Overcompensation of Ipomopsis aggregata following ungulate herbivory: getting to the root of it

Overcompensation;Fungal Associations;Arbuscular Mycorrhizal Fungi;Ipomopsis aggregata;Ungulate Herbivory;Water Limitations;Nutrient Limitations

Allsup, Cassandra

关键词: Overcompensation;    Fungal Associations;    Arbuscular Mycorrhizal Fungi;    Ipomopsis aggregata;    Ungulate Herbivory;    Water Limitations;    Nutrient Limitations;   

Others  :  https://www.ideals.illinois.edu/bitstream/handle/2142/72780/Cassandra_Allsup.pdf?sequence=1&isAllowed=y

美国|英语

来源: The Illinois Digital Environment for Access to Learning and Scholarship

【 摘 要 】

The idea that some plants benefit from being eaten is counterintuitive, yet there is now considerable evidence demonstrating enhanced fitness following herbivory, i.e., plants overcompensate. The mechanistic underpinnings of overcompensation, however, are unclear.For example, it has been assumed that plants growing in high resource conditions are best able to compensate for herbivory. However, just the opposite has been found for dicotyledonous plants exhibiting patterns of overcompensation; with most occurring in resource-poor conditions. These studies, however, have ignored the potential effects of below-ground interactions with other organisms such as arbuscular mycorrhizal fungi (AMF) and other fungal associates that could provide the necessary nutrients needed.A long-term study of the monocarpic biennial, scarlet gilia, Ipomopsis aggregata, showed that ungulate herbivory by mule deer and elk can result in a three-fold increase in plant fitness. We hypothesized that fungal associations would facilitate the compensatory response most commonly observed in an Arizona population of scarlet gilia; perhaps mutualistic associations with fungi, such as arbuscular mycorrhizal fungi, would explain the phenomenon of overcompensation altogether. However, fungal removal experiments indicate that fungi are not mutualistic but parasitic. The reduction in fungi altered the compensatory response, particularly under water limited conditions, increasing compensation from equal to over. In a year of normal precipitation, a fungicide treatment reduced the compensatory response from overcompensation to a marginally significant trend toward overcompensation, by simultaneously increasing the reproductive success of both browsed and unbrowsed plants. We also show experimentally that the interactive effects of water and fungicide maximize fruit production following ungulate herbivory. Overall, our results are counter to the “modification of tolerance hypothesis”, that plants associating with mycorrhizal fungi will have higher tolerance to herbivory. It is likely that arbuscular mycorrhizal fungi and dark septate endophytes are competing with plants for nutrients, carbon and water following herbivory, limiting the magnitude of compensation.Both water availability and herbivory also had significant effects on levels of fungal colonization and species distribution patterns. Specifically, drought conditions enhanced overall levels of fungal colonization. In addition, ungulate herbivory, lead to higher colonization of hyphae and arbuscules under drought conditions. It is likely that under drought conditions, fungi colonize browsed plants at higher levels due to the root becoming a sink for carbon, generated by regrowth tissue following the release of apical dominance.Ungulate herbivory also enhanced, or tended to enhance, the richness and diversity of the fungal community in roots and soils. An increase in species following browsing, particularly Scuttellospora sp. may indicate that specific fungal species are responsible for the parasitic response of the soil fungal community on the compensatory response of I. aggregata. These results suggest that soil fungal community loads and fungal species dictate the magnitude of fitness compensation following ungulate herbivory.These studies on the interactive effects of herbivory and soil fungal communities on the compensatory response of I. aggregata were extended by incorporating a series of phosphorus (P) treatments (the primary nutrient supplied to a host plant by mycorrhizal fungi) to assess the interactive effects of P on plant compensation and arbuscular mycorrhizal colonization. Results show that soil nutrient levels and the soil inhabiting fungal community interact with herbivory to determine the growth and compensatory response of scarlet gilia. Specifically, the compensatory response is limited by P availability, with nutrient availability being more important for browsed plants than for unbrowsed plants. Phosphorus is also shown to decrease mycorrhizal allocation to hyphae, arbuscules and internal spores within plant roots. Whereas plants equally compensated under low nutrient conditions, they overcompensated under the highest level of P, due to an increase in the fitness of browsed plants. Furthermore, the removal of soil fungi with a fungicide treatment resulted in overcompensation under the lowest and highest nutrient conditions, due primarily, to an increase in the fitness of browsed plants. These results support the findings of others that under high P conditions plants shift to soil P when plants are able to obtain nutrients through their own root systems, decreasing fungal colonization and enhancing plant fitness following herbivory.This study represents one of few to consider the interactive effects of mammalian herbivory and fungal associations on plant fitness and represents the only study addressing the phenomenon of overcompensation. It also represents one of few studies focusing on plant reproduction as opposed to biomass alone; aboveground biomass and fruit production were at best weakly correlated (R2=0.29, p=0.001), thus biomass may not give a clear picture of changes that are ultimately of evolutionary importance.