DISCUSSION
Even if we did not find direct evidence of sexual dimorphism in B. cordata , our results suggests that plant-sex affects arthropod communities through both top-down and bottom-up mechanisms; and that this effect has a strong temporal component linked to the plant phenology. We suggest that seasonal variation on plant sex- arthropod interactions might be particularly important for plants that experience seasonal environments and that accounting for plant seasonality effects has the potential to reconcile previous debates about plant-sex preference and performance.
Sexual dimorphism inB uddleia cordata and its implications on sex-biased herbivory
Differences between sexes (i.e., sexual dimorphism) are common in dioecious plants. These differences that are the result of sex-specific gene expression and physiological trade-offs affect the arthropod communities associated with plants of different sexes (Mooney and Singer 2001, Nell et al. 2018). But contrary to our initial expectation, we did not find sex-related differences in the two plant traits that we evaluated: leaf thickness and water content (Fig. 1). These results are consistent with the observations by Moreira et al. (2019) who found no sex-related differences in water content, and in nitrogen and phosphorous concentrations in B. cordata during a study conducted in September 2017. Nevertheless, we observed a strong temporal variation in the water content of B. cordata ’s leaves that is consistent with the highly seasonal climate of the preserve, having the highest leaf water content during the rainy season in August, and the lowest leaf water content during the dry season in February (Fig. 1). It is important to highlight that while our results do not suggest sexual dimorphism, there are multiple important axis of variation that we did not evaluate. For example, other studies have found differences in the secondary metabolites content of B. cordata’ s males and females (Moreira et al. 2019). Furthermore, the female-biased sex-ratio that we found in B. cordata ’s population at PSAER is consistent with differences in life-history traits between individuals of different sex.
The response of arthropods to plant sexual dimorphism has been studied during the last century mostly in the context of herbivore preference and performance, showing a great support for the hypothesis of sex-biased herbivory (Danell et al. 1985, Boecklen et al. 1990, Hjaltén 1992, Agren et al. 1999, Cornelissen and Stiling 2005, Granados-Sánchez et al. 2008, Kabir et al. 2014). This hypothesis suggests that male plants experience higher herbivory than female plants due to male plants allocating more resources on vegetative growth, while female plants allocate more resources into reproduction and defensive traits (Cornelissen and Stiling 2005, Ribeiro-Mendes et al. 2012). For example, in a review, Agren et al. (1999) showed that in 25 out of 39 studies male plants were preferred over female plants by herbivores, and herbivore densities were higher in male plants than in females during field experiments. Nevertheless, Sargent and McKeough (2022) in a recent meta-analysis, that included 58 new observations of herbivory and 41 of secondary chemistry compared to the original database used by Cornelissen and Stiling (2005), found evidence that a male-sex bias in herbivory is not the rule. Our results did not show differences in herbivory rates between plants of different sex, and thus constitute another example against the herbivory-bias hypothesis. Nevertheless, it is important to notice that our quantification method for herbivory might not adequately capture the damaged produced by sap-sucking insects, such as Hemiptera, and this group was the second most important group of herbivores in our sample.
Overall, recent studies contrast with the previously proposed pattern of male-preference in sex-biased herbivory, by either finding no differences in herbivory or female-preference examples. Even if we accept the expectation of female plants allocating more resources on reproduction compared to male plants, there are many compensatory mechanisms that may reduce the effect of a higher reproductive resource assignment on vegetative traits (Delph 1999). Furthermore, in some scenarios, we might expect male-plant reproductive allocation to be higher than in female plants, for example in wind-pollinated plants with a large production of nitrogen-rich pollen (Delph et al. 1993, Harris and Pannell 2008). In fact, there is evidence of cases in which male plants show higher concentration of secondary metabolites associated with defense against herbivores (Hjaltén 1992, Bañuelos et al. 2004, Zhang et al. 2019, Yang et al. 2020); including our study systemB. cordata (Moreira et al. 2019). Finally, even if we did not find sex-bias in leaf water content and thickness, we found a strong seasonal pattern observed in these metrics that raises the question of whether other variables that show sex-dependence (like the secondary compounds recorded by Moreira et al. 2019) would also display a temporal variation pattern. A seasonal dependent pattern of plant traits could explain some of the contradictory results regarding which plant sex displays more defensive traits found in the literature (i.e., Sargent and McKeough 2022). It could also suggest that the effect of plant sex on arthropod communities varies through time, and it highlights the need for conducting studies in dioecious plants, especially those experiencing seasonal environments, while accounting for seasonal variation.