Timing alters how a heat shock affects a host-parasitoid interaction.

Abiotic factors' effects on species are now well-studied, yet they are still often difficult to predict, especially for strongly interacting species. If these altered abiotic factors and species interactions occur as discrete events in time, such complications may occur because of the events' relative timing. One such discrete abiotic factor is the short-duration, large magnitude increase in temperature called a heat shock. This study investigates how the timing of heat shocks affects the successful attack and reproduction of a parasitoid wasp (Aphidius ervi) attacking its host, the pea aphid (Acyrthosiphon pisum). We tested three relative timings: 1) heat shock before the wasp attacks hosts, 2) heat shock while the wasp is foraging, and 3) heat shock after the wasp has attacked hosts. In each scenario we compared wasp mummy production (pupal stage) with and without a heat shock. Our results showed that a heat shock had the largest effect when it occurred while wasps actively foraged, with fewer mummies produced when exposed to a heat shock compared to the no heat shock control. Follow-up behavioral tests suggest this was caused by wasps becoming inactive during heat shocks. In contrast, when heat shocks were applied three days before or after foraging, we found no difference in mummy production between the heat shock treatment and no heat shock control. These results show the potential importance of timing when considering the ramifications of an altered abiotic factor, especially with relatively discrete abiotic events and interactions.

Combined effects of night warming and light pollution on predator-prey interactions.

Interactions between multiple anthropogenic environmental changes can drive non-additive effects in ecological systems, and the non-additive effects can in turn be amplified or dampened by spatial covariation among environmental changes. We investigated the combined effects of night-time warming and light pollution on pea aphids and two predatory ladybeetle species. As expected, neither night-time warming nor light pollution changed the suppression of aphids by the ladybeetle species that forages effectively in darkness. However, for the more-visual predator, warming and light had non-additive effects in which together they caused much lower aphid abundances. These results are particularly relevant for agriculture near urban areas that experience both light pollution and warming from urban heat islands. Because warming and light pollution can have non-additive effects, predicting their possible combined consequences over broad spatial scales requires knowing how they co-occur. We found that night-time temperature change since 1949 covaried positively with light pollution, which has the potential to increase their non-additive effects on pea aphid control by 70% in US alfalfa. Our results highlight the importance of non-additive effects of multiple environmental factors on species and food webs, especially when these factors co-occur.

Multilevel statistical models and the analysis of experimental data.

Data sets from ecological experiments can be difficult to analyze, due to lack of independence of experimental units and complex variance structures. In addition, information of interest may lie in complicated contrasts among treatments, rather than direct output from statistical tests. Here, we present a statistical framework for analyzing data sets containing non-independent experimental units and differences in variance among treatments (heteroscedasticity) and apply this framework to experimental data on interspecific competition among three tadpole species. Our framework involves three steps: (1) use a multilevel regression model to calculate coefficients of treatment effects on response variables; (2) combine coefficients to quantify the strength of competition (the target information of our experiment); and (3) use parametric bootstrapping to calculate significance of competition strengths. We repeated this framework using three multilevel regression models to analyze data at the level of individual tadpoles, at the replicate level, and at the replicate level accounting for heteroscedasticity. Comparing results shows the need to correctly specify the statistical model, with the model that accurately accounts for heteroscedasticity leading to different conclusions from the other two models. This approach gives a single, comprehensive analysis of experimental data that can be used to extract informative biological parameters in a statistically rigorous way.

The expanding role of movement behavior in insect conservation ecology.

Insect conservation will rely on incorporating behavior into management. Dispersal behavior is one such vital behavior for conservation, but it is generally poorly understood at the species level. We reviewed recent literature to identify intricacies that complicate including dispersal behavior in conservation management. Many previous theories used to predict the need to disperse do not explicitly address successful dispersal. Additionally, we found identifying barriers to dispersal as a possible way to improve conservation management, but it is necessary to consider multiple parts of dispersal (emigration, matrix navigation, immigration). Species' dispersal is context-specific. Therefore, to effectively incorporate dispersal behavior into conservation, more research is necessary on individual species' responses to their environment, how they navigate to optimal sites, and their fitness after dispersal events.

