Interactive Effects Of Pathogens, Plant Defenses And Predators On Herbivore Performance And Population Dynamics

Variation in plant defenses and predation has the potential to cause profound changes in herbivore performance and population dynamics. Evaluating the complex interactive effects of plant defenses and predators that lead to the exponential or density-dependent growth of herbivorous insects is critical for understanding their population dynamics. For my doctoral research I (i) investigated the effects of pathogen-induced plant defenses on herbivores, (ii) measured the effects of constitutive and induced plant defenses on the strength of herbivore density-dependent growth and (iii) evaluated the influence of plant resistance on predator-prey interactions. Chapter 1 evaluates how different strains of Potato virus Y differentially affect plant defensive pathways, showing that strains that strongly induce the salicylic acid pathway increase susceptibility to chewing herbivores, while not affecting the performance of its vector, a phloem feeding aphid. Chapter 2 demonstrates that plants with low constitutive levels of defense cause strong density-dependent population growth in aphids, whereas populations on plants with high levels of constitutive defense show density-independent growth. Building on chapter 2, chapters 3 and 4 focus on the critical role of plant defenses in predator-prey interactions. Chapter 3 shows that plant resistance affects not only the consumptive, but also the nonconsumptive effects of predators on prey. I demonstrate that aphid prey could not exhibit predator-induced behavioral responses on plants with high levels of resistance. Chapter 4 explores the underlying mechanisms by which variation in plant defenses affect insect population: directly, through changes in herbivore population growth, or indirectly, by modifying predator impacts on prey populations. Chapter 4 shows that predators only cause prey density-dependent population growth when the herbivorous prey are feeding on low-resistance plants, which are still able to induce high levels of herbivore-associated cues. Collectively, these results highlight the strong effect that plant defenses have on herbivore population dynamics. This work has important implications; it suggests that induced plant responses to prey should be accounted for in biological control assessments, as these responses determine the efficiency of predators on target prey

JAE data_dryad

Consequences of variation in plant defenses and herbivore density on herbivore development, reproduction and density-dependent population growt

Data from: Plant resistance reduces the strength of consumptive and non-consumptive effects of predators on aphids

1. The impact of predators on prey has traditionally been attributed to the act of consumption. Prey responses to the presence of the predator (non-consumptive effects), however, can be as important as predation itself. While plant defences are known to influence predator–prey interactions, their relative effects on consumptive vs. non-consumptive effects are not well understood. 2. We evaluated the consequences of plant resistance and predators (Hippodamia convergens) on the mass, number of nymphs, population growth, density and dispersal of aphids (Macrosiphum euphorbiae). We tested for the effects of plant resistance on non-consumptive and consumptive effects of predators on aphid performance and dispersal using a combination of path analysis and experimental manipulation of predation risk. 3. We manipulated plant resistance using genetically modified lines of tomato (Solanum lycopersicum) that vary incrementally in the expression of the jasmonate pathway, which mediates induced resistance to insects and manipulated aphid exposure to lethal and risk predators. Predation risk predators had mandibles impaired to prevent killing. 4. Plant resistance reduced predation rate (consumptive effect) on high resistance plants. As a consequence, predators had no impact on the number of nymphs, aphid density or population growth on high resistance plants, whereas on low resistance plants, predators reduced aphid density by 35% and population growth by 86%. Path analysis and direct manipulation of predation risk showed that predation risk rather than predation rate promoted aphid dispersal and varied with host plant resistance. Aphid dispersal in response to predation risk was greater on low compared to high resistance plants. The predation risk experiment also showed that the number of aphid nymphs increased in the presence of risk predators but did not translate into increased population growth. 5. In conclusion, the consumptive and non-consumptive components of predators affect different aspects of prey demography, acting together to shape prey population dynamics. While predation risk accounts for most of the total effect of the predator on aphid dispersal and number of nymphs, the suppressive effect of predators on aphid population occurred largely through consumption. These effects are strongly influenced by plant resistance levels, suggesting that they are context dependent

Data from: Constitutive and herbivore-induced plant defenses regulate herbivore population growth

1. Induced plant defenses regulated by the phytohormones jasmonic acid and salicylic acid are predicted to influence herbivore population dynamics, in part because they can operate in a density-dependent manner. While there is ample evidence that induced plant responses affect individual performance and growth of herbivores, whether they scale-up to regulate herbivore population dynamics is still unclear. 2. We evaluated the consequences of variation in plant defenses and herbivore density on herbivore development, reproduction and density-dependent population growth. We investigated potential mechanisms affecting the strength of herbivore density-dependent processes by manipulating jasmonate expression, quantifying plant defensive traits (phytohormones jasmonic acid and salicylic acid and serine proteinase inhibitors) and adding aphids (Macrosiphum euphorbiae) at different densities to plants to simulate different initial population density and herbivore load. We manipulated jasmonate defenses by using genetically modified lines of tomato plants (Solanum lycopersicum) with elevated or suppressed jasmonate-dependent defenses. Jasmonate-insensitive plants cannot induce the jasmonic acid pathway, while jasmonate-overexpressing plants constitutively express jasmonate-dependent defenses. 3. We found that jasmonate defenses provided resistance against aphids and influenced density-dependent processes. Jasmonate-overexpressing plants reduced aphid reproduction, prolonged developmental time, dampened aphid populations across all aphid densities, and caused density-independent aphid population growth. Aphid feeding on jasmonate-overexpressing plants did not activate the salicylic acid pathway, thus on this plant line jasmonate defenses affected aphid responses. In contrast, jasmonate-insensitive plants increased aphid reproduction, shortened the developmental time, reduced population growth only at high initial densities, and promoted strong negative density-dependent population growth. Aphid feeding on jasmonate-insensitive plants did not induce jasmonate-dependent defenses, but induced the salicylic acid pathway in a density-dependent manner, which resulted in negative density-dependent aphid population growth. 4. Aphid feeding on jasmonate-insensitive and overexpressing plant differentially activated the salicylate pathway, revealing a negative crosstalk between the defensive phytohormones jasmonic acid and salicylic acid. By muting or enhancing jasmonate-mediated responses and quantifying salicylic acid phytohormone induction, we demonstrated that plant defenses are a key factor driving not only the performance, but also the density dependence processes of herbivore populations

