Change search
ReferencesLink to record
Permanent link

Direct link
Trophic, Indirect, and Evolutionary Interactions in a Plant–Herbivore–Parasitoid System
Umeå University, Faculty of Science and Technology, Ecology and Environmental Science.
2008 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The aim of this thesis project was to elucidate patterns and processes associated with the biotic interactions in a natural plant–herbivore–parasitoid food web characterized by spatial and temporal heterogeneity with regard to species composition.

The system examined is based on island populations of the perennial herb Meadowsweet (Filipendula ulmaria, Rosaceae), located in the Skeppsvik Archipelago. The area is subject to isostatic rebound, amounting to 0.85 cm per year; this makes it possible to calculate the age of the rising islands. Meadowsweet colonizes new islands when they are about 100 years old.

Meadowsweet is consumed by two major herbivores in the study area: Galerucella tenella and Altica engstroemi (Coleoptera: Chrysomelidae). Both herbivores overwinter in the topsoil and successful colonization occurs when the islands reach a height that prevents the beetles from being removed or killed as a result of wave wash during the winter. I found that both herbivores significantly reduced individual plant fitness and population growth rate. A “cafeteria experiment” with Galerucella showed that this beetle discriminated between plants from different islands, avoiding plants from old islands which contained high concentrations of putative defence compounds, while readily accepting plants from younger islands which contained lower concentrations of these chemicals. Further, the plant species exhibited a trade-off between growth and production of the putative defence compounds. Taken together, these results were interpreted as providing evidence of herbivore-driven evolution of resistance in Meadowsweet. Further, laboratory studies suggested that Galerucella gradually includes a less preferred host plant (Rubus arcticus, Rosaceae) in its diet as Meadowsweet resistance increases. This implies that Galerucella drives its own host-breadth enlargement by selectively inducing a ‘rent rise’ in the original host, Meadowsweet.

In a number of field studies I showed that the oligophagous parasitoid Asecodes mento (Hymenoptera: Eulophidae) has a strong positive effect on Meadowsweet seed set by removing large numbers of G. tenella larvae. This top-down effect is, however, altered by the presence of a close relative of G. tenella, namely G. calmariensis, which is monophagous on Purple loosestrife (Lythrum salicaria, Lythraceae). G. tenella experiences associational susceptibility when coexisting with G. calmariensis since the latter supports a higher and more fit pool of shared parasitoids and because Meadowsweet attracts a higher proportion of the shared parasitoid females than Purple loosestrife. This implies that G. tenella densities are very low in coexisting populations and that Meadowsweet experiences associational resistance and produces more seeds when co-occurring with Purple loosestrife. Thus, selection for increased resistance in Meadowsweet is likely to be relaxed in populations mixed with Purple loosestrife.

I conclude that the evolution of plant resistance is likely to depend on the length of time and intensity of selection. When Meadowsweet colonizes new islands it experiences a period of enemy-free space; followed by a midlife and ageing with selection by herbivores. The intensity of this selection does, however, depend on the presence of additional plant and herbivore species.

Place, publisher, year, edition, pages
Umeå: Ekologi, miljö och geovetenskap , 2008. , 16 p.
Keyword [en]
Plant resistance, coevolution, herbivory, Skeppsvik, food web, parasitism, maternal effect, natural selection, Filipendula ulmaria, Chrysomelidae
National Category
URN: urn:nbn:se:umu:diva-1490ISBN: 978-91-7264-469-4OAI: diva2:141234
Public defence
2008-02-08, Lilla hörsalen, KBC, Umeå universitet, Umeå, 10:00 (English)
Available from: 2008-01-18 Created: 2008-01-18 Last updated: 2009-07-03Bibliographically approved
List of papers
1. Insect herbivory controlled plant fitness and population growth in a 16-year study of Meadowsweet populations
Open this publication in new window or tab >>Insect herbivory controlled plant fitness and population growth in a 16-year study of Meadowsweet populations
(English)Manuscript (preprint) (Other (popular science, discussion, etc.))
urn:nbn:se:umu:diva-2900 (URN)
Available from: 2008-01-18 Created: 2008-01-18 Last updated: 2010-01-14Bibliographically approved
2. Tall herb herbivory resistance reflects historic exposure to leaf beetles in a boreal archipelago age-gradient.
Open this publication in new window or tab >>Tall herb herbivory resistance reflects historic exposure to leaf beetles in a boreal archipelago age-gradient.
2006 (English)In: Oecologia, ISSN 0029-8549, Vol. 148, no 3, 414-425 p.Article in journal (Refereed) Published
Abstract [en]