Self-perpetuating ecological-evolutionary dynamics in an agricultural host-parasite system.

Ecological and evolutionary processes may become intertwined when they operate on similar time scales. Here we show ecological-evolutionary dynamics between parasitoids and aphids containing heritable symbionts that confer resistance against parasitism. In a large-scale field experiment, we manipulated the aphid's host plant to create ecological conditions that either favoured or disfavoured the parasitoid. The result was rapid evolutionary divergence of aphid resistance between treatment populations. Consistent with ecological-evolutionary dynamics, the resistant aphid populations then had reduced parasitism and increased population growth rates. We fit a model to quantify costs (reduced intrinsic rates of increase) and benefits of resistance. We also performed genetic assays on 5 years of field samples that showed persistent but highly variable frequencies of aphid clones containing protective symbionts; these patterns were consistent with simulations from the model. Our results show (1) rapid evolution that is intertwined with ecological dynamics and (2) variation in selection that prevents traits from becoming fixed, which together generate self-perpetuating ecological-evolutionary dynamics.

Correction: Aphid symbionts and endogenous resistance traits mediate competition between rival parasitoids.

[This corrects the article DOI: 10.1371/journal.pone.0180729.].

Salinity Improves Performance and Alters Distribution of Soybean Aphids.

We know numerous abiotic factors strongly influence crop plants. Yet we often know much less about abiotic effects on closely interacting organisms including herbivorous insects. This lack of a whole-system perspective may lead to underestimating the threats from changing factors. High soil salinity is a specific example that we know threatens crop plants in many places, but we need to know much more about how other organisms are also affected. We investigated how salinity affects the soybean aphid (SBA; Aphis glycines Matsumura; Hemiptera: Aphididae) on soybean plants (Glycine max [L.] Merr.; Fabales: Fabaceae) grown across a range of saline conditions. We performed four complementary greenhouse experiments to understand different aspects of how salinity might affect SBA. We found that as salinity increased both population size and fecundity of SBA increased across electrical conductivity values ranging from 0.84 to 8.07 dS m-1. Tracking individual aphids we also found they lived longer and produced more offspring in high saline conditions compared to the control. Moreover, we found that salinity influenced aphid distribution such that when given the chance aphids accumulated more on high-salinity plants. These results suggest that SBA could become a larger problem in areas with higher salinity and that those aphids may exacerbate the negative effects of salinity for soybean production.

Contrasting the potential effects of daytime versus nighttime warming on insects.

Mean increases in temperatures associated with climate change are largely driven by increases in minimum (nighttime) temperatures; however, most climate change studies disproportionately increase maximum (daytime) temperatures. We review current literature to compare the potential effects of increasing daytime and nighttime temperatures on insects and their interactions within ecological communities. Although few studies have explicitly addressed the effects of nighttime warming, we draw from broader literature on how insects are affected by temperature to identify possible mechanisms that the timing (day or night) of warming may affect insects. Specifically, we discuss daily temperature variation, thermal performance curves, behaviour and activity patterns, nighttime recovery from hot days, and bottom-up effects mediated by plants. Although limited, the existing evidence suggests nighttime and daytime warming can have different effects, and thus we encourage scientists to use the most realistic warming treatments possible to truly understand how insects and their communities will be affected by climate change.

Aphid symbionts and endogenous resistance traits mediate competition between rival parasitoids.

