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Adaptive Radiation Into Ecological Niches with Eruptive Dynamics: A

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Adaptive Radiation Into Ecological Niches with Eruptive Dynamics: A Journal of Animal Blackwell Publishing, Ltd. Ecology 2005 Adaptive radiation into ecological niches with eruptive 74, 397–408 dynamics: a comparison of tenthredinid and diprionid sawflies PETER W. PRICE*, HEIKKI ROININEN†§ and TAKAYUKI OHGUSHI‡ *Northern Arizona University, Department of Biological Sciences, Flagstaff, Arizona 86011–5640, USA; †Vantaa Research Centre, Finnish Forest Research Institute, PO Box 18, 01301 Vantaa, Finland; and ‡Center for Ecological Research, Kyoto University, Kamitanakami, Hirano-cyo, Otsu 520–2113, Japan Summary 1. We tested the hypothesis that the bottom-up influence of coniferous plant resources promotes the probability of outbreak or eruptive dynamics in sawflies. The literature was examined for three geographical regions − North America north of Mexico, Europe and Japan. 2. In each region tenthredinid sawflies (Hymenoptera: Tenthredinidae) were signifi- cantly more likely to be eruptive on conifers than on angiosperms. 3. The diprionid sawflies (Hymenoptera: Diprionidae) that attack conifers exclusively showed a significantly higher probability of eruptive dynamics than the tenthredinid sawflies on angiosperms in two regions, North America and Europe, and in Japan the trend was in the same direction. 4. The probability of species showing eruptive dynamics on coniferous hosts was not significantly different among tenthredinids and diprionids on conifers in North America, Europe and Japan. 5. The weight of evidence supports the hypothesis of conifers supporting a higher per- centage of eruptive species than angiosperms. 6. In the adaptive radiation of tenthredinid sawflies from flowering plants onto conifers, larches (Larix) appear to be particularly favourable for colonization, but pines (Pinus) have not been colonized in any region, a pattern likely to be explained by the growth characteristics of the host plants. 7. Among tenthredinid species in Europe, where sawfly/host relationships are best known, there is a significant trend for an increasing proportion of outbreaking species from herbs, to shrubs, to trees. 8. The results indicate for the first time the strong bottom-up effects of plant resources on the population dynamics of sawflies, involving general features of host plant taxa and growth characteristics. Key-words: Diprionidae, Hymenoptera, insect herbivore population dynamics, plant resources, Tenthredinidae. Journal of Animal Ecology (2005) 74, 397–408 doi: 10.1111/j.1365-2656.2005.00935.x eruptive population dynamics, while others are more Introduction latent in their dynamics. Even within the same insect During the process of adaptive radiation some species family and genus, some species may be outbreak species appear to enter into ecological niches that result in while others remain uncommon or rare in their communities (cf. Hunter 1991, 1995a). For example, no Correspondence: Peter W. Price, Department of Biological family of forest moths (Macrolepidoptera) includes Sciences, Northern Arizona University, Flagstaff, Arizona 86011–5640, USA. Fax: (928) 523 7500; 100% of outbreaking species, or 100% of non-out- E-mail: [email protected] breaking species. And, while species that are well © 2005 British §Present address: Department of Biology, University of Joensuu, defended against natural enemies and/or are gregarious, Ecological Society PO Box 111, 80101 Joensuu, Finland. are well represented in the outbreaking species, these 398 traits are not present in all the outbreaking species precise placement of eggs into the plant substrate. P. W. Rice, (Hunter 1991, 1995a). Other characters associated fre- Therefore, according to the Phylogenetic Constraints H. Roininen & quently with eruptive dynamics are spring feeding, high Hypothesis (Price et al. 1990; Price 2003) we may T. Ohgushi fecundity, polyphagy, clustering of eggs and reduced expect the same kinds of population dynamics, but this dispersal ability (Wallner 1987; Haack & Mattson is clearly not the general case. 1993; Larsson, Björkman & Kidd 1993; Hunter 1995a,b). We test the hypothesis that it is the host plant type Therefore, valuable insights may be gleaned from an that results in different population dynamics, with examination of additional factors that might contribute angiosperm hosts resulting in more latent dynamics, to patterns of dynamics in herbivorous insects. In and conifer hosts producing a higher probability of particular, the resources utilized by herbivores have not eruptive population dynamics. We test this hypothesis been emphasized in the search for patterns in eruptive by examining the dynamics of tenthredinid sawflies species population dynamics. that have colonized conifers. If plant resources are the The sawflies (Hymenoptera: Symphyta) show similar basis for bottom-up dynamics in diprionid sawflies, mixing of outbreak and latent dynamics within families they should play a similar role in the dynamics of ten- and genera as in the Macrolepidoptera (Hanski & thredinid sawflies on conifers. Unfortunately, the recip- Otronen 1985; Hanski 1987; Haack & Mattson 1993; rocal test is not available because no pine sawflies have Larsson et al. 1993; Hunter 1995a); but a clear phylo- colonized angiosperms (Smith 1979; Haack & Mattson genetic difference exists between the tenthredinid 1993; Larsson et al. 1993). Therefore, in this paper we sawflies (Tenthredinidae), with a relatively small per- ask the question: in the adaptive radiation of the ten- centage of outbreak species, and the diprionid sawflies thredinid sawflies, has the new adaptive zone of conifer (Diprionidae), with a high number of outbreak species feeding resulted in a higher probability of eruptive (Haack & Mattson 1993; Price 2003). In North America, population dynamics than on the angiosperms? In the for example, about 3% of tenthredinids on angiosperms discussion we consider a mechanistic hypothesis to were estimated to be eruptive species, while 40% of dip- explain the shift in dynamics. We were also interested in rionids on conifers were calculated as outbreak species the kinds of conifer species utilized by tenthredinids (Price 2003). The adaptive radiation of the tenthredi- when compared to diprionids, which may reveal limits nid sawflies has centred on the angiosperms and that on the scope of their radiation onto conifers. of diprionid sawflies has been on conifers. Does this major distinction in resources utilized play a role in dif- Methods ferent frequencies of eruptive population dynamics? The tenthredinids and diprionids are regarded The tenthredinid and diprionid sawflies have radiated by some as sister families (e.g. Gauld & Bolton 1996; mainly in the northern hemisphere, especially in cool Schulmeister 2003), or perhaps the diprionids con- temperate climates. Therefore, we chose for study three stitute a subfamily of the Tenthredinidae (Rasnitsyn geographical regions with relatively well-known sawfly 1980), or are at least nested within the tenthredinids faunas, host plant records and characteristics of popu- (Schulmeister, Wheeler & Carpenter 2002). Vilhelmsen’s lation behaviour: North America north of Mexico, (2001) hypothesis showed that tenthredinids were more Europe and Japan. For each region we searched the basal in the phylogeny than diprionids, from which we literature to find the number of sawfly species in the can conclude that angiosperm feeding evolved before common and pine sawflies, the numbers recorded as conifer feeding. Indeed, the superfamily Tenthredinoidea, outbreak or pest species and, for the tenthredinids, the including both tenthredinid and diprionid sawflies, is number of species on herbs, grasses and ferns, shrubs, thought to have radiated in the late Cretaceous, co- angiosperm trees and gymnosperm (= coniferous) trees. incident with the radiation of the angiosperms (Gauld We accepted designations as outbreak or pest species & Bolton 1996). Therefore, during the radiation of the provided in the literature. Outbreak species are com- tenthredinoid group, expansion was perhaps first on monly recognized in the forestry literature, which was angiosperms, followed by colonization of a new adap- employed by Haack & Mattson (1993) and Larsson tive zone on conifers. However, because conifers were et al. (1993) to summarize outbreak history for sawflies present long before angiosperms radiated, the lineages in North America and Europe. In addition, we used of tenthredinid and diprionid sawflies may not differ sources that noted garden, agricultural and orchard much in age, suggesting equal opportunity for radi- pests, which contributed to the list of sawflies on herbs ation. Gauld & Bolton (1996, p. 95) suggest that the and grasses, shrubs and other woody growth (e.g. for tenthredinoids ‘may have been the dominant exophytic North America: Westcott 1973; Hill 1987; Arnett 1993; leaf-eating group of insects’ during the Palaeocene and Metcalf & Metcalf 1993). The term ‘pest species’ has Eocene, as the Macrolepidoptera did not radiate until been used commonly in the literature on small-plot the Oligocene. Hence, radiation could proceed appar- agriculture and gardens, in situations where angiosperm © 2005 British ently unimpeded by significant competition. herbs and shrubs are commonly grown. We have Ecological Society, Journal of Animal The tenthredinid and diprionid sawflies share a com- accepted the designation in the literature as a pest spe- Ecology, 74, mon phylogenetic heritage, with similar morphology cies as a criterion for including with outbreak species in 397–408 of the ovipositor for laying eggs into plant tissue, and order to capture
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