Competition in depleting resource environments shapes the thermal response of population fitness in a disease vector

Mathematical models that incorporate the temperature dependence of lab-measured life history traits are increasingly used to predict how climatic warming will affect ectotherms, including disease vectors and other arthropods. These temperature-trait relationships are typically measured under laboratory conditions that ignore how conspecific competition in depleting resource environments—a commonly occurring scenario in nature—regulates natural populations. Here, we used laboratory experiments on the mosquito Aedes aegypti, combined with a stage-structured population model, to show that intensified larval competition in ecologically-realistic depleting resource environments can significantly diminish the vector’s maximal population-level fitness across the entire temperature range, cause a 6°C decrease in the optimal temperature for fitness, and contract its thermal niche width by 10°C. Our results provide evidence for future studies to consider competition dynamics under depleting resources when predicting how eukaryotic ectotherms will respond to climatic warming.

Competition in depleting resource environments shapes the thermal response of mosquito population fitness

ABSTRACTA population’s maximal growth rate (rm) depends on the survivorship, development, and reproduction of its individuals. In ectotherms, these (functional) traits respond predictably to temperature, which provides a basis for predicting how climatic warming could affect natural populations, including disease vectors and the diseases they transmit.Such predictions generally arise from mathematical models that incorporate the temperature-dependence of traits (thermal performance curves) measured under laboratory conditions. Therefore, the accuracy of these predictions depends on the relevance of lab-measured trait thermal performance curves to natural conditions. However, the joint effect of temperature and resource availability—another key limiting environmental factor in nature—on traits is largely unknown.We investigated how larval competition for ecologically-realistic depleting resources affects the thermal performance of rm and its underlying life history traits in the disease vector in Aedes aegypti. We show that competition at food concentrations below a certain threshold drastically depresses rm across the entire temperature range, causes it to peak at a lower temperature, and narrows the breadth of temperatures over which rm is positive (the thermal niche breath).This resource-dependence of the thermal performance curve of rm is driven primarily by the fact that competition delays development and increases juvenile mortality. This is compounded by reduced size at maturity, which in turn decreases adult lifespan and fecundity.These results show that intensified larval competition in depleting resource environments can significantly affect the temperature-dependence of rm by modulating the thermal responses of underlying traits in a predictable way. This has important implications for forecasting the effects of climate change on population dynamics in the field of not just disease vectors, but holometabolous insects in general.

Microbiota-mediated competition between pest insects and its application to the evolution-proof protection of crops

Species that share the same resources often avoid costly competition with contextdependent behaviors. This is the case of the invasive insect pest Drosophila suzukii which larvae’s ecological niche overlaps with that of Drosophila melanogaster in ripe, but not rotten, fruit. Previous research showed D. suzukii prevents costly larval competition by not ovipositing in substrates with D. melanogaster eggs. We discovered D. suzukii females respond to cues produced by D. melanogaster adults associated to gut microbiota bacteria. This behavior of D. suzukii varied over time and among populations, revealing subtle condition-dependence. In particular, D. suzukii females that bore D. melanogaster gut bacteria stopped avoiding sites with D. melanogaster cues. The adaptive significance of the behavior was investigated by reproducing experimentally in-fruit larval competition. D. suzukii larvae only suffered from competition with D. melanogaster if the competitor was associated to its microbiota, suggesting D. suzukii has evolved a solution to avoid its offspring develops in challenging environments. We argue that D. suzukii’s competition avoidance behavior has features enabling the design of an evolution-proof repellent to protect crops.

Effects of Interspecific Larval Competition on Developmental Parameters in Nutrient Sources Between Drosophila suzukii (Diptera: Drosophilidae) and Zaprionus indianus

