individuals of these clonal species may become senescent. All oak species in sand pine scrub, which had a nearly closed overstory, had lower frequencies of bearing oaks and mean numbers of acorns compared with similar-sized individuals of the same species in the more open-canopied southern ridge sandhill and scrubby flatwoods associations, suggesting light limitation. The annual production of acorns by a given oak species was correlated across vegetative associations and annual acorn production of oak species was correlated for species within the same section. Intermediate-size class oaks contributed the most acorns per unit area, suggesting that stands managed with short fire-return times will provide fewer acorns to wildlife than stands managed to produce more variable distributions of oak size classes. However, our study suggests that long-unburned stands, such as those studied here, will maintain relatively constant levels of acorn production as a consequence of ramet replacement within the clones of these shrubby oaks to create a variable distribution of size classes. Of the oak species studied, Q. myrtifolia had the highest acorn production and the smallest acorns, while Q. laevis had the lowest acorn production and the largest acorns, suggesting an allocation trade-off between acorn numbers and size.

Goldenrod stem galler preference and performance: effects of multiple herbivores and plant genotypes.

Few studies have examined how the preference-performance relationship of an herbivore for different genotypes of its host plant is affected by the presence and/or feeding activity of other members of the herbivore assemblage. In an outdoor garden, we manipulated the abundance of three common herbivores, the meadow spittlebug, a leaf beetle, and an aphid, on replicate 1-m2 plots of 16 different genotypes of tall goldenrod, Solidago altissima. Adults of the goldenrod stem galler, Eurosta solidaginis, were subsequently released into the garden to oviposit among the host plants. Oviposition preference was strongly influenced by plant genotype and the presence of two of the herbivores, spittlebugs and leaf beetles. The effects of the herbivores were additive: the presence of leaf beetles reduced preference by 6%, spittlebugs by 18%, and both herbivores combined by 25%. Plant genotype-herbivore species interaction effects on stem-galler preference, which would indicate the presence of genetic variation among goldenrod genotypes in their norms of reaction for their acceptability as a host to the stem galler, were absent in this study. The performance of the stem galler was also significantly affected by goldenrod genotype, but in general was not affected by the presence of herbivores early in the season (the exception was a positive correlation between the proportion of ramets infested by all herbivores and gall size). Overall, we could find no correlation between preference and performance. This is in accord with results from previous studies on this system that were performed in the absence of herbivores, suggesting that the presence of herbivores in this study did not qualitatively alter the preference-performance relationship. We suggest that the lack of a positive correlation between host-plant preference and larval performance may reflect a constraint on the discriminatory ability of female stem gallers preventing them from selecting the best hosts among plants that differ in genotype and level of environmental stress (e.g., presence of interspecific herbivores).

Host-plant genotype and other herbivores influence goldenrod stem galler preference and performance.

Ecologists have labored to find an explanation for the lack of a positive correlation between host preference and offspring performance in herbivorous insects. This study focuses on how one herbivore species can influence another herbivore species' ability to accurately assess the suitability of different host-plant genotypes for larval development. In particular, we examined the role that an early season xylem-feeding homopteran (meadow spittlebug, Philaenus spumarius) has on the preference-performance correlation of a late-season dipteran stem galler (Eurosta solidaginis) among different goldenrod genotypes. In a greenhouse, we released adult stem gallers into replicate cages that contained ramets from four different goldenrod genotypes crossed with three densities of spittlebugs (0, 1, or 8 nymphs placed 2 weeks previously on each ramet). Spittlebug feeding caused a density-dependent decline in ramet growth rates, which in turn caused a corresponding decrease in host-plant preference by the stem gallers (number of ovipunctures per bud or proportion of ramets attacked). Goldenrod genotype and the interaction between spittlebugs and genotypes also influenced host-plant preference by the stem galler. Goldenrod genotype had the greatest impact on stem galler offspring performance (gall size or survivorship). Spittlebug density also affected performance, but only through its interaction with goldenrod genotype. On some genotypes, the survivorship of stem-galler larvae decreased with increasing spittlebug density, while on other genotypes, survivorship remained unchanged, or actually increased, with increasing spittlebug density. This suggests that there was genetic variance among goldenrod genotypes in their norms of reaction for their suitability as a host to the stem gallers. One possible explanation for why spittlebugs caused a significant reduction in preference, but not in performance, was that spittlebugs had very few long-term effects on the host plant. Flower number, flowering phenology, and the allocation of the ramet's biomass to different structures (below-ground organs, stems, leaves, and flowers) were unchanged with respect to spittlebug density. The only effect of spittlebugs was a 3-4% decrease in ramet height at the end of the growing season. We argue that the lack of a positive correlation between host-plant preference and larval performance may reflect a constraint on the discriminatory ability of female stem gallers. The damage to goldenrods caused by spittlebugs prior to attack by the stem gallers is similar in effect to potentially innumerable other causes of goldenrod stress (e.g., reduction in ramet growth rates). As a consequence, stem gallers may not be able to discern the subtle differences among stresses that identify those that will negatively affect the fitness of stem-galler offspring. The fact that goldenrod genotypes differ in their response to stresses would only further complicate the host-selection process. We propose that the stem gallers may have evolved a strategy that uses simple cues as the basis for rejecting similarly stressed plants, whether all of those plant genotype-stress combinations reduce performance or not.