Heikki Roininen

Host Selection and Larval Performance of Two Willow-Feeding Sawflies

Host selection by ovipositing females and larval performance of two willowfeeding sawflies, Nematus salicis and N. pavidus, were investigated in laboratory choice and feeding experiments. In the field N. salicis is more specialized in its host utilization than N. pavidus, which is commonly found on a great number of willow species. In the Multiple Choice Oviposition Experiment females of both sawfly species exhibited a strong preference for one of six willow species offered. In No Choice Oviposition Experiments N. salicis retained its high selectivity while N. pavidus laid eggs equally on several willows. Host utilization spectra of larvae, as measured by larval growth and survival, were noticeably wider than those of ovipositing females. In N. salicis larval performance was optimal on willows that were also preferred by females, but in polyphagous N. pavidus conformity between host selection by ovipositing females and the larval performance was negligible. Host plant spectra of these sawflies are largely determined by behavior of ovipositing females and not by food utilization efficiency or survival of larvae. We suggest that host specialization of the sawflies studied has developed from behavioral processes of adults and is guided by specific plant characteristics such as phenolic glycosides in willow leaves. The physiological specialization of larvae may proceed more slowly and be secondary. In general we emphasize the role of behavioral constraints and adaptations in the ecology and evolution of host utilization by herbivorous insects.

EVOLUTION OF GALL MORPHOLOGY AND HOST-PLANT RELATIONSHIPS IN WILLOW-FEEDING SAWFLIES (HYMENOPTERA: TENTHREDINIDAE)

Abstract.— There are over 200 species of nematine sawflies that induce galls on willows (Salix spp.). Most of the species are monoor oligophagous, and they can be separated into seven or eight different groups based on the type of gall that they induce. We studied the evolution of different gall types and host plant associations by reconstructing the phylogeny of five outgroup and 31 ingroup species using DNA sequence data from the mitochondrial cytochrome b gene. Maximum‐parsimony and maximum‐likelihood analyses resulted in essentially the same phylogeny with high support for important branches. The results show that: (1) the galling species probably form a monophyletic group; (2) true closed galls evolved only once, via leaf folders; (3) with the possible exception of leaf rollers, all gall type groups are mono‐ or paraphyletic; (4) similar gall types are closer on the phylogeny than would be expected by a random process; (5) there is an apparent evolutionary trend in galling site from the leaf edge towards the more central parts of the host plant; and (6) many willow species have been colonized several times, which excludes the possiblity of parallel cladogenesis between willows and the gallers; however, there are signs of restrictions in the evolution of host use. Many of the patterns in the evolutionary history of nematine gallers have also been observed in earlier studies on other insect gallers, indicating convergent evolution between the independent radiations.

Response of galling insects to natural browsing by mammals in Alaska

Along the Tanana River, near Fairbanks, Alaska, natural browsing by the snowshoe hare, Lepus americanus, and moose, Alces alces, pruned back growth and resulted in resprouting of more juvenile growth in host plants. This resulted in longer leading shoots of stems in young trees of Populus balsamifera and ramets of the shrub, Salix novae-angliae, both species in the family Salicaceae. Total numbers of shoots were the same on uncaged and caged plots, the latter excluding moose and snowshoe hare, but the ramets of Salix novae-angliae were slightly younger on uncaged plots, indicating that dieback of older ramets accelerated under natural browsing. The most common herbivores in August 1993 were two leaf-folding sawfly species in the genus Phyllocolpa (Hymenoptera: Tenthredinidae). Densities of the two Phyllocolpa species, one on Populus balsamfera and one on Salix novae-angliae, were 83 and 85% higher on ramets or stems in uncaged plots. Also, the combined number of other rarer galling species were higher in browsed, uncaged plots. Mean length of leading shoots in ramets and stems accounted for 35 and 30% of variation in densities of Phyllocolpa species on Populus balsamifera and Salix novae-angliae in plots, respectively. Thus, the increased galling insect densities are accounted for as far as our studies permit by increased vigor of host plants indicated by shoot length. On Salix novae-angliae also faster dieback of older senescent ramets may have an important effect on the resource quality for gallers.