Insects use endogenous mechanisms and infection with protective symbionts to thwart attacks from natural enemies. Defenses that target specific enemies, however, potentially mediate competition between rivals and thereby impact community composition. Following its introduction to North America to control pea aphids (Acyrthosiphon pisum), the parasitoid Aphidius ervi competitively displaced other parasitoids, except for the native Praon pequodorum. The pea aphid exhibits tremendous clonal variation in resistance to A. ervi, primarily through infection with the heritable bacterial symbiont Hamiltonella defensa, although some symbiont-free aphid genotypes encode endogenous resistance. Interestingly, H. defensa strains and aphid genotypes that protect against A. ervi, provide no protection against the closely related, P. pequodorum. Given the specificity of aphid defenses, we hypothesized that aphid resistance traits may contribute to the continued persistence of P. pequodorum. We conducted multiparasitism assays to determine whether aphid resistance traits mediate internal competition between these two solitary parasitoid species, but found this was not the case; P. pequodorum was the successful internal competitor across lines varying in susceptibility to A. ervi. Next, to determine whether resistance traits influence competitive interactions resulting in the stable persistence of P. pequodorum, we established replicated cages varying in the proportion of resistant aphids and recorded successful parasitism for each wasp species over time. As expected, A. ervi outcompeted P. pequodorum in cages containing only susceptible aphids. However, P. pequodorum not only persisted, but was the superior competitor in populations containing any proportion (20-100%) of resistant aphids (20-100%). Smaller scale, better replicated competition cage studies corroborated this finding, and no-competition and behavioral assays provide insight into the processes mediating competition. Genetic variation, including that acquired via infection with protective symbionts, may provide a supply of hosts susceptible only to particular enemies, mediating competition with effects on community richness and stability.

The Effects of Salinity on the Herbivorous Crop Pest Tetranychus urticae (Trombidiformes: Tetranychidae) on Soybean and Corn.

Many environmental factors, including soil characteristics, are critical for plants, herbivorous arthropods, and their interactions. Despite increasing evidence that soil salinity drastically impacts plants, little is known about how salinity affects the herbivorous arthropod pests feeding on those plants. We investigated how soil salinity affects the twospotted spider mite (Tetranychus urticae Koch) feeding on corn (Zea mays L.) and soybean (Glycine max L.). We performed two greenhouse studies, one focusing on the impact of salinity on individual mite fecundity over a period of 3 d and the other focusing on population growth of T. urticae over 7 d. Both experiments were performed across varying salinity levels; electrical conductivity values ranged from 0.84 to 8.07 dS m-1. We also performed the 3-d fecundity experiment in the field, across naturally varying saline conditions. Overall, the twospotted spider mite performed better as salinity increased; both fecundity and population growth tended to have a positive linear correlation with salinity. These studies suggest that salinity can be important for herbivores, just as it is for plants. Moreover, the negative effects of soil salinity on crop plants in agroecosystems may be further compounded by a greater risk of pest problems. Salinity may be another important environmental stressor that can directly influence crop production while also indirectly influencing herbivorous pests.

Specificity of Multi-Modal Aphid Defenses against Two Rival Parasitoids.

Insects are often attacked by multiple natural enemies, imposing dynamic selective pressures for the development and maintenance of enemy-specific resistance. Pea aphids (Acyrthosiphon pisum) have emerged as models for the study of variation in resistance against natural enemies, including parasitoid wasps. Internal defenses against their most common parasitoid wasp, Aphidius ervi, are sourced through two known mechanisms- 1) endogenously encoded resistance or 2) infection with the heritable bacterial symbiont, Hamiltonella defensa. Levels of resistance can range from nearly 0-100% against A. ervi but varies based on aphid genotype and the strain of toxin-encoding bacteriophage (called APSE) carried by Hamiltonella. Previously, other parasitoid wasps were found to commonly attack this host, but North American introductions of A. ervi have apparently displaced all other parasitoids except Praon pequodorum, a related aphidiine braconid wasp, which is still found attacking this host in natural populations. To explain P. pequodorum's persistence, multiple studies have compared direct competition between both wasps, but have not examined specificity of host defenses as an indirectly mediating factor. Using an array of experimental aphid lines, we first examined whether aphid defenses varied in effectiveness toward either wasp species. Expectedly, both types of aphid defenses were effective against A. ervi, but unexpectedly, were completely ineffective against P. pequodorum. Further examination showed that P. pequodorum wasps suffered no consistent fitness costs from developing in even highly 'resistant' aphids. Comparison of both wasps' egg-larval development revealed that P. pequodorum's eggs have thicker chorions and hatch two days later than A. ervi's, likely explaining their differing abilities to overcome aphid defenses. Overall, our results indicate that aphids resistant to A. ervi may serve as reservoirs for P. pequodorum, hence contributing to its persistence in field populations. We find that specificity of host defenses and defensive symbiont infections, may have important roles in influencing enemy compositions by indirectly mediating the interactions and abundance of rival natural enemies.

