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.     

Plant phenology-mediated indirect effects: The gall midge opens the phenological window wider for a leaf beetle

We examined whether larvae of the gall midge Rabdophaga rigidae (Diptera: Cecidomyiidae) can modify the seasonal dynamics of the density of a leaf beetle, Plagiodera versicolora (Coleoptera: Chrysomelidae), by modifying the leaf flushing phenology of its host willow species, Salix serissaefolia and Salix eriocarpa (Salicaceae). To test this, we conducted field observations and a laboratory experiment. The field observations demonstrated that the leaf flushing phenology of the willows and the seasonal dynamics of the beetle density differed between shoots with stem galls and shoots without them. On galled shoots of both willow species, secondary shoot growth and secondary leaf production were promoted; consequently, leaf production showed a bimodal pattern and leaf production periods were 1 to 2 months longer than on non‐galled shoots. The adult beetle density on galled shoots was thus enhanced late in the season, and was found to change seasonally, synchronizing with the production of new leaves on the host willow species. From the results of our laboratory experiment, we attributed this synchrony between adult beetle density and willow leaf flush to beetles’ preference to eat new leaves rather than old. Indeed, beetles consumed five times more of the young leaves when they were fed both young and old leaves. These results indicate that stem galls indirectly enhance the adult beetle density by enhancing food quality and quantity late in the beetle‐feeding season. We therefore conclude that midge galls widen the phenological window for leaf beetles by extending the willows’ leaf flush periods.     

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.     

Growth of coyote willow and the attack and survival of a mid-rib galling sawfly,Euura sp.

We studied the relationship between variation in age and shoot characteristics of the host plant Salix exigua Nuttall (coyote or sandbar willow) and the attack and survival of Euura sp. (an unnamed leaf-midrib galling sawfly). Variation in shoot characteristics resulted from reduced growth as willow ramets aged. Mean shoot length per ramet and mean longest leaf length per shoot decreased by 95% and 50% respectively between 1- and 9-year-old willow ramets. All measured shoot characteristics-shoot length, longest leaf length, number of leaves per shoot, and mean internode length-were significantly negatively correlated with ramet age (r ² ranged from –0.23 to –0.41). Correlations between shoot characteristics were highly positive, indicating that plants also grew in a strongly integrated fashion (r ² ranged from 0.54 to 0.85). Four hypotheses were examined to explain sawfly attack patterns. The host-plant hypothesis was supported in explaining enhanced larval sawfly survival through reduced plant resistance. As willow ramets aged, the probability of Euura sp. attack decreased over 10-fold, from 0.315 on 1-year-old ramets to 0.024 on 2- to 9-year-old ramets. As shoot length increased, the probability of sawfly attack increased over 100-fold, from 0.007 on shoots <100 mm, to 0.800 on shoots in the 1001–1100 mm shoot length class. These attack patterns occurred even though 1-year-old ramets and shoots >500 mm each represented less than 2% of the total shoots available for oviposition. Host plant induced mortality of the egg/early instar stage decreased by 50% on longer leaves and was the most important factor determining survival differences between vigorous and non-vigorous hosts. Sawfly attack was not determined by the resource distribution hypothesis. Although shoots <200 mm contained 82% of the total leaves available, they contained only 43% of the galls initiated. The attack pattern also was not explained by the gall volume hypothesis. Although gall volume increased on longer shoots, there was no significant variation in mid or late instar mortality over shoot length, as would be expected if food resources within smaller galls were limited. The natural enemy attack hypothesis could not explain the pattern of oviposition since predation was greater on longer shoots and leaves. In addition, larval survival was related to oviposition behavior. Due to a 69% reduction in late instar death and an 83% reduction in parasitism, survival of progeny in galls initiated close to the petiole base was 2.8 times greater than in galls initiated near the leaf tip. A 75% reduction in gall volume over this range of gall positions may account for the observed increases in late instar mortality and parasitism.     