Two invasive drosophilids, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) and Zaprionus indianus (Gupta) (Diptera: Drosophilidae) are expanding their geographic distribution and cohabiting grape production in the Mid-Atlantic. The ecological and economic impact of these two species within vineyards is currently unknown. Zaprionus indianus was presumably not capable of ovipositing directly into grapes because they lack a serrated ovipositor and may use D. suzukii oviposition punctures for depositing their own eggs. Therefore, an interspecific larval competition assay was performed at varying larval densities using commercial medium and four commonly grown wine grapes in Virginia to investigate the impact Z. indianus larvae may have on the mortality and developmental parameters of D. suzukii larvae. Zaprionus indianus did not affect D. suzukii mortality or development parameters even at high interspecific densities when reared in commercial medium, but it did cause higher D. suzukii mortality within grapes. Mortality was also influenced by the variety of grape in which the larvae were reared, with smaller grapes having the highest D. suzukii mortality. Presence of Z. indianus also increased development time to pupariation and adult emergence for most interspecific competition levels compared with the intraspecific D. suzukii controls. Pupal volume was marginally affected at the highest interspecific larval densities. This laboratory study suggests that competition from Z. indianus and grape variety can limit D. suzukii numbers, and the implications on D. suzukii pest management be further verified in the field.

Oviposition site attraction of Aedes albopictus to sites with conspecific and heterospecific larvae during an ongoing invasion in Medellín, Colombia

Background Aedes aegypti and Aedes albopictus are two globally invasive vectors with similar ecological niches. Encounters between them can result in either competitive exclusion or stable co-existence, but it is unclear what drives these variable outcomes. Larval competition in favor of Ae. albopictus is a main hypothesis for the competitive exclusion of Ae. aegypti observed in some regions. However, the role of oviposition preference in determining the degree of competitive larval interactions in the field is not well understood. In this study, we used a combination of mark-release-recapture methods with ovitraps in the open-field and a semi-field cage to test whether gravid Ae. albopictus seek oviposition sites in response to the presence, species, and density of either conspecific or heterospecific Ae. aegypti larvae in the aquatic habitat. We conducted our study in Medellín, Colombia, where Ae. aegypti is a long-term resident and Ae. albopictus is a recent invader. Results In the open-field and semi-field cage experiments, gravid Ae. albopictus showed strong preference for ovitraps with larvae over those without. They consistently preferred ovitraps with higher density of conspecific (Ae. albopictus) larvae and low density of heterospecific (Ae. aegypti) larvae over traps with no larvae or high density of heterospecific (Ae. aegypti) larvae. In the semi-field cage experiment, traps with low density of Ae. albopictus were not preferred more or less than any other trap, but in the open-field experiment they were preferred over traps without larvae. Conclusions We demonstrate, through open-field and semi-field cage experiments, that Ae. albopictus are more attracted to oviposition sites with larvae and that the combination of species and density of larvae influence attraction. This demonstrated preference could increase interspecific larval competition as Ae. albopictus actively seek containers with conspecific and heterospecific larvae. Any resulting competition with Ae. aegypti may favor one species over the other and alter the distribution or abundance of both. Because these species vary in vectorial capacity and insecticide resistance, effects of interspecific competition could ultimately impact arbovirus transmission rates and the success of vector control efforts.

Impact of Larval Competition on Life-History Traits of the Black Soldier Fly (Diptera: Stratiomyidae)

The black soldier fly, Hermetia illucens (L.), is economically important due to its use in waste management and as an alternative protein source for livestock, poultry, and aquaculture. While industry promotes mass production of the black soldier fly, little is known about the impact of larval competition on development time, resulting immature and adult weight, or adult longevity. The goal of this research was to examine the life-history traits of black soldier flies when reared at four densities (500, 1,000, 1,500, and 2,000 larvae/4-liter container) provided 54-g Gainesville diet at 70% moisture (feed rates of 0.027, 0.036, 0.054, and 0.108 g) every other day. Results were as expected with the lowest larval density (500) producing heavier individuals (by 26%) than the greatest larval density (2,000) across all life stages. In addition to weights, larvae reared at the lowest density developed 63% faster than those reared at the greatest density. In regard to pupal development time, those reared at the lowest larval density developed 3% slower than the greatest density. A 21% difference between the two extreme densities was found in survivorship to prepupal stage, with the lowest larval density having the greatest survivorship (92%) compared with the greatest larval density (70%). All densities displayed over 90% adult emergence rates. Such information is vital for optimization of the process of converting waste products to protein at an industrial scale with the black soldier fly.