In this paper, we introduce the coevolution-by-coexistence hypothesis which predicts that the strength of a coevolutionary adaptation will become increasingly apparent as long as the corresponding selection from an interacting counterpart continues. Hence, evolutionary interactions between plants and their herbivores can be studied by comparing discrete plant populations with known history of herbivore colonization. We studied populations of the host plant, Filipendula ulmaria (meadow sweet), on six islands, in a Bothnian archipelago subject to isostatic rebound, that represent a spatio-temporal gradient of coexistence with its two major herbivores, the specialist leaf beetles Galerucella tenella and Altica engstroemi. Regression analyses showed that a number of traits important for insect-plant interactions (leaf concentrations of individual phenolics and condensed tannins, plant height, G. tenella adult feeding and oviposition) were significantly correlated with island age. First, leaf concentrations of condensed tannins and individual phenolics were positively correlated with island age, suggesting that plant resistance increased after herbivore colonization and continued to increase in parallel to increasing time of past coexistence, while plant height showed a reverse negative correlation. Second, a multi-choice experiment with G. tenella showed that both oviposition and leaf consumption of the host plants were negatively correlated with island age. Third, larvae performed poorly on well-defended, older host populations and well on less-defended, younger populations. Thus, no parameter assessed in this study falsifies the coevolution-by-coexistence hypothesis. We conclude that spatio-temporal gradients present in rising archipelagos offer unique opportunities to address evolutionary interactions, but care has to be taken as abiotic (and other biotic) factors may interact in a complicated way.

Animals, Beetles/growth & development/*physiology, Cold Climate, Ecosystem, Evolution, Feeding Behavior, Filipendula/chemistry/*parasitology/*physiology, Geography, Larva/growth & development, Sweden
urn:nbn:se:umu:diva-6242 (URN)10.1007/s00442-006-0390-7 (DOI)16502319 (PubMedID)
Available from: 2007-12-07 Created: 2007-12-07Bibliographically approved
3. Herbivore-induced "rent rise" in the host plant may drive a diet breadth enlargement in the tenant.
Open this publication in new window or tab >>Herbivore-induced "rent rise" in the host plant may drive a diet breadth enlargement in the tenant.
2008 (English)In: Ecology, ISSN 0012-9658, Vol. 89, no 1, 126-133 p.Article in journal (Refereed) Published
Abstract [en]

Inter- and intraspecies variations in host plant traits are presumably involved in many host shifts by insect herbivores, and elucidating the mechanisms involved in such shifts has been a crucial goal in insect-plant research for several decades. Here we propose that herbivore-induced evolutionary increases in host plant resistance may cause oligophagous insect herbivores to shift to other sympatric plants as currently preferred host plants become increasingly unpalatable. We tested this hypothesis in a system based on the perennial herb Filipendula uhnaria (Rosaceae), whose herbivory defense has become gradually stronger due to prolonged selection by Galerucella tenella (Coleoptera: Chrysomelidae) herbivory in a boreal archipelago. We. show that Galerucella gradually increases its use of the alternative host plant Rubus arcticus (Rosaceae) in parallel to gradually increased resistance in Filipendula. Our results imply that, by driving the evolutionary increase in Filipendula resistance, Galerucella is also gradually making the original host species more unpalatable and thereby driving its own host-breadth enlargement. We argue that such self-inflicted "rent rises" may be an important mechanism behind host plant shifts, which in turn are believed to have preceded the speciation of many phytophagous insects.