Community structure, survival and mortality factors in arctic populations of Eupontania leaf gallers

We studied survival, mortality factors, and community structure of nine species of leaf-galling sawflies, Eupontania spp., living on ten willow species (Salix spp.) at six sites on the Russian arctic tundra. The sawfly species represented two different gall types: the viminalis-type, which forms pea-shaped galls on the underside of leaf blades, and the vesicator-type, which forms bean-shaped galls on both sides of the leaf blade. Gall communities in the northernmost site had only one parasitoid species, but up to six parasitoids were found at the southernmost site. Inquiline parasitoids were encountered only in the two southern sites. Survival of the larvae varied between 20.0 and 82.8% among galler species at different sites. Parasitoids were the most important mortality factor for the sawflies. They caused mortality of 7.8-65.4%, depending on galler species and site, and it was highest in the northernmost site. Plant-specific mortality varied from 1.7 to 28.4% by galler species and it tended to decrease towards the north. Mortality from parasitoids was greater in the vesicator-type gallers than in the viminalis-type gallers. The total mortality caused by parasitoids in the arctic communities does not appear to differ from that in the diverse southern communities of Eupontania in Middle Europe, Scandinavia and North America, despite the assemblage having only a few members in the Arctic. The largest difference between the southern and the northern communities was the lack of inquiline parasitoids in the north. Our data do not support the hypothesis that abiotic, rather than biotic, factors would be more important in determining the abundance of populations of herbivorous insects in the harsh arctic environment.     

Plant stress and larval performance of a dipterous gall former

According to the plant vigour hypothesis, galling insects should respond positively and perform better on vigorous plants or plant parts, the opposite of the predictions of the plant stress hypothesis. I carried out field experiments to analyse the effects of sustained abiotic stress on the interactions between the common reed (Phragmites australis) and a gall-forming fly (Lipara lucens). The reed shoot diameter (a measure of plant vigour) is strongly affected by environmental conditions, where dry and/or nutrient-poor habitats produce thinner (stressed) shoots. L. lucens gall density is negatively correlated with shoot diameter. In a survival experiment with a wide range of shoot diameters, larval mortality was also highly correlated with shoot quality. Gall formation was higher on thinner, stressed shoots. An analysis of the gall tissues revealed that galls induced by L. lucens contain a high amount of a nutrient-rich feeding tissue. The impact of L. lucens is higher on thinner shoots. The results of this study showed that L. lucens performs better on stressed hosts, which contradicts the plant vigour hypothesis for galling insects. The low nutrient availability in the stressed shoots can be compensated by the production of galls with a nutrient-rich feeding tissue.     

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.     

Distribution and oviposition preference of galling sawflies in arctic Canada

The distribution and ecology of insects in arctic regions are poorly known. The aim of this study was to determine the distribution of galling sawflies in the Canadian arctic and their oviposition preference. The Swedish Tundra Northwest 1999 expedition visited 17 sites in the Canadian arctic. We determined the occurrence of galling sawflies at all the sites and studied the oviposition preference of two leaf-galling sawflies, Eupontania arctica and Pontania nivalis, on Salix reticulata and S. glauca, respectively. Galling sawflies were abundant at only one site, the mainland site at Ivvavik National Park. Only a few galls in total were found at the remaining sites, suggesting that galling sawflies are rare in the higher arctic, and potential explanations for this pattern are discussed. Shoots with leaf galls were longer than shoots without galls on both S. reticulata and S. glauca. These differences could not be explained by a higher number of leaves on longer shoots. This suggests that long shoots are preferred by sawflies because of faster development and better survival of larvae on long shoots.     

The giant willow aphid (Tuberolachnus salignus) and its effects on the survival and growth of willows

1. The giant willow aphid (Tuberolachnus salignus) is an invasive pest that can attain large populations on willows (Salix spp.). This has the potential to have a negative impact on the extensive use of willows for soil conservation, and as a source of pollen and nectar for honey bees in New Zealand.
2. A willow nursery field trial was established to evaluate the aphid populations, and the survival and growth of young plants of several willow species and hybrids, during two growing seasons from planting.
3. The willow species and hybrids varied widely in their susceptibility to the aphid, with large aphid populations and plant mortality in the most susceptible willows, and reductions in plant growth in all but aphid-resistant willows. The effects on the plants were not seen in the first season, but occurred during the second season.
4. The aphid can be expected to have some negative impacts in New Zealand, with reductions in growth of some willows commonly used for soil conservation, and for pollen and nectar for honey bees.

     

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.     

