Release of phylogenetic constraints through low resource heterogeneity: the case of gall-inducing sawflies

Abstract. 1. A group of six unusual sawfly species, which do not conform to the phylogenetic constraints hypothesis as it has been applied to sawflies, was examined in natural populations. All species were in the genus Pontania (Hymenoptera: Tenthredinidae), which induce galls on leaves of willow species (Salicaceae). An understanding of these non‐conformist species was important as a test of the validity of the general hypothesis. 2. The six species of sawfly, Pontania mandshurica, P. cf. arcticornis, P. aestiva, P. arcticornis, P. pacifica, and P. nr. pacifica, showed no oviposition preference for long, vigorous shoots, in contrast to 37 documented tenthredinid species that have demonstrated such a preference. Rather, the non‐conformist species attacked the shortest shoot length classes more frequently and larval establishment in galls was successful. 3. The evident escape from the phylogenetic constraint, which commonly limits sawfly attack to the most vigorous shoots in a willow population, resulted from low apparent heterogeneity of the resources exploited by these Pontania species. At the time of female oviposition, shoots and leaves were too uniform to allow discrimination by females among shoot length classes, resulting in random, or near random attack of shoots. 4. The unusual relative uniformity of resources to which sawflies were exposed resulted from several characteristics. (1) Females emerged early relative to shoot growth phenology, making discrimination among shoot length and vigour difficult or impossible. (2) Low heterogeneity in leaf length resulted in resource similarity independent of shoot length. (3) Abscission of leaves occurred after emergence of larvae from leaf galls so that differential abscission of leaves in relation to shoot length became irrelevant. (4) In some cases, low variance in shoot lengths was evident in old ramets lacking long, vigorous shoots. Probably as a result of low resource heterogeneity, larvae survived well across all shoot length classes, revealing no ovipositional preference and larval performance linkage related to the exploitation of the longest shoot length classes in a population of willows, as in the conformist species. Therefore, larval survival did not provide positive feedback on female preferential behaviour for long shoots, as in the conformist species studied.     

Preference and performance of a gall-inducing sawfly: a test of the plant vigor hypothesis

To test the Plant Vigor Hypothesis, we determined female oviposition preference of Phyllocolpa leavitii (Hymenoptera: Tenthredinidae) for shoot lengths on 20 clones of Salix discolor (Salicaceae) and examined larval performance by determining larval survival based on clone, shoot length, and leaf length for each Phyllocolpa gall observed. Sawfly galls were found on significantly longer shoots compared to shoots without galls, and shoots with 2, 3, 4, and 5 galls were successively longer than shoots with fewer galls. Furthermore, a much higher proportion of longer shoots had galls that did shorter shoots. These data demonstrate strong sawfly oviposition preference for long shoots. However, when shoot length was adjusted for numbers of available leaves per shoot, the number of galls per available leaf showed a weaker, but still positive relationship with shoot size. Using a logistic regression on survival of Phyllocolpa larvae, we detected highly significant effects of clone, shoot length, leaf length, and the square of leaf length on survival. Additionally, much higher sawfly survival on the long shoots of one clone caused a significant clone by shoot-length interaction. Survival was positively correlated with shoot length, indicating directional selection favoring oviposition on longer shoots; still, shoot length explained only 11.8% of the variation in survival. The directional component of selection favored oviposition on smaller leaves as survival was inversely related to leaf length; however, disruptive selection for leaf length oviposition preference was also detected, with survival of Phyllocolpa galls lowest on intermediate leaf lengths. This study provided evidence supporting the preference prediction of the Plant Vigor Hypothesis. However, much of the data contradicted the performance prediction of the Plant Vigor Hypothesis, with only a modest amount of evidence supporting the performance prediction.     

Spatial Distribution of Galls Caused by <Emphasis Type="Italic">Aculus tetanothrix</Emphasis> (Acari: Eriophyoidea) on Arctic Willows

The distribution of galls caused by Aculus tetanothrix (Acari: Eriophyoidea) on three Salix species was studied. The factors influencing this distribution were analysed, i.e. willow species, study area and shoot length. Spatial pattern of gall distribution within the shoot was also examined. The study was conducted in Russia, Kola Peninsula. Densities of galls caused by A. tetanothrix differed significantly among willow species. Considerably higher gall density was recorded in the White Sea coast than in the Khibiny Mountains. This may be explained by the influence of a milder maritime climate that favors mite occurrence compared to a harsh and variable mountain climate that limits mite abundance. There was no relationship between the gall density and the shoot length. The highest density of galls was recorded on the inner offshoots; within the offshoot, there was a maximum density on the fifth leaf. This pattern was repeatable for all shoots studied, independent of the study area, willow species and length of shoots, suggesting the optimal conditions for A. tetanothrix exist on leaves in the middle part of a shoot. This distribution pattern may be an effect of the trade-off between the costs and benefits resulting from leaf quality and mite movement along the shoot. This hypothesis, however, needs to be tested experimentally.     