Plant resistance reduces the strength of consumptive and non-consumptive effects of predators on aphids

Plant resistance reduces the strength of consumptive and non-consumptive effects of predators on aphid

Data on the effects of plant defenses and predators on herbivores

Data from manipulative laboratory and field experiments

Cranberry resistance to dodder parasitism: induced chemical defenses and behavior of a parasitic plant

Parasitic plants are common in many ecosystems, where they can structure community interactions and cause major economic damage. For example, parasitic dodder (Cuscuta spp.) can cause up to 80–100 % yield loss in heavily infested cranberry (Vaccinium macrocarpon) patches. Despite their ecological and economic importance, remarkably little is known about how parasitic plants affect, or are affected by, host chemistry. To examine chemically-mediated interactions between dodder and its cranberry host, we conducted a greenhouse experiment asking whether: (1) dodder performance varies with cranberry cultivar; (2) cultivars differ in levels of phytohormones, volatiles, or phenolics, and whether such variation correlates with dodder parasitism; (3) dodder parasitism induced changes in phytohormones, volatiles, or phenolics, and whether the level of inducible response varied among cultivars. We used five cranberry cultivars to assess host attractiveness to dodder and dodder performance. Dodder performance did not differ across cultivars, but there were marginally significant differences in host attractiveness to dodder, with fewer dodder attaching to Early Black than to any other cultivar. Dodder parasitism induced higher levels of salicylic acid (SA) across cultivars. Cultivars differed in overall levels of flavonols and volatile profiles, but not phenolic acids or proanthocyanidins, and dodder attachment induced changes in several flavonols and volatiles. While cultivars differed slightly in resistance to dodder attachment, we did not find evidence of chemical defenses that mediate these interactions. However, induction of several defenses indicates that parasitism alters traits that could influence subsequent interactions with other species, thus shaping community dynamics429510

Tjiurutue.etal.Oecologia.2017.Metadata.

These are data from a manipulative experiment asking how damage by gypsy moths on cranberry affected attachment by a parasitic plant, dodder, as well as induced chemical defenses (phytohormones, volatiles and phenolics) that could be mechanisms mediating these interactions. The attachment and chemistry were assessed in two separate, parallel experiments in the greenhouse in Amherst, MA, USA in 2011. There is one worksheet for each of these responses (the 3 chemicals plus dodder attachment) and a worksheet describing all the variables

Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense

The host-associated microbiome is vital to host immunity and pathogen defense. In aquatic ecosystems, organisms may interact with environmental bacteria to influence the pool of potential symbionts, but the effects of these interactions on host microbiome assembly and pathogen resistance are unresolved. We used replicated bromeliad microecosystems to test for indirect effects of arthropod-bacteria interactions on host microbiome assembly and pathogen burden, using tadpoles and the fungal amphibian pathogen Batrachochytrium dendrobatidis as a model host-pathogen system. Arthropods influenced host microbiome assembly by altering the pool of environmental bacteria, with arthropod-bacteria interactions specifically reducing host colonization by transient bacteria and promoting antimicrobial components of aquatic bacterial communities. Arthropods also reduced fungal zoospores in the environment, but fungal infection burdens in tadpoles corresponded most closely with arthropod-mediated patterns in microbiome assembly. This result indicates that the cascading effects of arthropods on the maintenance of a protective host microbiome may be more strongly linked to host health than negative effects of arthropods on pools of pathogenic zoospores. Our work reveals tight links between healthy ecosystem dynamics and the functioning of host microbiomes, suggesting that ecosystem disturbances such as loss of arthropods may have downstream effects on host-associated microbial pathogen defenses and host fitness2861905CONSELHO NACIONAL DE DESENVOLVIMENTO CIENTÍFICO E TECNOLÓGICO - CNPQCOORDENAÇÃO DE APERFEIÇOAMENTO DE PESSOAL DE NÍVEL SUPERIOR - CAPESFUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULO - FAPESP312895/2014-3; 300896/2016-6; 302518/2013-4não tem2014/23388-7; 2013/50741-7; 2014/50342-8; 2017/26162-8; 2016/03344-