Long term oviposition preference and larval performance of Schizomyia macrocapillata (Diptera: Cecidomyiidae) on larger shoots of its host plant Bauhinia brevipes (Fabaceae)

The Plant Vigor Hypothesis (PVH) proposes that natural selection on female oviposition choice results from higher fitness of larvae on more vigorous and larger plant modules. For six consecutive years we tested the PVH predictions by investigating the effect of shoot size of Bauhinia brevipes (Fabaceae) on the oviposition preference and offspring survival of the gall-midge Schizomyia macrocapillata (Diptera: Cecidomyiidae). Additionally, we analyzed the effects of bottom-up and top-down mortality forces on the system. The hypersensitive reaction (bottom-up effect) accounted for more than 90% larval mortality of S. macrocapillata, making available few galls to be found and killed by natural enemies (top-down effect). Smaller shoots were always more abundant while longer shoots were rare. Nevertheless, the percent number of galls induced by S. macrocapillata was up to 10-fold greater on the largest shoots, corroborating the preference prediction of the PVH. Schizomyia macrocapillata should use over-exploit larger shoots to maximize the preference for, and consequently increase the performance on these shoots. Our results partially support the performance prediction of the PVH: (1) the observed survival was higher than expected on longer shoots, and (2) the ratio of survival per shoot was positively related with shoot length only in 2 years. Thus, we found a link between female preference and larval performance on large-sized shoots, at least in some years. The gall-midge attack pattern in this study might be an evolved response to maximize the female preference and increased larval performance on longer shoots of the host plant.     

Temporal change in the location of egg-laying by a bud-galling sawfly,Euura mucronata,on growing shoots of Salix cinerea

Summary Temporal change in the egg-laying behaviour of Euura mucronata was studied on growing shoots of Salix cinerea. Many new shoots arise from each previous year's shoot of S. cinerea; they grow very rapidly at the beginning of the oviposition period of E. mucronata, but their growth pattern changes dramatically during the 3 weeks of oviposition. When oviposition commences, all new shoots are equally long, and E. mucronata females lay eggs on them randomly; but toward the end of oviposition, eggs are laid on the longest of the new shoots, which originate on the distal part of the previous year's shoot. By the end of oviposition, the mean proportion of ovipositor borings that had resulted in egg-laying was 65.8% on distal shoots and declined linearly to 25% on shoots arising from the base of the previous year's shoot. The proportion of attacked buds from which larvae emerged declined non-linearly from 13.8% on the distal shoot to 3.5% on the basal shoots. The position of the shoot accounted for 67% and 73% of the variance in success of egg-laying and larval development, respectively.     

Selection ofAzolla forms resistant to the water lily aphid,Rhopalosiphum nymphaeae Life history of Rhopalosiphum nymphaeae

Genotypic and environmentally determined differences inSalix viminalis L. suitability forDasineura marginemtorquens (Bremi) (Diptera: Cecidomyiidae) growth and survival were investigated in laboratory and field experiments. Earlier studies have documented high neonate larval mortality on certainS. viminalis genotypes. Here we present results from laboratory experiments which show no difference in larval establishment behaviour on resistant and susceptible willow genotypes. These data indicate that larvae are not able to detect the plant characteristic responsible for resistance. In a field study insect performance was measured on willow shoots of dissmilar size. Adult body size was positively correlated to willow shoot length. In turn, body size was positively correlated to potential fecundity. These results are discussed in relation to observed high densities ofD. marginemtorquens in vigorously growing willows cultivated for biomass production.     

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.     

Vigour of a dioecious shrub and attack by a galling herbivore

1. The pattern of attack by the leaf‐galling insect Neopelma baccharidis (Homoptera: Psyllidae) was studied in three populations of the dioecious shrub Baccharis dracunculifolia (Asteraceae) in south‐eastern Brazil. The plant vigour hypothesis, which predicts higher rates of attack and increased herbivore performance on the longest plant shoots, was tested. This work also provides further information for the study of differential herbivory in dioecious plants. 2. In total, 9200 shoots were collected randomly from 46 male and 47 female plants belonging to the three populations. Shoot length, number of leaves per shoot, rate of galling, and survival of psyllids did not differ between male and female plants. Another population on the Campus of the Federal University of Minas Gerais was used only to determine the pattern of shoot growth. 3. The hypothesis of sex‐mediated herbivory was not corroborated in this study. 4. The frequency of galling increased with increasing shoot length, as predicted by the plant vigour hypothesis. Nevertheless, the number of oviposition sites (leaf buds) increased with shoot length. 5. The performance of the galling herbivore was not related to shoot length in the plant populations studied. 6. In conclusion, Neopelma baccharidis did not select shoots based on length only.     

