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Interactions between natural enemies and the dioecious herb Silene dioica
Umeå University, Faculty of Science and Technology, Ecology and Environmental Science. (Evolutionär ekologi)
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

About 6% of all angiosperms are dioecious. This separation of sexual function to male and female individuals, and the fundamentally different patterns of reproductive resource allocation that follows that separation, are thought to have important ecological and evolutionary consequences for plant enemy interactions.  I have studied whether intersexual differences in susceptibility to natural enemies can be explained by intersexual differences in resource allocation. In cases when sexual dimorphic traits form the target resource of a particular enemy I expected the enemy to select the best resource.

The study system is the perennial dioecious herb, Silene dioica (Caryophyllaceae) and three of its specialist natural enemies, two insect herbivores the fly Delia criniventris (Anthomyiidae) and the twirler moth Caryocolum viscariella (Gelechiidae) and one systemic anther smut fungus Microbotryum violaceum. All three share the same food recourse, the floral stems, of their host plant. I studied the interaction on nine islands in a rising Bothinan archipelago over seven consecutive years.

Both herbivores attacked female plants more than male plants (D. criniventris, 32.8% females, 30.7% males; C. viscariella, 4% females, 2% males). This attack pattern was consistent over years and islands and also correlated with a number of sexually dimorphic traits suggesting that females offer the better resource.

Herbivore attack had no effect on plant survival but a significant effect on re-flowering the following year. Non-attacked females had an estimated mean re-flowering rate of 30.2%, and non-attacked males of 31%. Herbivore-attacked females had an estimated re-flowering rate of 46% compared with 38.4% for males. Females showed a stronger compensatory response to attack and tended to re-flower more often than males.

Attack rates differed markedly in the different stages of primary succession. They were consistently higher in the youngest zone and decreased in parallel to progressing succession. This zonal pattern of decreasing attack rates correlated with several plant attributes, a decrease in plant size and nitrogen content, and an increased content of secondary compounds, but not to host plant density. We failed to come up with a simple explanation for the spatial structure with chronic high attack rates in the younger zones. However, the consistent patterns in attack rate suggest that a suite of abiotic and biotic factors interact and reinforce the strength and direction of selection.

In general females were more frequently diseased by the anther smut Microbotryum violaceum than males with two exceptions. Disease frequencies were male biased on islands with low disease levels and in one of the seven study years. The change in disease frequencies from male to female bias confirm earlier studies suggesting that the relative contribution of the two components of infection risk, disease encounter and per contact infection probability can vary with population disease level. The change in the proportions of diseased males and females that was observed in one of the study years, followed a year of extreme weather conditions (prolonged drought). Both sexes showed a similar decline in flowering but diseased females decreased more than diseased males. This difference in response can be explained if considering that disease is more resource demanding in females than in males. Except for resources needed for mycelial growth and spore production, in females resources are also needed to restructure their sex expression and produce anthers.

My study shows (i) that in dioecious species traits that are sexually dimorphic are of great importance for understanding the outcome of interactions with natural enemies, (ii) that the strengths and directions of enemy-host plant interactions are strongly shaped by both biotic and abiotic conditions.

Place, publisher, year, edition, pages
2009. , 41 p.
Keyword [en]
Silene dioica, Delia criniventris, Caryocolum viscariella, Microbotryum violaceum, plant-herbivore interactions, plant -pathogen interactions, sex bias, sex rato, successional gradients, fitness effects, Skeppsvik Archipelago
National Category
Ecology
Research subject
Ecological Botany
Identifiers
URN: urn:nbn:se:umu:diva-20989ISBN: 978-91-7264-769-5 (print)OAI: oai:DiVA.org:umu-20989DiVA: diva2:210263
Public defence
2009-04-25, Stora hörsalen (KB3B1), KBC, Linnaeus väg 6, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2009-04-03 Created: 2009-03-31 Last updated: 2009-04-03Bibliographically approved
List of papers
1. Sex-biased herbivory in Silene dioica.: Which sex is the better resource?
Open this publication in new window or tab >>Sex-biased herbivory in Silene dioica.: Which sex is the better resource?
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(English)Manuscript (Other academic)
Abstract [en]

In cases when sexual dimorphic traits form the target resource of a particular herbivore we would expect the herbivore to select the best resource. We studied the interaction between to specialist insect herbivores Delia criniventris and Caryocolum viscariella that share the same food resource, the floral stems, of their host plant the perennial and dioecious herb, Silene dioica. We studied the interaction on nine islands in a Bothinan archipelago over seven consecutive years. Both herbivores attacked female plants more than male plants (D. criniventris, 32.8% females, 30.7% males; C. viscariella, 4% females, 2% males). The pattern was consistent over years and islands. We also found a number of sexually dimorphic traits suggesting females to be the better resource. We have presented evidence that female-biased herbivory does occur in dioecious plants and, as with male-biased herbivory, it may occur because herbivores utilise the better resource which will vary depending upon feeding strategy. We conclude that in dioecious species we need identify the dimorphism responsible for the sex sustaining the greatest attack rates and avoid being blinded by the expectation of male herbivory.

