Early land plants: Plentiful but neglected resources for herbivores ?
Authors:   , Duhin Audrey 
Published: August 2024

There are many types of interactions between living organisms. Among these, we can find the herbivory interaction. This is most of the time a case of antagonism, as are prey‐predator relationships. This is a phenomenon that is fairly well studied for certain groups of plants such as angiosperms (flowering plants). These plants are considered to be at the highest level of evolution and are referred as "higher plants". On the other hand, other types of plants are less studied in general, and in particular on the subject of herbivory. This is the case for the bryophytes, which are the first plant species to have colonized the terrestrial habitat. They had to develop various strategies during their ground colonization, such as resistance to UV radiation and desiccation. Ferns are also under‐studied, but they are the first group in evolution presenting a vascular system, necessary for a growth superior to about ten centimeters to which mosses are constrained. Plants are constantly subjected to different stresses in their environments. These can be abiotic (i.e. due to non‐living environmental factors such as temperature, humidity, soil type, etc.) or biotic (i.e. due to living organisms such as pathogens, herbivores, other plants in competition, etc.). In this work, a particular focus is made on herbivory. In this interaction, plants must adopt a strategy to survive to herbivores’ consumption and several possibilities are offered to them. Indeed, they can tolerate the attacks or defend themselves. This last option is declined in several facets, like having a low nutrients content or like exhibit physical structures as spines or trichomes. Another possibility is to contain toxic chemical compounds, which can be volatile or not. These defenses can be combined and are also sometimes inducible by a particular stress. This phenomenon is regulated by phytohormones in the plant. In this thesis, different types of defenses are studied in primitive plants such as mosses and ferns. Thus, in a first chapter, the nutrient content of 15 mosses and ferns was analyzed in terms of proteins, amino acids and sugars. In parallel, leaves were fed to two types of herbivores: snails (Cochlicella baraba) and caterpillars (Spodoptera exigua). These two generalist phytophagous species do not survive nor develop sustainably to their reproductive adult stage on the proposed treatments, except for the artificial diet and maize, used as controls. However, it was shown that these plants have a high enough nutrient level to allow development, but that the compositions in amino acids and sugars differ qualitatively. In a second chapter, defenses and physical factors were addressed. Bioassays with caterpillars were also carried out in this part. The treatment proposed to the herbivores were artificial diet mixed with powder made from 15 different primitive plants and two flower plants or no plant used as control. We obtained results showing that the insects grew well on diets containing tissue from one of the bryophyte species, from the aquatic fern, or from one of the flowering plants used as a control. In addition, possible structures such as trichomes were investigated. The aquatic fern species included in the study was the only species that shown these structures, but uses them for flotation purposes, rather than as defensive weapon. Water and silica content analyses complete the data collected in this chapter. Silica concentration is quite variable, intra‐ and interspecifically speaking. It was not possible to detect a significant difference between different plants. Moreover, no correlation between the content of this element could be established. On the other hand, it was possible to differentiate in a statistically significant way the species of ground ferns with a lower water content than the rest of the plants used. This suggests, however, that these physical defenses are not involved in the lower plants' strategy to combat herbivores. The next chapter was dedicated to the chemical defenses. For this part, only two species of pteridophytes were used, namely a lycopod and a fern. To carry out the investigations of chemical defenses, extractions were carried out using different solvents, such as water combined with 0.1% formic acid, methanol, and dichloromethane. The extracts obtained were dried and mixed with artificial diet. Those supplemented diets were then used to feed polyphagous caterpillars. These insects had difficulty gaining weight and developing on two of the extracts made with the fern species. In a second step, fractions were made from the worst extract, the aqueous one. The fractions were again added to artificial diet and offered to the caterpillars. One of the fractions was found to be more toxic than the others, and contained phloroglucinols. This is a class of compounds known to be involved in the defense of plants like eucalyptus. It was therefore concluded that these molecules might play the same role for the fern species studied here. In the fourth chapter of this thesis, phytohormones and volatile organic compounds (VOCs) emitted by a fern species after attacks by specialized aphids (Idiopterus nephrelepidis) or caterpillars (S. exigua), or mechanical damage were investigated. It was not possible to detect a hormonal response of the plants. Change in the VOCs emitted as a result of the aggression by the aphids were, as well, not detectable. On the other hand, it was shown that this fern species changes its odor when consumed by caterpillars or when subjected to wounds alone, both cases being discernible. This mechanism is therefore not limited to flowering plants and could be useful for pteridophytes. We can hypothesize that they would attract beneficials such as parasitoids, helping them to overcome herbivores’ attacks. Overall, the results of this PhD demonstrate that the study of herbivory in lower plants is complex and deserves research attention, while highlighting the importance of studying these plant groups from an evolutionary perspective. Moreover, these plants are called “primitive”, but their present‐day representatives encounter the same constraints as the so‐called higher plants. The early land plants are as successful and adapted to their environment as the flowering plants.