The role of vision and color in the close proximity foraging behavior of four coccinellid species.

The role of vision and color in close-proximity foraging behavior was investigated for four species of lady beetles: Coccinella septempunctata, Hippodamia convergens, Harmonia axyridis, and Coleomegilla maculata. The effect of light level and color cues on consumption rates varied among the four predator species. The consumption rates of these predators on the pea aphid Acyrthosiphon pisum (Harris) was measured under light and dark conditions. C. septempunctata,H. convergens, and Ha. axyridis consumed significantly more aphids in the light than in the dark, while the consumption rate of Col. maculata was not affected by light level. Foraging ability was also measured on red and green color morphs of the pea aphid on red, green, and white backgrounds. C. septempunctata consumed significantly more of the aphid morph that contrasted with the background color, and showed no difference between morphs on the white background. H. axyridis consumed significantly more red morph aphids regardless of background. The remaining two species showed no difference in consumption rates on the two color morphs. The variation in the use of visual cues demonstrates how different species of predators can exhibit different foraging behaviors when searching for the same prey.

On their best behavior: how animal behavior can help determine the combined effects of species interactions and climate change.

The increasingly appreciated link between climate change and species interactions has the potential to help us understand and predict how organisms respond to a changing environment. As this connection grows, it becomes even more important to appreciate the mechanisms that create and control the combined effect of these factors. However, we believe one such important set of mechanisms comes from species' behavior and the subsequent trait-mediated interactions, as opposed to the more often studied density-mediated effects. Behavioral mechanisms are already well appreciated for mitigating the separate effects of the environment and species interactions. Thus, they could be at the forefront for understanding the combined effects. In this review, we (1) show some of the known behaviors that influence the individual and combined effects of climate change and species interactions; (2) conceptualize general ways behavior may mediate these combined effects; and (3) illustrate the potential importance of including behavior in our current tools for predicting climate change effects. In doing so, we hope to promote more research on behavior and other mechanistic factors that may increase our ability to accurately predict climate change effects.

Rag1 aphid resistant soybeans alter the movement and distribution of soybean aphid (Hemiptera: Aphididae).

Herbivorous insects often move and distribute according to the quality of the plant they are on, and this behavior could influence interactions with plants bred for herbivore resistance. However, when an insect is normally considered sedentary, less is known about the potential importance of movement. We performed experiments to determine if a resistant soybean variety alters the movement and distribution, both within and between plants, of the soybean aphid Aphis glycines Matsumura. We did this by counting apterous aphids on leaves of resistant and susceptible soybean plants across several days. In individual plant tests aphid distribution was different between susceptible and resistant soybeans. Most notably aphids on resistant plants were quickly found off the original leaf on which they were placed and were ultimately distributed throughout the resistant soybean. Aphids on susceptible plants, however, tended to stay on their initial leaf of placement. Follow up experiments indicated this was primarily because of the movement of individuals and not differential demography on various plant parts. In experiments where aphids were able to walk to an adjacent plant there appeared to be a net movement of aphids off resistant plants and on to susceptible plants. Aphid populations on susceptible plants were higher when the plant was adjacent to a resistant plant than when adjacent to another susceptible plant. The effect of resistant plants on aphid movement and distribution could lead to unintended side-effects such as greater spread of plant viruses or altered effectiveness of biological control agents.