The ecological and epidemiological consequences of reproductive interference between the vectors Aedes aegypti and Aedes albopictus

Vector ecology is integral to understanding the transmission of vector-borne diseases, with processes such as reproduction and competition pivotal in determining vector presence and abundance. The arbovirus vectors Aedes aegypti and Aedes albopictus compete as larvae, but this mechanism is insufficient to explain patterns of coexistence and exclusion. Inviable interspecies matings—known as reproductive interference—is another candidate mechanism. Here, we analyse mathematical models of mosquito population dynamics and epidemiology which include two Aedes -specific features of reproductive interference. First, as these mosquitoes use hosts to find mates, reproductive interference will only occur if the same host is visited. Host choice will, in turn, be determined by behavioural responses to host availability. Second, females can become sterilized after mis-mating with heterospecifics. We find that a species with an affinity for a shared host will suffer more from reproductive interference than a less selective competitor. Costs from reproductive interference can be ‘traded-off’ against costs from larval competition, leading to competitive outcomes that are difficult to predict from empirical evidence. Sterilizations of a self-limiting species can counterintuitively lead to higher densities than a competitor suffering less sterilization. We identify that behavioural responses and reproductive interference mediate a concomitant relationship between vector ecological dynamics and epidemiology. Competitors with opposite behavioural responses can maintain disease where human hosts are rare, due to vector coexistence facilitated by a reduced cost from reproductive interference. Our work elucidates the relative roles of the competitive mechanisms governing Aedes populations and the associated epidemiological consequences.

The ecological and epidemiological consequences of reproductive interference between the vectors Aedes aegypti and Aedes albopictus

Vector ecology is integral to understanding the transmission of vector-borne diseases, with processes such as reproduction and competition pivotal in determining vector presence and abundance. The arbovirus vectors Aedes aegypti and Aedes albopictus compete as larvae, but this mechanism is insufficient to explain patterns of coexistence and exclusion. Inviable interspecies matings - known as reproductive interference - is another candidate mechanism. Here, we analyse mathematical models of mosquito population dynamics and epidemiology which include two Aedes-specific features of reproductive interference. First, as these mosquitoes use hosts to find mates, reproductive interference will only occur if the same host is visited. Host choice will, in turn, be determined by functional responses to host availability. Second, females can become sterilised after mis-mating with heterospecifics. We find that a species with an affinity for a shared host will suffer more from reproductive interference than a less selective competitor. Costs from reproductive interference can be “traded-off” against costs from larval competition, leading to competitive outcomes difficult to predict from empirical evidence. Sterilisations of a self-limiting species can counter-intuitively lead to higher densities than a competitor suffering less sterilisation. We identify that functional responses and reproductive interference mediate a concomitant relationship between vector ecological dynamics and epidemiology. Competitors with opposite functional responses can maintain disease where human hosts are rare, due to vector coexistence facilitated by a reduced cost from reproductive interference. Our work elucidates the relative roles of the competitive mechanisms governing Aedes populations and the associated epidemiological consequences.

Larval foraging decisions in competitive heterogeneous environments accommodate diets that support egg-to-adult development in a polyphagous fly

In holometabolous insects, larval nutrition is a key factor underpinning development and fitness. Heterogeneity in the nutritional environment and larval competition can force larvae to forage in suboptimal diets, with potential downstream fitness effects. Little is known about how larvae respond to competitive heterogeneous environments, and whether variation in these responses affects current and next generations. Here, we designed nutritionally heterogeneous foraging arenas by modifying nutrient concentration, where groups of the polyphagous fruit fly Bactrocera tryoni could forage freely at various levels of larval competition. Larval foraging preferences were highly consistent and independent of larval competition, with greatest foraging propensity for high (100%) followed by intermediate (80% and 60%) nutrient concentration diets, and avoidance of lower concentration diets (less than 60%). We then used these larval preferences (i.e. 100%, 80% and 60% diets) in fitness assays in which larvae competition was maintained constant, and showed that nutrient concentrations selected by the larvae in the foraging trials had no effect on fitness-related traits such as egg hatching and pupation success, adult flight ability, sex ratio, percentage of emergence, nor on adult cold tolerance, fecundity and next-generation pupal weight. These results support the idea that polyphagous species can exploit diverse hosts and nutritional conditions with minimal fitness costs to thrive in new environments.