Oviposition Stimulant for a Gall-Inducing Sawfly, Euura lasiolepis, on Willow is a Phenolic Glucoside

The ovipositional stimulation for the shoot galling sawfly, Euura lasiolepis, whose natural host is the North American willow, Salix lasiolepis, was studied in response to its original host, Finnish willows, poplar species, and individual phenolic glucosides and fractions. The major phenolic glucosides in the natural host were salicortin and tremulacin, which were also the major components in the Finnish S. purpurea and S. rosmarinifolia. The natural host, S. lasiolepis, was chosen over six Finnish willow species in multiple-choice tests. Multiple-choice tests with six Finnish willow species and one Finnish popular species showed that S. rosmarinifolia was significantly more attractive than any of the other species by at least 16-fold. No-choice testing with phenolic glucosides showed the tremulacin fraction to be the significant ovipositional stimulant, which elicited probes with the ovipositor at least 19 times more frequently than other glucosides. A tremulacin fraction at 1.5% elicited significantly more probes than a tremulacin fraction tested at 0.4%. In addition, tremulacin was the only glucoside to induce prolonged and repeated probing with the ovipositor, lasting a mean of 6.4 sec per bout per female. Only single probes lasting a fraction of a second were observed in response to other glucosides. This is the second study showing a direct effect of a phenolic glucoside as an ovipositional stimulant for a sawfly, and it also suggests the existence of a mechanism that enables females to respond positively in a graded way to shoot length heterogeneity in host plants and populations.

Importance of phenolic glucosides in host selection of shoot galling sawfly,Euura amerinae, onSalix pentandra

The effects of phenolic glucosides on the oviposition behavior ofEuura amerinae L. (Hymenoptera: Tenthredinidae) were tested in multiple oviposition experiments using different shoot length categories ofSalix pentandra L. (with different amounts of phenolic glucosides) and in experiments with pure phenolic glucosides (salidroside, arbutin, salicin, 90% salicortin, 90% 2′-O-acetylsalicortin) or composite total fractions of phenolic glucosides from three willow species (S. pentandra, S. myrsinifolia Salisb.,S. triandra L.). This was the first time that the effects of pure phenolic glucosides on the oviposition behavior of sawfly species were tested. Total fraction of phenolic glucosides fromS. pentandra and its main individual glucoside, 2′-O-acetyl-salicortin, stimulated the strongest ovipositional behavior inE. amerinae. The results show clearly that females ofE. amerinae can recognize and choose their host willow,S. pentandra, on the basis of phenolic glucosides. Moreover, they are probably able to use phenolic glucosides as a cue in shoot selection within host-plant individuals.

THE EVOLUTION OF HOST-PLANT USE AND SEQUESTRATION IN THE LEAF BEETLE GENUS PHRATORA (COLEOPTERA: CHRYSOMELIDAE)

Leaf beetles in the genus Phratora differ in host plant use and in the chemical composition of their larval defensive secretion. Most species specialize on either poplars or willows (family Salicaceae), but two species feed on birch (family Betulaceae). Phratora vitellinae utilizes salicylates from the host plant to produce its larval secretion, which contains salicylaldehyde, while other Phratora species produce an autogenous secretion. To reconstruct the evolutionary history of host plant use and the larval secretion chemistry in this genus, we sequenced 1383 base pairs of the mt cytochrome oxidase I gene for six European and one North American Phratora species and three outgroup taxa. Bootstrap values of the complete nucleotide sequence were 99‐100% for six of eight nodes in the maximum parsimony tree. They were 71% and 77% for the two other nodes. The maximum parsimony tree and the maximum likelihood tree based on nucleotide sequence showed the same relationships as a maximum parsimony tree based on the amino acid sequence. Beetle phylogeny overlapped broadly with host plant taxonomy and chemistry, and it revealed historical constraints influencing host plant use. However, there was one host shift from the willow family (Salicaceae) to the birch family (Betulaceae). The use of host plant phenol glycosides for the larval defensive secretion evolved along the lineage that led to P. vitellinae. Phratora vitellinae feeds on the taxonomically widest range of host plants, which are characterized by moderate to high levels of salicylates. The results support the hypothesis that the use of salicylates for the larval secretion evolved twice independently in chrysomeline leaf beetles.

The effects of reindeer grazing on the composition and species richness of vegetation in forest–tundra ecotone

We conducted an 8-year exclosure experiment (1999–2006) in a forest–tundra ecotonal area in northwestern Finnish Lapland to study the effects of reindeer grazing on vegetation in habitats of variable productivity and microhabitat structure. The experimental sites included tundra heath, frost heath and riparian habitats, and the two latter habitats were characterized by hummock-hollow ground forms. The total cover of vegetation, cover of willow (Salix spp.), dwarf birch (Betula nana), dwarf shrubs, forbs and grasses (Poaceae spp.) increased in exclosures in all habitats. The increase in the total cover of vegetation and in the covers of willow and dwarf birch tended to be greatest in the least productive tundra heath. Opposing to the increase in the dominant vascular plant groups, the cover and species number of bryophytes decreased in exclosures. We conclude that the effects of reindeer grazing on vegetation composition depend on environmental heterogeneity and the responses vary among plant groups.

