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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.