The bacterium Xylella fastidiosa re-emerged as a plant pathogen of global importance in 2013 when it was first associated with an olive tree disease epidemic in Italy. The current threat to Europe and the Mediterranean basin, as well as other world regions, has increased as multiple X. fastidiosa genotypes have now been detected in Italy, France, and Spain. Although X. fastidiosa has been studied in the Americas for more than a century, there are no therapeutic solutions to suppress disease development in infected plants. Furthermore, because X. fastidiosa is an obligatory plant and insect vector colonizer, the epidemiology and dynamics of each pathosystem are distinct. They depend on the ecological interplay of plant, pathogen, and vector and on how interactions are affected by biotic and abiotic factors, including anthropogenic activities and policy decisions. Our goal with this review is to stimulate discussion and novel research by contextualizing available knowledge on X. fastidiosa and how it may be applicable to emerging diseases.
Terrestrial invertebrate carcasses are an important resource for insects developing in pitcher plants. However, little is known of the role of these carcasses in other containers, which also receive leaf fall and stemflow inputs. This experiment investigated effects of accumulated invertebrate carcasses as a resource for two competing mosquitoes, Aedes albopictus (Skuse) and Aedes aegypti (L.), whether either species differentially benefited from accumulated carcasses, and if such a benefit affected interspecific competition. First, we measured accumulation of invertebrate carcasses in standard containers at a field site. We then used a replacement series with five different species ratios at the same total density, and varied the input of invertebrate carcasses [dead Drosophila melanogaster (Meigen) ] in three levels: none, the average input from our field site, or the maximum input recorded at our field site. Survivorship, development time, and mass were measured for each mosquito species as correlates of population growth, and were used to calculate a population performance index, lambda'. There were strong positive effects of invertebrate carcass additions on all growth correlates and lambda'. Differences in performance between species were pronounced in small or no carcass additions and absent in large inputs of invertebrate carcasses, but there was little evidence that inputs of invertebrate carcasses altered the competitive advantage in this system. These results suggest that terrestrial invertebrate carcasses may be an important resource for many types of container communities, and large accumulations of dead invertebrates may reduce resource competition between these mosquitoes, thus favoring coexistence. We propose that the total amount of resource, including accumulated invertebrate carcasses, may explain observed patterns of replacement involving these mosquitoes.
Terrestrial invertebrate carcasses are an important resource for insects developing in pitcher plants. However, little is known of the role of these carcasses in other containers, which also receive leaf fall and stemflow inputs. This experiment investigated effects of accumulated invertebrate carcasses as a resource for two competing mosquitoes, Aedes albopictus (Skuse) and Aedes aegypti (L.), whether either species differentially benefited from accumulated carcasses, and if such a benefit affected interspecific competition. First, we measured accumulation of invertebrate carcasses in standard containers at a field site. We then used a replacement series with five different species ratios at the same total density, and varied the input of invertebrate carcasses [dead Drosophila melanogaster (Meigen) ] in three levels: none, the average input from our field site, or the maximum input recorded at our field site. Survivorship, development time, and mass were measured for each mosquito species as correlates of population growth, and were used to calculate a population performance index, lambda'. There were strong positive effects of invertebrate carcass additions on all growth correlates and lambda'. Differences in performance between species were pronounced in small or no carcass additions and absent in large inputs of invertebrate carcasses, but there was little evidence that inputs of invertebrate carcasses altered the competitive advantage in this system. These results suggest that terrestrial invertebrate carcasses may be an important resource for many types of container communities, and large accumulations of dead invertebrates may reduce resource competition between these mosquitoes, thus favoring coexistence. We propose that the total amount of resource, including accumulated invertebrate carcasses, may explain observed patterns of replacement involving these mosquitoes.