Host preference and allozyme differentiation in shoot galling sawfly, Euura atra

Adaptive responses to various plant species may be a primary mechanism that leads to the formation of host races or sibling species among plant-feeding insects(Bush, 1969, 1975;Price and Willson, 1976;Wood, 1980; Guttman et aI., 1981; Futuyma, 1983, 1986). Resource-associated genetical (Diehl and Bush, 1984; Futuyma and Peterson, 1985, and references therein; Pashley, 1988; Feder et al., 1988; Waring et al., 1990) and behavioral (Feder and Bush, 1989; Tauber and Tauber, 1989, and references therein) differentiation of sympatric populations of phytophagous insect species has been observed. Several factors alone or in combination can be responsible for this differentiation: I) postmating reproductive isolation between the host races, 2) genetic bottlenecks in the founding of new host races, 3) different larval survival on different host plants, 4) differences in the host recognition of adults, or 5) temporal differences in the emergence of adults (see Feder et aI., 1988). Local populations of phytophagous insects associated with certain plant species are often highly specialized in their food selection (e.g., Tauber and Tauber, 1989). A common explanation to such specificity is that behavior is molded by selection to fit the conditions of optimal larval performance. However, a physiological trade-offhas not been observed generally among different host races of insects (Wasserman and Futuyma, 1981; Futuyma et al., 1984; Fitt, 1986; Hare and Kennedy, 1986; Futuyma and Philippi, 1987; Prokopy et al., 1988). An alternative explanation is that local populations at first differentiate their host recognition behavior and the physiological differentiation takes place secondarily later on (Futuyma, 1983, 1986). This hypothesis is supported by studies that have shown

Bottom-up and top-down influences in the trophic system of a willow, a galling sawfly, parasitoids and inquilines

Strong bottom-up effects dominated the trophic system of the host plant, Salix pentandra, the specialist galling sawfly ; Euura amerinae, inquilines in the genus Eurytoma and the most common parasitoid attacking both genera of herbivores, Pteromalus. capreae. A young willow population provided the basic resources for the second and third trophic levels, and the inquilines and parasitoid species showed strong positive, but density-independent, responses to food supply. Colonized trees ranged from 3 to 7 years old in 1989, and the Euura population had increased by 1991, declined significantly by 1992, and went almost extinct in 1994. The sex ratio declined steadily from 1989 to 1992. Populations of Eurytoma and Pteromalus tracked their resources closely, without influencing the major aspects of Euura population change dictated by availability of young trees and the rapid development of host resistance correlated with tree age. Trees continuously colonized by Euura from before 1989 to 1992 were much more favorable to both higher trophic levels than trees colonized for the first time between 1989 and 1992, indicating the importance of host heterogeneity in the system. Overall, effects from the host plant up the trophic system were very much stronger than the effects of carnivores down the food web.

Chapter 16 – Working toward Theory on Galling Sawfly Population Dynamics

This chapter discusses the theory on galling sawfly population dynamics. If theory is considered to be a factually and empirically based mechanistic explanation of pattern in nature, then there is little in the field of population dynamics. Adults emerge in the spring and mate, and females oviposit into rapidly growing young willow shoots with their sawlike ovipositor. As willow ramets age they produce shoots of decreasing length, becoming less and less susceptible to sawfly attack. Attraction of females to long shoots is not accounted for by protein concentration in shoots or total phenolics concentrations. Long shoots have higher concentrations of certain phenolic glycosides than do short shoots, especially tremulacin and salicortin. An unusual feature of these galling sawflies is that they modify resources to the advantage of individuals in the same generation and in subsequent generations. The carnivores in the system that kill Euura larvae have a generally weak impact, and do not help to explain population variation from clone to clone, or from year to year. All species of Euura sawflies attack woody plants, and all have similar life histories. Trees pass rapidly through a phase that is susceptible to stem-galling sawflies, making the population dynamics of gallers predictable, but unstable. Another hypothesis that is tested repeatedly is the plant vigor hypothesis. As the hypothetical framework expands, the demands for testing hypotheses increases, which rapidly becomes time-consuming and costly. As the research scope broadens, there is a remarkable reluctance among funding agencies to foot the bill.