Impact of Rag1 aphid resistant soybeans on Binodoxys communis (Hymenoptera: Braconidae), a parasitoid of soybean aphid (Hemiptera: Aphididae).

Multiple strategies are being developed for pest management of the soybean aphid, Aphis glycines Matsumura; however, there has been little published research thus far to determine how such strategies may influence each other, thereby complicating their potential effectiveness. A susceptible soybean (Glycine max L.) variety without the Rag1 gene and a near isogenic resistant soybean variety with the Rag1 gene were evaluated in the laboratory for their effects on the fitness of the soybean aphid parasitoid, Binodoxys communis (Gahan). The presence or absence of the Rag1 gene was verified by quantifying soybean aphid growth. To test for fitness effects, parasitoids were allowed to attack soybean aphids on either a susceptible or resistant plant for 24 h and then aphids were kept on the same plant throughout parasitoid development. Parasitoid fitness was measured by mummy and adult parasitoid production, adult parasitoid emergence, development time, and adult size. Parasitoids that attacked soybean aphids on susceptible plants produced more mummies, more adult parasitoids, and had a higher emergence rate compared with those on resistant plants. Adult parasitoids that emerged from resistant plants took 1 d longer and were smaller compared with those from susceptible plants. This study suggests that biological control by B. communis may be compromised when host plant resistance is widely used for pest management of soybean aphids.

Response of coccinellid larvae to conspecific and heterospecific larval tracks: a mechanism that reduces cannibalism and intraguild predation.

Cannibalism, where one species feeds on individuals of its own species, and intraguild predation (IGP), where a predator feeds on other predatory species, can both pose significant threats to natural enemies and interfere with their biological control of pests. Behavioral mechanisms to avoid these threats, however, could help maintain superior pest control. Here, we ask whether larvae of Coccinella septempunctata (Coleoptera: Coccinellidae) and Harmonia axyridis (Coleoptera: Coccinellidae) respond to larval tracks deposited by the other and whether this behavioral response reduces the threat of cannibalism and IGP. In petri dish experiments, we show that both H. axyridis and C. septempunctata avoid foraging in areas with conspecific larval tracks. Using a method of preventing larvae from depositing tracks, we then demonstrate that the frequency of cannibalism is greater for both species when larvae are prevented from depositing tracks compared with when the tracks are deposited. For multi-species interactions we show in petri dish experiments that C. septempunctata avoids H. axyridis larval tracks but H. axyridis does not avoid C. septempunctata larval tracks, demonstrating an asymmetry in response to larval tracks that parallels the asymmetry in aggressiveness between these species as intraguild predators. On single plants, we show that the presence of H. axyridis larval tracks reduces the risk of IGP by H. axyridis on C. septempunctata. Our study suggests that larval tracks can be used in more ways than previously described, in this case by changing coccinellid larval behavior in a way that reduces cannibalism and IGP.

Species response to environmental change: impacts of food web interactions and evolution.

How environmental change affects species abundances depends on both the food web within which species interact and their potential to evolve. Using field experiments, we investigated both ecological and evolutionary responses of pea aphids (Acyrthosiphon pisum), a common agricultural pest, to increased frequency of episodic heat shocks. One predator species ameliorated the decrease in aphid population growth with increasing heat shocks, whereas a second predator did not, with this contrast caused by behavioral differences between predators. We also compared aphid strains with stably inherited differences in heat tolerance caused by bacterial endosymbionts and showed the potential for rapid evolution for heat-shock tolerance. Our results illustrate how ecological and evolutionary complexities should be incorporated into predictions of the consequences of environmental change for species' populations.