1. Ecological theory predicts that vector preference for certain host species or discrimination between infected versus uninfected hosts impacts disease incidence. However, little information exists on the extent to which vector withinhost feeding preference mediates transmission. This may be particularly important for plant pathogens, such as sharpshooter transmission of the bacterium Xylella fastidiosa, which are distributed irregularly throughout hosts.2. We documented the within-host distribution of two vector species that differ in transmission efficiency, the leafhoppers Draeculacephala minerva and Graphocephala atropunctata, and which are free to move throughout entirely caged alfalfa plants. The more efficient vector D. minerva fed preferentially at the base of the plant near the soil surface, whereas the less efficient G. atropunctata preferred overwhelming the top of the plant.3. Next we documented X. fastidiosa heterogeneity in mechanically inoculated plants. Infection rates were up to 50% higher and mean bacterial population densities were 100-fold higher near the plant base than at the top or in the taproot.4. Finally, we estimated transmission efficiency of the two leafhoppers when they were confined at either the base or top of inoculated alfalfa plants. Both vectors were inefficient when confined at the top of infected plants and were 20-60% more efficient when confined at the plant base.5. These results show that vector transmission efficiency is determined by the interaction between leafhopper within-plant feeding behaviour and pathogen withinplant distribution. Fine-scale vector and pathogen overlap is likely to be a requirement generally for efficient transmission of vector-borne pathogens.
Intraguild predation (IGP) is a dominant community module in terrestrial food webs that occurs when multiple consumers feed both on each other and on a shared prey. This specific form of omnivory is common in terrestrial communities and is of particular interest for conservation biology and biological control given its potential to disrupt management of threatened or pest species. Extensive theory exists to describe the dynamics of three-species IGP, but these models have largely overlooked the potential for other, exterior interactions, to alter the dynamics within the IGP module. We investigated how three forms of feeding outside of the IGP module by intraguild predators (i.e. trophic supplementation) affect the dynamics of the predators (both IG predator and IG prey) and their shared resource. Specifically, we examined how the provision of a constant donor-controlled resource, the availability of an alternative prey species, and predator plant-feeding affect the dynamics of IGP models. All three forms of trophic supplements modified the basic expectations of IGP theory in two important ways, and their effects were similar. First, coexistence was possible without the IG prey being a superior competitor for the original shared resource if the IG prey could effectively exploit one of the types of trophic supplements. However, supplements to the IG predator restricted the potential for coexistence. Second, supplements to the IG prey ameliorated the disruptive effects of the IG predator on the suppression of the shared resource, promoting effective control of the resource in the presence of both predators. Consideration of these three forms of trophic supplementation, all well documented in natural communities, adds substantial realism and predictive power to intraguild predation theory.
Over the last decade, the plant disease huanglongbing (HLB) has emerged as a primary threat to citrus production worldwide. HLB is associated with infection by phloem-limited bacteria ('Candidatus Liberibacter' spp.) that are transmitted by the Asian citrus psyllid, Diaphorina citri. Transmission efficiency varies with vector-related aspects (e.g., developmental stage and feeding periods) but there is no information on the effects of host-pathogen interactions. Here, acquisition efficiency of 'Candidatus Liberibacter asiaticus' by D. citri was evaluated in relation to temporal progression of infection and pathogen titer in citrus. We graft inoculated sweet orange trees with 'Ca. L. asiaticus'; then, at different times after inoculation, we inspected plants for HLB symptoms, measured bacterial infection levels (i.e., titer or concentration) in plants, and measured acquisition by psyllid adults that were confined on the trees. Plant infection levels increased rapidly over time, saturating at uniformly high levels (≈10(8) copy number of 16S ribosomal DNA/g of plant tissue) near 200 days after inoculation-the same time at which all infected trees first showed disease symptoms. Pathogen acquisition by vectors was positively associated with plant infection level and time since inoculation, with acquisition occurring as early as the first measurement, at 60 days after inoculation. These results suggest that there is ample potential for psyllids to acquire the pathogen from trees during the asymptomatic phase of infection. If so, this could limit the effectiveness of tree rouging as a disease management tool and would likely explain the rapid spread observed for this disease in the field.