Why does the bud-galling sawfly,Euura mucronata,attack long shoots?

Summary The bud-galling sawfly, Euura mucronata, attacked longer shoot length classes on its host, Salix cinerea, more frequently than shorter shoots. Shoot length accounted for 76 to 93 percent of the variance in number of galls per 100 shoots in three habitats: forest, watermeadow, and lakeside. The reasons for this pattern were addressed with studies on shoot length in relation to: 1. Number of resources (buds) per shoot; 2. Success in establishment of larvae in galls; 3. Gall size and resources per gall; and 4. Survival of larvae after establishment as influenced by plant resistance and natural enemy attack. The most important factors proved to be success in establishment of larvae, with percent of variance accounted for ranging from 57 to 77 percent in three of four sites where relationships were significant, and survival after establishment of larvae, with variance accounted for ranging from 40 to 54 percent in the same three sites. The pattern of survival was dictated by plant resistance and not by natural enemies. These two additive factors resulted in a general relationship across all sites of increasing emergence of fully developed larvae per cohort as shoot length increased, accounting for 78 percent of the variance. These adaptive advantages to attacking longer shoots are sufficient to account for the pattern of increased probability of shoots being attacked as they increase in length.     

Multiple effects of precipitation onSalix lasiolepis and populations of the stem-galling sawfly,Euura lasiolepis

Relatively low winter precipitation (e.g., 18–28 cm from October to May compared to 45 to 65 cm) caused reduced growth of the arroyo willow,Salix lasiolepis, with number of shoots per stem initiated and shoot length reduced. Resources were reduced for the stem-galling sawfly,Euura lasiolepis, which declined in numbers after the relatively dry winter of 1980–81. Sawfly phenology was advanced relative to willow phenology in the 1981 generation, causing an additional reduction in resource availability. These direct effects of precipitation on the sawfly were increased by indirect effects on survivorship of the 1981 generation. Egg death in galls increased on water-stressed willow plants, forming the major mortality in the generation. This resulted in very low survival in the generation and an even lower population in the 1982 generation, even though resources recovered after high precipitation during the 1981–82 winter (46.7 cm). An experiment using high, medium, and low water treatments on potted willow plants demonstrated that the effects on willows and sawflies could be reproduced using only water as a variable.     

Impact of two shoot-galling biological control candidates on Russian knapweed, Acroptilon repens

Russian knapweed, Acroptilon repens, is one of the most serious exotic invaders of temperate grasslands in North America. Here we present results from a field experiment in which we quantified the impact of two potential biological control agents, the gall wasp Aulacidea acroptilonica V.Bel. (Hymenoptera, Cynipidae) and the gall midge Jaapiella ivannikovi Fedotova (Diptera, Cecidomyiidae), on A. repens under field conditions in the plant’s native range in Uzbekistan. Attack by A. acroptilonica reduced shoot length by 21%, above-ground biomass by 25% and seed output by 75%, while attack by J. ivannikovi reduced shoot length by 12%, above-ground biomass by 24%, and seed output by 92%. The results of these field experiments are likely to accurately reflect the potential of these two gall formers to reduce above-ground biomass and sexual reproduction of A. repens shoots, since the shoots were part of a clonal network. Despite this, the attacked shoots were not able to compensate for the reallocation of plant resources to gall formation. Moreover, the mean number of galls per shoot obtained in the experiments was within the range of observed gall incidences in the native range. The impact of these two gall-forming insects on Russian knapweed in North America will depend on the population size the species reach and on the timing of attack. The highest impact is likely to occur when the insects attack shoots that have not yet started producing flower-buds.     

