Top-down and bottom-up plant-mediated interactions on wild Lima bean, "Phaseolus lunatus"

Abstract

Plants are attacked by a wide array of insect herbivores, which are in turn attacked by natural enemies. Plants represent the base of these tritrophic interactions, and their traits affect higher trophic levels in many different ways. These effects have been referred to as bottom-up effects. Alternatively, higher trophic levels such as herbivores and their natural enemies can also affect lower trophic levels, this is known as top-down effects. In this thesis, I investigated the complex interactions among different trophic levels comprising several insects from different guilds that feed on various plants organs. I examined the extent to which the actors of such tritrophic interactions can influence each other, as well as other insects in the community. Lima bean (Phaseolus lunatus) is used as a model system in chemical ecology. This plant has been domesticated for the consumption of its seed, leading to many chemical and physical changes in this organ. Such changes can alter the interactions with the insects that attack these seeds. In the first chapter of my thesis, I investigated the effect of Lima bean domestication on one of its main storage pest, the seed beetle Zabrotes subfasciatus. Particularly, I focused on the increase of seed size, one of the major effects of domestication, and its impact on the intraspecific competition of this pest insect. I found that as a result of the domestication process, Lima bean seeds were more suitable for the seed beetle. The initial number of eggs on a seed and the weight of female beetles that emerged were negatively correlated, but only for wild seeds. Unravelling the changes in plant insect interactions caused by plant domestication may contribute to the development of pest control strategies. Seeds of wild lima bean plants are not suitable for human consumption, mainly because they contain toxic defensive compounds in high concentration: cyanogenic glycosides (CNGs). In the second chapter, I examined these secondary compounds that have been mainly studied in the leaves of wild lima bean, and have been shown to be toxic to generalist insect herbivores as well as some mammals. However, a previous study tested the effect of these compounds present in the seeds on seed beetles (Z. subfasciatus), and found no correlation between the performance of this insect and the seed CNG concentration. I investigated the potential role of CNG compounds in the seed of wild Lima bean as seedling resistance to herbivore as well as nitrogen storage compounds for plant growth. I found no correlation between seed CNG content and germination rate and seedling growth, but I showed that seeds with high CNG content produced seedling with a higher CNG content. Chapter three consists on a study on tritrophic interactions. The effect of parasitoids on the plant (topdown) is generally investigated for the potential reduction in herbivory damage they can cause. However, it is increasingly recognized that parasitoids can have other effects on plant, through physiological changes in their host. These types of top-down effect of parasitoids on plant are virtually unexplored. Here, I explored the effect of parasitoid on plant growth. In a field experiment, wild lima bean plants were exposed to three treatments. In the first one, no herbivores were allowed to feed on the plant. In a second one, plants were attacked by an herbivorous caterpillar, Spodoptera latifascia, which is naturally present in the same areas as our study plant. Third, some plants were also attacked by herbivores, but in presence of an ectoparasitoid (Euplectrus platyhypenae), present in the same area. I found that the herbivores triggered an overcompensation of the plant growth, which was attenuated by parasitoid presence. In addition, parasitoids could reduce the delay in seed production induced by herbivory. These interesting results are among the first to show that parasitoids can influence plant growth through its host. In the previous chapters, I focused on the separate effects of bottom-up and top-down forces on tritrophic interactions. Recent findings suggest herbivores present on the same plant at different times can influence each other through changes induced in the plant. Yet, this notion remains understudied. In the fourth chapter, I investigated top-down forces in a tritrophic interaction taking place at the end of the season, when wild lima bean plants are producing seeds. One of the main seed predators of seeds of wild Lima bean plants is the bruchid beetle Z. subfasciatus, which is in turn parasitized by the braconid ectoparasitoid Stenocorse bruchivora. I observed that seeds that had been previously damaged by seed beetles were still able to germinate. Thus, I designed a series of experiments to test the effect of bruchid beetles and their parasitoids on the germination and performance of the seedlings. I found a negative effect of bruchid beetles the germinated seedling performance, which was strongly attenuated by parasitoids. Furthermore, I also tested the bottom-up consequences of seed infestation on subsequent herbivorous insect feeding on plants germinated from seeds that endured different intensity and type of insect damage. I showed that plants produced by seeds with high levels of insect damage are less defended and leaf herbivores perform better on them than plants produced by seeds with low damage or no damage. In the last chapter of my thesis, I focused on a tritrophic interaction at the seed level, in order to investigate the interactive effects of beetle larval density inside the seed and the presence of parasitoids on bruchid development. Herbivore density has already been shown to influence parasitoid density, without changing the interaction between herbivores and parasitoids. However, the extent to which herbivore density influences the per capita effects of parasitoids on their host remains understudied. In addition, direct effects of parasitoids on their host (parasitism) are well studied, but there are only a few studies that investigate indirect non-consumptive effects of parasitoids on their host (e.g. induction of host defensive behavior by parasitoid sole presence). To study these interactions, we used a tritrophic interaction taking place at the wild lima bean seed level, between a seed beetle (Z. subfasciatus) and its parasitoids (S. bruchivora). This system is ideal because females of Z. subfasciatus glue their eggs on the seed coat and larval development is confined inside a small seed. This allows the manipulation of beetle larval densities in the seeds by removing eggs from the seed coat. The increase in beetle density had a negative effect on beetle performance, certainly due to intraspecific competition. This cascaded up to parasitoids which parasitism rate was significantly reduced. Parasitoids altered beetle development time, which can be explained by parasitoid nonconsumptive effects on their host. Together, the chapters of the current thesis add to the growing body of knowledge on how plantmediated interactions on different trophic levels and insect guilds affect the ecology and evolution of each of its participants and ultimately the insect community associated with Lima bean plants. Future studies should aim at shedding more light on the mechanisms that underlie herbivore-mediated parasitoids effects on plants, a topic that is particularly understudied.