National Category
Ecology
Research subject
Ecological Botany
Identifiers
urn:nbn:se:umu:diva-20991 (URN)
Available from: 2009-03-31 Created: 2009-03-31 Last updated: 2012-02-01
2. Male and female resposes to florivory in the perennial herb Silene dioica
Open this publication in new window or tab >>Male and female resposes to florivory in the perennial herb Silene dioica
(English)Manuscript (Other academic)
Abstract [en]

 In dioecious species the two sexes differ in amount and timing of allocation to reproduction and as a consequence we would expect different sex specific responses to equal losses to herbivory. We studied the response of Silene dioica male and female plants to herbivory of two specialist insect herbivores Caryocolum viscariella and Delia criniventris that share the same food resource, the floral stems. We tracked the fates of marked individuals located in nine populations over eight consecutive years in a Bothnian archipelago. We found no differences in survival probabilities between attacked and non-attacked plants or between the sexes. We found that attacked plants of both sexes re-flowered to a higher extent compared to non-attacked plants. However, there was an inter-sexual difference in response to attack. Attacked females tended to re-flower more often than males and therefore showed a stronger compensatory response to this type of herbivore attack. The likely mechanism for this difference is that females in response to attack of floral stems early in season will save more resources than males and that these resources will be retained in the basal rosette to be used for future reproductive events. This suggests a positive effect on plant life time fecundity in females. However, there is also a negative effect of florivory on number of capsules produced as capsule production was halved in attacked compared to non-attacked females. The demographic implications of these direct and indirect effects of florivory remain to be understood.

 

National Category
Ecology
Research subject
Ecological Botany
Identifiers
urn:nbn:se:umu:diva-21001 (URN)
Available from: 2009-03-31 Created: 2009-03-31 Last updated: 2012-02-01
3. Rates of insect herbivory on Silene dioica change across primary successional zones.
Open this publication in new window or tab >>Rates of insect herbivory on Silene dioica change across primary successional zones.
Show others...
(English)Manuscript (Other academic)
Abstract [en]

The strengths and directions of herbivore-host plant interactions are strongly shaped by environmental conditions that also affect a number of plant traits (density, size, nutritional quality). We studied spatio-temporal patterns in attack rates of two specialist herbivores Delia criniventris and Caryocolum viscariella that utilize the same food resource, the floral stems, of their shared host plant Silene dioica across young, intermediate and old successional zones in the primary succession in a Bothinan archipelago. Our data from nine islands collected during seven consecutive years showed that attack rates were consistently higher in the youngest zone and decreased in parallel to progressing succession. This zonal pattern of decreasing attack rates correlated with several plant attributes, a decrease in plant size and nitrogen content, and an increased content of secondary compounds, but not to host plant density. We failed to come up with a simple explanation for the spatial structure with chronic high attack rates in the younger zones. However, the consistent patterns in attack rate suggest that a suite of abiotic and biotic factors interact and reinforce the strength and direction of selection.

National Category
Ecology
Research subject
Ecological Botany
Identifiers
urn:nbn:se:umu:diva-21000 (URN)
Available from: 2009-03-31 Created: 2009-03-31 Last updated: 2012-02-01
4. Which sex is most sensitive to a sexually transmitted disease?: A case study of the Microbortyum vioalaceum-Silene dioica association
Open this publication in new window or tab >>Which sex is most sensitive to a sexually transmitted disease?: A case study of the Microbortyum vioalaceum-Silene dioica association
(English)Manuscript (Other academic)
Abstract [en]

 In contrast to the many studies that have addressed whether herbivores discriminate between male and female plants of dioecious plant species, only a few studies have asked whether the two sexes differ in susceptibility to fungal attack. Most of these have dealt with the anther smut Microbotryum violaceum-Silene association and have generally reported a change from male to female biased disease frequencies in parallel to increasing overall disease frequencies. We followed the study system on nine island populations over seven years in a rising Bothnian archipelago. We found an overall pattern that female plants were more diseased than male plants with two exceptions. Disease frequencies were male biased on islands with low disease levels and in one of the seven study years. The change in disease frequencies from male to female bias confirm earlier studies suggesting that the relative contribution of the two components of infection risk, disease encounter and per contact infection probability can vary with population disease level. The change in the proportions of diseased males and females that was observed in one of the study years, followed a year of extreme weather conditions (prolonged drought). Both sexes showed a similar decline in flowering but diseased females decreased more than diseased males. This difference in response can be explained if considering that disease is more resource demanding in females than in males. Except for resources needed for mycelial growth and spore production, in females resources are also needed to restructure their sex expression and produce anthers. Thus in dioecious species traits that are sexually dimorphic are of great importance for understanding the outcome of interactions with natural enemies, including parasitic fungi.

 

National Category
Ecology
Research subject
Ecological Botany
Identifiers
urn:nbn:se:umu:diva-21002 (URN)
Available from: 2009-03-31 Created: 2009-03-31 Last updated: 2012-02-01

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