Preference and performance linkage in aPhyllocolpa sawfly on the willow,Salix miyabeana,on Hokkaido

A leaf-folding sawfly in the genusPhyllocolpa (Hymenoptera: Tenthredinidae) attackingSalix miyabeana (Salicaceae) was studied near Sapporo, Hokkaido, along the Ishikari River in 1993. Host plant individuals were young trees 4–7 years old which were growing rapidly, producing some long shoots with large leaves. On a gradient of shoot length classes from 0–5 cm long to over 80 cm long, shoots were much more abundant in the shorter shoot length classes. However, attacks by ovipositing females increased as shoot length increase from 0 attacks on the shortest shoots to 5.17 attacks per shoot on the longest shoots. The frequency of attack per leaf increased from 0 to 0.13 over the same range of shoot lengths. This pattern of attack resulted in a high frequency of larval establishment in feeding sites, between 0.96 and 1.00, in all attacked shoot length categories. However, probability of survival to a late instar larva increased with shoot length and corresponded to the attack pattern, indicating a preference-performance linkage between female ovipositional decisions and larval survival. The patterns found for thisPhyllocolpa species are similar for galling sawflies in North America and Europe, especially in the genusEuura, members of which make stem, bud and leaf midrib galls. Extending the pattern to aPhyllocolpa species broadens identification of pattern and ultimately the generality of the emerging theory on populations of galling sawflies.     

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 age and attack by the bud galler,Euura mucronata

Summary As ramets of the willow, Salix cinerea L. (Salicaceae) aged shoot length decreased in the six populations studied in S.E. Finland. Many traits correlated positively with shoot length: basal diameter, number of internodes, internode length, leaf size, and length of growing period. The bud-galling sawfly, Euura mucronata (Hartig) Man. (Churchill) (Hymenoptera: Tenthredinidae), responded positively to shoot length or correlated traits, and negatively to ramet age in three forest populations. This herbivore attacked the most vigorous plants in a population, and numbers of attacks declined as ramets aged and senesced. The generality of this kind of herbivore response to plant quality is emphasized.     

Patterns of interspecific associations of stem gallers on willows

Abstract.  The pattern of interspecific associations of three stem-galling sawfly species ( Euura atra , E. elaeagnos , E. purpureae ) and three stem-galling gallmidge species ( Rabdophaga sp. 3–5) was investigated on five willow taxa ( Salix alba , S. fragilis , S.  ×  rubens , S. elaeagnos , S. purpurea ) at five natural sites in Central Europe. The willow species harboured specific species associations of two stem gallers, each pair consisting of one Euura and one Rabdophaga species. The stem gallers were patchily distributed and their densities varied significantly among willow host plant species, host plant individuals, and host plant sexes. Four of the six species showed a significant increase in galling rate with shoot length. The other two species were the sawfly and cecidomyiid pair that induce galls on S. purpurea . The preference of stem gallers to longer shoots was generally not related to higher larval performance in terms of survival. Only one species, Rabdophaga sp. 5, was found to be more abundant on male plants. The correlation of densities of the species pairs of stem gallers was independent of willow sexes. Species pairs of stem gallers co-occurring on the same willow species tended to attack different shoots within the same host plant individual. When species pairs co-occurred on shoots they were usually found in similar densities as when occurring alone on shoots. The stem-galling sawflies usually formed galls at the basal part of a shoot, whereas the gallmidge R . sp. 5 ( R . sp. 3 and R . sp. 4 showed no clear tendency) preferred the middle or distal part of a shoot. This is interpreted with differences of their phenology and oviposition period.     

Plant wound compounds from oviposition scars used in host discrimination by a stem-galling sawfly

The stem-galling sawfly Euura lasiolepisuses one or more plant wound compounds resulting from oviposition scars as cues in host discrimination (avoiding sites occupied by conspecifics). Four experiments were conducted to test hypotheses about how Euurapartitions resources. Experiment 1 demonstrated that Euuraavoids ovipositing on nodes with scars from previous ovipositions. Experiment 2 showed no evidence that the sawfly uses oviposition-deterring pheromones and indicated there is a time lag following oviposition before the oviposition scar becomes a deterrent. Experiment 3 showed that sawflies avoid artificially formed scars, demonstrating that a plant cue alone can lead to host discrimination. Experiment 4 showed that visual or tactile cues are not necessary for host discrimination and indicated that a plant wound compound functions as an oviposition deterrent. Both experimental results and field surveys showed that Euuraoviposition scars were more uniformly distributed than expected if sawflies were ignoring previous ovipositions.     

How does spittlebug oviposition affect shoot growth and bud production in two willow species?

We measured the effects of oviposition by the spittlebug Aphrophora pectoralis on shoot growth and bud production in two willow species, Salix miyabeana and Salix sachalinensis. In autumn, adult females of A.pectoralis insert their ovipositor into the apical region of 1-year-old shoots, resulting in the death of most shoot tips within 1week. Consequently, an increase in the number of dead buds and a decrease in the number of vegetative buds on 1-year-old shoots was recorded. In the following spring, the growth of current-year shoots was greatly increased on 1-year-old shoots damaged by spittlebug oviposition. Furthermore, spittlebug oviposition increased the production rate of vegetative buds in both S.miyabeana and S.sachalinensis. However, no impact on the production rate of reproductive buds was detected in either willow. We conclude that the compensatory growth of current-year shoots and an increase in vegetative buds in the two willow species was caused by oviposition of A.pectoralis.     

