Plant-Mediated Indirect Interactions And Response Mechanisms Of Grasshoppers To Large Herbivore Grazing

Grasslands are ecosystems that are dominated by plants and their associated herbivores within the abiotic setting.Grasslands host a high diversity of plants and animals,and the complex interactions among these species are the key determinants of the structure and the dynamics of the ecological community.Studies on the species interactions are essential to fully understand the operational mechanisms of grassland systems and to better predict the ecosystem responses to climate changes and human activities.In the case of plant-mediated interactions among species within the herbivorous guild,the vast majority of work has traditionally focused on closely related species of similar size(e.g.,interspecific relationships between insects).However,within grassland ecosystems,plants and insects often coexist with large herbivores.The role of large herbivore grazing in driving the richness and composition of insect communities has generated great interest.In recent years,ecologists have come to recognize the importance of these indirect species interactions.Some researchers suggest that the indirect interactions induced by large herbivores play a critical role in shaping species distribution and community structure of grasslands.However,compared with the direct interaction between species,indirect interactions are more complex and subtle.Many questions surrounding these biotic interactions remain to be answered due to the paucity of carefully designed controlled experiments.Our studies explored the indirect interactions and underlying mechanism between large domestic herbivore(cattle Bos taurus)and small herbivorous insects(grasshopper Euchorthippus unicolor and E.cheui)in the eastern region of the Eurasian steppe.We used a set of field and laboratory manipulative experiments to investigate the potential pathways whereby large domestic herbivores affect Euchorthippus grasshoppers,including plant quantity,microclimate conditions,and plant quality.Additional fertilization experiment were further conducted to identify potential effects of plant quality(traits)in the interactions between large herbivore and grasshoppers.Our study is of great importance for development of species coexistence theory,in addition to having significant implications for controlling pest and for maintaining the biodiversity and stability of grasslands.We report the main results and conclusions as follows:We investigated the effects of large herbivore grazing on the population demographics of E.unicolor grasshoppers.The results showed that E.unicolor shares similar dietary preferences with domestic cattle: it feeds predominately on Leymus chinensis,the dominant plant in community,and seldom on forbs.The diets of cattle and grasshopper therefore completely overlap.The population density of E.unicolor grasshopper was 51% lower in grazed plots than in ungrazed plots.Cattle grazing had a negative effect on the performance of female and male E.unicolor.Cattle grazing did not affect plant biomass significantly in any of the plant functional groups that were used in the studies.Cattle grazing did decrease the height of L.chinensis,but had no significant impacts on the density or cover of L.chinensis.The average air temperature at 35 cm above ground significantly increased in grazed plots.Grazing also significantly increased N content of L.chinensis leaves by 38%,and decreased the C:N ratio of L.chinensis leaves by 27%.Further analysis found that changes of plant nitrogen content exerts the greatest impact on the population density and performance of E.unicolor grasshoppers.Our study found that the negative effect of cattle on grasshoppers appeared to be the result of an increase in plant nitrogen content in grazed areas.Our results demonstrate that plant quality is a critical factor in regulating plantherbivore interactions,especially for insect herbivores,which are more sensitive to alterations of plant quality than plant quantity.We explored the effects of large herbivore grazing on a grasshopper community and the relationships between two dominant grasshoppers E.cheui and E.unicolor.The results showed that E.cheui(early-season species)and E.unicolor(later-season species)were staggered in appearance throughout the growing season with 4-5 weeks between the peaks in their life cycles.The temporal co-occurrence patterns between the two species was unaffected by livestock grazing.However,the species abundance was significantly influenced by the occurrence of grazing.Remarkably higher E.cheui abundance and lower E.unicolor abundance resulted in a reversion of the proportion of both species in total grasshopper abundance.Mixed linear modeling revealed that the response of both grasshoppers predominantly reflects the differences in plant quality(nitrogen content rather than defensive chemistry)of their host plant L.chinensis induced by livestock grazing,but in a contrasting fashion.The difference in response between E.cheui and E.unicolor may result from their specific nutritional requirements.In summary,our results provide evidence that dominant insect species can avoid competition by partitioning resources in time.Livestock grazing may not affect insect coexistence patterns,but they can have strong and contrasting effects on their population size by inducing alterations in plant quality.We examined whether changes in the traits of the host plant would affect population and individual responses of Euchorthippus grasshoppers.The results showed that the traits of L.chinensis leaves appeared to have significant deviations under different nitrogen application levels.Nitrogen additions significantly reduced the C:N ratio of L.chinensis leaves.These additions also significantly increased protein content without altering the soluble carbohydrates content and water content of L.chinensis leaves.Additional implications of the nitrogen on L.chinensis leaves induced a significant reduction in leaf toughness and a significant increase in total phenolic content.Further experiments confirmed that the change of host plant traits can significantly affect the population density,individual feeding behavior and performance of Euchorthippus grasshoppers in both field and laboratory conditions.Nitrogen additions caused a significant decline in E.unicolor population density and individual performance(survival rate,body size and body weight)in the field,despite an increase in the quality of host plant and the unchanged plant quantity.In the lab,E.cheui preferred Leymus leaves collected from a higher nitrogen treatment,while E.unicolor preferred leaves collected from a lower nitrogen treatment.Euchorthippus grasshoppers did not have compensatory feeding behavior,indicating that grasshoppers mainly rely on actively selecting food to balance nutrient intake in order to achieve optimal fitness with their system.This study supports the nutrient balance hypothesis(the geometric framework)that organisms are predicted to have specific dietary intake targets for each nutrient,and a mismatch between an organism's intake target and the nutrient content of its food may result in a surplus or a deficit of particular elements.The input of external nutrients into an ecosystem can therefore have an unpredictable cascading effect on higher trophic species by changing the ratio and rate of their resource's nutrient supply.This study provides a better understanding of the mechanisms of species coexistence and the maintenance of species diversity.Large herbivores can exert strong indirect effects on herbivorous insects through their overlapping foraging preferences.By systematically detecting all potential pathways,we found that the indirect effects of large herbivores can be mediated by plant nutrients.Additionally,this trait-mediated indirect effect can be transmitted to multiple levels of insects.Moreover,the response of insects to grazing-induced changes may be species-specific and dependent on the insects' own food and/or microsite preferences,which is determined by the morphology,physiology and ecological characteristics.Trait-mediated indirect effects may therefore add uncertainty to ecosystems responding to future environmental changes.This study has important implications for grassland management and conservation.Our results suggest that moderate and rotational grazing regime may result in patches which vary in plant resource quality.It may optimize the total insect abundance and richness integrated over the growing season since insect species within an assemblage usually have significant differences of diet preference and thereby different “patch requirements” in the ecosystem.Our study implies that disturbance and environmental heterogeneity is a key driver of species coexistence at a landscape scale because this variation may drive differential preferences of coexisting species for food or habitat patches that occur in space and time.