Impacts of climate change on organisms are already apparent, with effects ranging from the individual to ecosystem scales. For organisms engaged in mutualisms, climate may affect population performance directly or indirectly through mediated effects on their mutualists. We tested this hypothesis for two stink bugs, Acrosternum hilare and Murgantia histrionica, and their gut-associated symbionts. We reared these species at two constant temperatures, 25 and 30°C, and monitored population demographic parameters and the presence of gut-associated symbionts with diagnostic PCR primer sets. Both stink bugs lost their respective gut symbionts within two generations at 30°C. In addition, the insect survivorship and reproductive rates of both A. hilare and M. histrionica at 30°C were lower than at 25°C. Other demographic parameters also indicated a decrease in overall insect fitness at the high temperature. Collectively our data showed that the decrease in host fitness was coupled with, and potentially mediated by, symbiont loss at 30°C. This work illustrates the need to better understand the biology of animal-symbiont associations and the consequences of local climate for the dynamics of these interactions.The effect of climate on organisms, communities, and the environment at large has become a pressing issue for biologists and environmental scientists. Recent studies indicate that previous forecasts were conservative in their predictions for the magnitude of global warming (29). Up-to-date models suggest that the global mean surface temperature will increase by 1.8 to 4°C by the year 2100 (11). The ecological impact of such warming is already apparent (35) in the effects seen on species fitness (24), range shifts (22), species interactions (10), and community structure (32).It is important to note that many macroorganisms live in symbiosis with microbes and that host fitness may be affected indirectly by higher temperatures due to the disruption of mutualistic relationships. Some corals, for example, have symbiotic relationships with photosynthesizing dinoflagellates (zoothanxellae) that provide them with nutrients (31). Higher water temperatures in reef ecosystems, among other factors, induce the expulsion of microbial symbionts by the host, resulting in coral bleaching (15). Therefore, it is plausible that observed effects of climate on species distribution or performance might stem from disruption of symbiotic interactions as much as from direct effects on host biology.Despite the current interest in insect-microbe symbioses, the vast majority of such systems have been poorly studied. A group of insects that has recently received some attention are the true bugs (Hemiptera, Pentatomomorpha). Studies in the early 1900s suggested that mutualistic bacteria colonized a portion of the gut of insects in different pentatomomorphan families (9). More specifically, monocultures of bacteria were present in high densities in the crypt-(or cecum-) bearing organ preceding the hindgut of hosts, with different bacterial taxa asso...
Compared to human‐ and wildlife‐transmitted pathogens, less emphasis has been placed on developing models of plant pathogen transmission by insects. Here, we describe the transmission ecology of the bacterium Xylella fastidiosa Wells et al., the causal agent of Pierce’s disease in grapevines, by its leafhopper vectors. First, we performed a meta‐analysis of transmission studies of X. fastidiosa by its two most important vectors in the Western USA, the invasive glassy‐winged sharpshooter, Homalodisca vitripennis Germar, and the native blue‐green sharpshooter, Graphocephala atropunctata Signoret (both Hemiptera: Cicadellidae). The importance of vector number, pathogen acquisition period, and inoculation access period (IAP) for transmission differed between the two species. We fit these transmission datasets to two biologically derived transmission models, i.e., a binomial and a Poisson probability model. The Poisson model provided substantially better fit and produced estimates of H. vitripennis transmission efficiency that were dramatically lower than for G. atropunctata. We also conducted a separate pair of experiments that decoupled vector number from IAP. These experiments supported the results of the meta‐analysis. Interestingly, high vector loads not only increased transmission rate, but also shortened X. fastidiosa incubation period in grapevines. This work provides quantitative estimates of transmission of an economically important pathogen that is analogous to risk models for arthropod‐vectored human and wildlife diseases. In addition, this work suggests that heterogeneous vector loads may accelerate the disease cycle, increasing the potential for secondary spread in vineyards.
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