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.     

Biotechnological methods of <Emphasis Type="Italic">in vitro</Emphasis> propagation in willows (<Emphasis Type="Italic">Salix</Emphasis> spp.)

Many populations of high-mountainous relic dioecious willows in Central Europe only consist of female individuals and are thus limited in their reproductive potential. We completed micropropagation experiments with shoot apexes and nodal segments of common and endangered willow (Salix) species, which can help to reintroduce autochthonous genotypes to their natural sites. Until recently, cultivation of green young shoot apexes of S. alba and S. lapponum showed the highest percentage of regeneration. We successfully applied the two-times-sterilisation due to high contamination of natural explants. The OK medium was the most efficient culture medium. In vitro propagation of willows with unisexual catkins, anther and ovule cultures were tested and optimised. Isolated anthers were cultivated on selected media and then microcallus and calluses of S. caprea and calluses of S. viminalis were formed on the A medium. Among various tested and optimised media for the ovule culture, the CP medium was the most efficient one. In this case, only the microcalluses of S. viminalis were observed. We developed biotechnological procedures that can be useful in conserving fragmented populations of high-mountainous willows.     

The parasitoid community of <Emphasis Type="Italic">Andricus quercuscalifornicus</Emphasis> and its association with gall size,phenology, and location

Plant galls are preyed upon by a diverse group of parasitoids and inquilines, which utilize the gall, often at the cost of the gall inducer. This community of insects has been poorly described for most cynipid-induced galls on oaks in North America, despite the diversity of these galls. This study describes the natural history of a common oak apple gall (Andricus quercuscalifornicus [Cynipidae]) and its parasitoid and inquiline community. We surveyed the abundance and phenology of members of the insect community emerging from 1234 oak apple galls collected in California’s Central Valley and found that composition of the insect community varied with galls of different size, phenology, and location. The gall maker, A. quercuscalifornicus, most often reached maturity in larger galls that developed later in the season. The parasitoid Torymus californicus [Torymidae] was associated with smaller galls, and galls that developed late in the summer. The most common parasitoid, Baryscapus gigas [Eulophidae], was more abundant in galls that developed late in the summer, though the percentage of galls attacked remained constant throughout the season. A lepidopteran inquiline of the gall (Cydia latiferreana [Tortricidae] and its hymenopteran parasitoid (Bassus nucicola [Braconidae]) were associated with galls that developed early in the summer. Parasitoids and inquilines, in general, had a longer emergence period and diapause within the gall than the gall-inducer. The association of different parasite species with galls of different size and phenology suggests that different parasite species utilize galls with slight differences in traits.     

Plant resistance, plant traits, and host plant choice of the leaf-folding sawfly on the arroyo willow

Abstract. 1. The hypotheses that genetic variation in host plant resistance of the arroyo willow affected leaf folder ( Phyllocolpa sp.) (Hymenoptera: Tenthredinidae) density and that genetic variation in shoot length and leaf length was correlated with resistance were tested.
2. Willows grown in pots and exposed to ovipojsition by the leaf folding sawfly in cages had significantly different densities among clones, indicating variation in resistance caused by genetic differences among conspecific host plants.
3. There was a general correspondence between leaf folder density on potted cuttings and on the plants in the field that were the sources of cuttings.
4. In behavioural choice experiments, susceptible clones (with highest leaf fold densities) had the highest oviposition activity of female leaf folders compared to clones that were resistant to the leaf folder.
5. Clones differed significantly in shoot length and leaf length among clones grown in pots, among clones in the field, and between shoots with galls and shoots without galls on clones in the field.
6. Leaf folder density was significantly positively correlated with mean shoot length on field clones in 1985 and 1986, but was not correlated with leaf length, although leaf length and shoot length were correlated.
7. Leaf length variation among willow clones accounted for a significant portion of the variation in resistance of potted willows, but shoot length was unimportant.