Testing a new hypothesis: plant vigor and phylloxera distribution on wild grape in Arizona

Summary Longer, meaning more vigorous, shoots of a wild grape clone (Vitis arizonica) were more susceptible to attack by second and third generations of leaf-galling grape phylloxera,Daktulopsphaira vitifoliae, as the growing season progressed. Although there was no significant difference in mean shoot length between attacked and unattacked shoots within a clone at the beginning of shoot elongation, attacked shoots were significantly longer than unattacked shoots when elongation had ceased (P<0.01). Also, long attacked shoots had a significantly greater population of phylloxera galls than short attacked shoots (P<0.01) as the season progressed. The phylloxera population on long shoots increased rapidly while the population on short shoots remained the same. Longer shoots also produced significantly more axillary shoots than shorter shoots as the season progressed (P<0.001), and the number of axillary shoots accounted for 66 percent of the variance in number of attacked leaves on a shoot. Experimental evidence showed that there was a significantly greater percentage of available leaves attacked on long shoots than on short shoots (P<0.05) and the leaves on long shoots generally had a greater number of galls per leaf. The relationship between shoot length and probability of attack was also tested by comparing shoots lengths of 10 attacked clones and 10 unattacked clones at a second location. Mean shoot lengths of attacked clones were significantly longer than mean shoot lengths of unattacked clones (P<0.05), and mean shoot lengths of attacked shoots within a clone were significantly longer than unattacked shoots (P<0.001). Longer shoot length accounted for 81 percent of the variance in probability of attack. The reason for this pattern of attack was that long shoots produced newly expanding leaves over a longer time during the growing season and multivoltine phylloxera require undifferentiated tissue to initiate gall formation. Patterns of attack within a shoot were characterized by an uneven distribution of galls among leaves. This was due to development time between generations and the current availability of undifferentiated tissue at times of colonization. This study supports the hypothesis that some herbivore species are favored more by vigorous plants than by stressed plants.     

Gall mite (Eriophyes laevis) infestation and leaf removal affect growth of leaf area in black alder (Alnus glutinosa) short shoots

Summary We measured the effects ofEriophyes laevis mite galls on the relative growth of short shoot leaf area ofAlnus glutinosa. A portion of leaves was artificially removed from a set of short shoots with both high and low gall density to cause local stress conditions. Nontreated high and low gall density short shoots were used as controls. The results show that the relative growth of leaf area measured for short shoots is negatively affected by high gall density. Artificial leaf removal, on the other hand, had positive effects on leaf area growth. Interestingly, the growth of leaf area did not differ for high gall density short shoots with leaf removal and noninfested short shoots with no leaf removal. This result may be caused by the combined, opposite effects of leaf removal and gall infestation.     

Field test of resource regulation by the bud-galling sawfly, Euura mucronata, on Salix cinerea

The attack by the bud-galling sawfly, Euura mucronata , on its willow host was simulated by removing every other living bud from previous year's shoots in a natural stand of Salix cinerea . The impact of simulated attack on the growth of the willow and the subsequent attack by E. mucronata was estimated after one growing season. Experimental bud-killing resulted in a growth reaction in S. cinerea characterized by significant increase in the length of new shoots produced by the remaining buds Also the number of buds and E. mucronata galls per shoot were significantly higher on bud-removal branches as compared with control branches. The overall survival of E. mucronata larvae was better on long shoots than on short shoots. The result shows that sawfly attack increases the amount of high quality resources for the subsequent generation of the same sawfly as predicted by "resource regulation hypothesis". We conclude that these highly specialized insect herbivores have adapted to utilize and to maintain the willow's juvenile traits. Rapid regrowth of willows after damage may have originally arisen as an adaptation in response to other, less specific pressures such as mammal browsing or snow and ice damage.     