Animals, Beetles/growth & development/*physiology, Biodiversity, Ecosystem, Evolution, Feeding Behavior/*physiology, Filipendula/*parasitology/*physiology, Host-Parasite Interactions, Population Dynamics, Species Specificity
urn:nbn:se:umu:diva-11440 (URN)doi:10.1890/07-0252.1 (DOI)18376554 (PubMedID)
Available from: 2009-01-08 Created: 2009-01-08Bibliographically approved
4. Asymmetric indirect interactions mediated by a shared parasitoid: connecting species traits and local distribution patterns for two chrysomelid beetles
Open this publication in new window or tab >>Asymmetric indirect interactions mediated by a shared parasitoid: connecting species traits and local distribution patterns for two chrysomelid beetles
2006 (English)In: Oecologia, ISSN 0029-8549, Vol. 148, no 3, 475-481 p.Article in journal (Refereed) Published
Abstract [en]

This paper reports on an asymmetric indirect interaction between two chrysomelid beetles where one species (Galerucella tenella) experiences higher parasitization, and the other species (Galerucella calmariensis) lower parasitization, in mixed compared with monospecific populations. This pattern is likely to be a consequence of differences in life history characteristics, where the inferior species has a smaller body size, a lower fecundity and supports a lower parasitoid density than the superior species. This connection between life history characteristics and interspecific dominance in host–parasitoid systems corresponds to predictions from current community ecology theory, and provides a useful building-block in the development of a predictive theory of parasitoid effects on host coexistence.

Asecodes, Community theory, Galerucella, Host–parasitoid interactions
urn:nbn:se:umu:diva-7421 (URN)10.1007/s00442-006-0387-2 (DOI)
Available from: 2008-01-09 Created: 2008-01-09Bibliographically approved
5. Presence of Lythrum salicaria enhances the bodyguard effects of the parasitoid Asecodes mento for Filipendula ulmaria
Open this publication in new window or tab >>Presence of Lythrum salicaria enhances the bodyguard effects of the parasitoid Asecodes mento for Filipendula ulmaria
2007 (English)In: Oikos, ISSN 0030-1299, Oikos, Vol. 116, no 3, 482-490 p.Article in journal (Refereed) Published
Abstract [en]

This paper reports significant effects of a co-occurring plant species (Lythrum salicaria, Lythraceae) on the reproductive success of the perennial herb Filipendula ulmaria (Rosaceae). We studied 15 Filipendula populations in the Skeppsvik Archipelago; seven of which were monospecific and eight mixed with Lythrum. All the Filipendula populations studied harbored the chrysomelid beetle Galerucella tenella, and in 2005 seed set was strongly negatively correlated with the percentage leaf area consumed. Moreover, data from 2004 showed that 25–100% of the G. tenella larvae were parasitized by the hymenopteran parasitoid Asecodes mento, and we found a strong cascading top-down effect of parasitism in 2004 on Filipendula seed set in 2005. In 2004, parasitism (at the population level) was negatively correlated with percentage leaf area consumed and positively correlated with seed set in 2005. The parasitoid Asecodes also parasitized G. calmariensis, which is monophagous on Lythrum. Mixed populations of Filipendula and Lythrum supported higher densities of their shared ‘bodyguard’Asecodes. Further, Y-tube bioassays showed that floriferous Filipendula attracted more than twice as many gravid Asecodes females as floriferous Lythrum. Taken together, these findings suggest that coexistence of the two plants results in ‘associational resistance’ for Filipendula and ‘associational susceptibility’ for Lythrum. This scenario was supported for Filipendula since, for this species, we found lower leaf consumption followed by higher seed production in mixed than in monospecific populations. Considered together, our results show that bodyguards may increase the reproductive fitness of a perennial herb, and that the strength of the cascading ‘bodyguard’ effect can be strongly influenced by co-occurring plants through ‘apparent competition’. This is the first paper to demonstrate that, in the wild, plant species may use odors to compete for ‘bodyguards’, thereby causing asymmetrical ‘apparent competition’ between the herbivores involved. Our data emphasize the need to consider community factors in studies of trophic interactions.

urn:nbn:se:umu:diva-11941 (URN)doi:10.1111/j.0030-1299.2007.15357.x (DOI)
Available from: 2007-03-16 Created: 2007-03-16Bibliographically approved

Open Access in DiVA

fulltext(102 kB)352 downloads
File information
File name FULLTEXT01.pdfFile size 102 kBChecksum MD5
Type fulltextMimetype application/pdf

Search in DiVA

By author/editor
Stenberg, Johan
By organisation
Ecology and Environmental Science

Search outside of DiVA

GoogleGoogle Scholar
Total: 352 downloads
The number of downloads is the sum of all downloads of full texts. It may include eg previous versions that are now no longer available

Total: 489 hits
ReferencesLink to record
Permanent link

Direct link