Willow leaf traits affecting host use by the leaf-gall-forming sawfly

Gall-forming insects usually have very restricted host ranges, but plant traits affecting patterns of host use have rarely been examined. The sawfly Phyllocolpa sp. (Hymenoptera: Tenthredinidae) forms leaf-roll galls on three of seven Salix (Salicaceae) species that occur together on riverbanks in central Japan. We have attempted to explain this host-use pattern by invoking three plant traits: synchrony of leaf flush with the oviposition period of the sawfly, intrinsic leaf quality as a potential larval food, and leaf morphology. Two Salix species frequently used by the sawfly, Salix eriocarpa and Salix pierotii, had similar leaf traits suitable for larval survival. The third species, Salix serissaefolia, was used relatively less often and the sawfly frequently stopped laying eggs on the plant during oviposition, suggesting ovipositional selection. S. serissaefolia had the smallest leaves, and survival of sawfly larvae was lower on S. serissaefolia than on S. eriocarpa and S. pierotii, because of gall destruction, by other herbivorous insects, and leaf-size restrictions. Among the four unused species, Salix chaenomeloides had a late leaf-flush phenology, Salix gracilistyla had inferior leaf quality, and Salix gilgiana had linear leaves; these seemed to be critical factors for non-use. Salix subfragilis was also unused, but the reason for this could not be explained by the three leaf traits studied.     

Intra‐plant heterogeneity influences the preference and performance of juveniles and adults of a gall midge

Abstract 1. Field studies were conducted to evaluate the preference and performance of a gall‐inducing midge (Harmandia tremulae) within the crown of trembling aspen (Populus tremuloides). Females did not select oviposition sites preferentially within leaves, but did lay preferentially on young leaves. 2. Larvae were the only life stage involved in gall site selection within leaves and in gall initiation and development. Gall size, which was positively related to survival, was highest for galls on mid veins that were located close to the petiole. However, one‐third of galls were located on lateral veins and most galls were not adjacent to the petiole, indicating that many larvae choose sub‐optimal gall initiation sites. 3. Gall density was positively associated with leaf length, and leaf length, was positively associated with gall size. However, gall density per leaf was not related to larval survival in galls. This latter result may be a result of an observed inverse relationship between gall size and gall density for similar‐sized leaves. 4. The results partially support the plant vigour and optimal plant module size hypotheses, which predict that galler fitness in successfully induced galls should be highest on large, fast‐growing plant modules. The lack of a strong preference‐performance link supports the confusion hypothesis, which predicts that oviposition and gall site selection may often be suboptimal in systems where galler lifespan is short. This study suggests that small‐scale variations in plant quality within leaves, can render gall site selection by juveniles as important as that previously reported for adult females.     

The functional resource of a gall-forming adelgid

Interactions among shoots within plant modules could allow gall-insects to acquire resources from other plant parts near the feeding sites. As a result, nearby plant parts may act as a functional resource, or extended resource base. We tested for functional interconections between galls and adjacent ungalled shoots in Adelges cooleyi Gil. (Homoptera: Adelgidae) on Picea engelmanni, Engelmann spruce. Observations of gall and surrounding shoot weights showed that gall weights were twice normal shoot weights, but that surrounding shoot weights were unaffected. Reducing photosynthate availability by covering galls or surrounding shoots with opaque cloth suggested that functional interconnections exist among them; covering galls reduced surrounding current-year ungalled shoot weight, and covering surrounding shoots reduced their weight even further, but neither covering treatment affected gall or gall-insect weight. These patterns suggest that surrounding shoots constitute an extended and flexibly utilized resource base for adelgid galls. Resources made available via functional interconnections appeared to be equally available throughout adelgid galls. No differences were found in gall-insect performance in parts of the gall closer to connections with surrounding shoots compared to more distantly-located gall-insects. Further studies are required to examine patterns of resource movement among unmanipulated galls and shoots. Functional resources may be common features of plant/gall-insect interactions, potentially playing an important role in gall-insect reproductive success and habitat selection.     

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.     

Nematode‐induced galls in Miconia albicans: effect of host plant density and correlations with performance

The study of nematodes parasitizing native plants plays a crucial role in understanding plant–pathogen interactions. In the present study we describe the patterns of attack by an undescribed species of Ditylenchus occurring in Miconia albicans (Melastomataceae), a widespread, native shrub from the Brazilian cerrado. We also tested the hypothesis that nematode‐induced leaf galls negatively correlate to host plant performance and that gall density is a function of host plant density. We collected paired healthy and attacked shoots from 28 individuals of M. albicans and estimated the leaf area lost to nematode‐induced galls in up to 10 leaves per shoot. We analyzed the relationships between leaf area lost to nematode galls and reproductive traits. Nematode attack levels were also compared to the spatial distribution of the host plant. Inflorescence length and fruit production were significantly reduced in attacked shoots compared with healthy shoots. Seeds from attacked shoots showed no significant reduction in germinability or germination time when compared with seeds collected from healthy shoots. Gall density was positively correlated with host density. Despite being seldom studied in tropical ecosystems, nematodes may play an important role in plant fitness and in structuring tropical communities.