Agricultural soil legacy influences multitrophic interactions between crops, their pathogens and pollinators.

Soil legacy influences plant interactions with antagonists and below-ground mutualists. Plant-antagonist interactions can jeopardize plant-pollinator interactions, while soil mutualists can enhance plant-pollinator interactions. This suggests that soil legacy, either directly or mediated through plant symbionts, affects pollinators. Despite the importance of pollinators to natural and managed ecosystems, information on how soil legacy affects plant-pollinator interactions is limited. We assessed effects of soil management legacy (organic versus conventional) on floral rewards and plant interactions with wild pollinators, herbivores, beneficial fungi and pathogens. We used an observational dataset and structural equation models to evaluate hypothesized relationships between soil and pollinators, then tested observed correlations in a manipulative experiment. Organic legacy increased mycorrhizal fungal colonization and improved resistance to powdery mildew, which promoted pollinator visitation. Further, soil legacy and powdery mildew independently and interactively impacted floral traits and floral reward nutrients, which are important to pollinators. Our results indicate that pollination could be an overlooked consequence of soil legacy and suggests opportunity to develop long-term soil management plans that benefit pollinators and pollination.

Semiochemical Release and Ontogenetic Changes in a Primary Scent Gland of Podisus maculiventris.

The spined shoulder bug, Podisus maculiventris, is a generalist predator studied for its biocontrol potential. Despite our growing understanding of gland development, the conditions that elicit releases are largely unknown. To determine if male age or gland development affects the chemical composition and release behavior, we dissected adult male bugs and profiled the chemical composition of the male DAG 1, 7, and 14 d post-eclosion. To determine if gland development is related to sexual maturity, we counted the number of sperm present in the seminal vesicles at the same time points. Finally, we measured the diurnal release patterns of different aged males and in various male-female combinations. We observed that newly eclosed adults have under-developed glands and male seminal vesicles contained few sperm. One week post-eclosion the DAG contained previously reported semiochemical compounds and males contained many sperm. Mirroring the trend in reproductive maturation and gland development, the number of semiochemical releases increased with age and the majority of releases followed a scotophase pattern unaffected by sexual composition. These findings link male age to 1) dorsal abdominal gland development 2) release behavior and 3) sexual maturity, which will help our understanding of when these olfactory cues are present for other organisms, like prey, to perceive. Given the results, releasing adults that are at least 1 week post eclosion will maximize the non-consumptive effects of this biocontrol agent.

Light at night disrupts trophic interactions and population growth of lady beetles and pea aphids.

Natural variation in light has historically correlated with seasonality, providing an honest cue to organisms with seasonal life history cycles. However, with the onset of widespread light at night (LAN), the reliability of light as a cue has decreased in polluted areas, making its timing or intensity potentially clash with temperature trends. These clashing cues may influence biological systems on multiple levels. Yet, a few studies have connected behavioral underpinnings and larger community-level processes, resulting in a knowledge gap bridging individual-, population-, and community-level responses to mismatched cues. We experimentally investigated impacts of cool temperature and LAN on a lady beetle-aphid-fava system to test how light and temperature influenced aphid population growth and their underlying behavioral drivers. We used Coccinella septempunctata and Coleomegilla maculata beetles to understand the interaction of the environment and predation on pea aphid (Acyrthosiphon pisum) population growth. Aphids and their predators reacted differently to variation in light and temperature, influencing the strength of aphid-driven and predator-driven dynamics in the different conditions. We observed evidence of aphid-driven dynamics in the cool, light conditions where aphids excel and exhibited strong anti-predator behavior. In contrast, we found stronger predator-driven dynamics in warm conditions where lady beetle predatory success was higher. Overall, we found that LAN has context-dependent effects on insect communities due to the varied responses each player has to its environment.

Genetic Variation in Parental Effects Contributes to the Evolutionary Potential of Prey Responses to Predation Risk.

AbstractDespite the ubiquity of parental effects and their potential effect on evolutionary dynamics, their contribution to the evolution of predator-prey interactions remains poorly understood. Using quantitative genetics, here we demonstrate that parental effects substantially contribute to the evolutionary potential of larval antipredator responses in a leaf beetle (Leptinotarsa decemlineata). Previous research showed that larger L. decemlineata larvae elicit stronger antipredator responses, and mothers perceiving predators improved offspring responses by increasing intraclutch cannibalism-an extreme form of offspring provisioning. We now report substantial additive genetic variation underlying maternal ability to induce intraclutch cannibalism, indicating the potential of this adaptive maternal effect to evolve by natural selection. We also show that paternal size, a heritable trait, affected larval responses to predation risk but that larval responses themselves had little additive genetic variation. Together, these results demonstrate how larval responses to predation risk can evolve via two types of parental effects, both of which provide indirect sources of genetic variation for offspring traits.

Proportional fitness loss and the timing of defensive investment: a cohesive framework across animals and plants.

The risk of consumption is a pervasive aspect of ecology and recent work has focused on synthesis of consumer-resource interactions (e.g., enemy-victim ecology). Despite this, theories pertaining to the timing and magnitude of defenses in animals and plants have largely developed independently. However, both animals and plants share the common dilemma of uncertainty of attack, can gather information from the environment to predict future attacks and alter their defensive investment accordingly. Here, we present a novel, unifying framework based on the way an organism's ability to defend itself during an attack can shape their pre-attack investment in defense. This framework provides a useful perspective on the nature of information use and variation in defensive investment across the sequence of attack-related events, both within and among species. It predicts that organisms with greater proportional fitness loss if attacked will gather and respond to risk information earlier in the attack sequence, while those that have lower proportional fitness loss may wait until attack is underway. This framework offers a common platform to compare and discuss consumer effects and provides novel insights into the way risk information can propagate through populations, communities, and ecosystems.

Constitutive and herbivore-induced plant defences regulate herbivore population processes.

Herbivore-induced plant defences regulated by the phytohormones jasmonic acid (JA) and salicylic acid (SA) are predicted to influence herbivore population dynamics, in part because they can operate in a density-dependent manner. While there is ample evidence that herbivore-induced plant responses affect individual performance and growth of herbivores, whether they scale-up to regulate herbivore population dynamics is still unclear. We evaluated the consequences of variation in plant defences 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 JA and SA 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 defences by using genetically modified lines of tomato plants (Solanum lycopersicum) with elevated or suppressed jasmonate-dependent defences. Jasmonate-insensitive plants cannot induce the defences regulated by the JA pathway, while jasmonate-overexpressing plants constitutively express jasmonate-dependent defences. We found that jasmonate defences 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. Jasmonate-overexpressing plants showed high JA-dependent constitutive levels of resistance and were unable to activate the SA pathway in response to aphid feeding. In contrast, jasmonate-insensitive plants increased aphid reproduction, shortened 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 defences, but induced the SA pathway in a density-dependent manner, which resulted in negative density-dependent aphid population growth. Aphid feeding on jasmonate-insensitive and jasmonate-overexpressing plants differentially activated the salicylate pathway, revealing a negative crosstalk between the defensive phytohormones JA and SA. By muting or enhancing jasmonate-mediated responses and quantifying SA phytohormone induction, we demonstrated that plant defences are a key factor driving not only the performance, but also the density dependence processes and population growth of herbivores.

Plant genotypic diversity interacts with predation risk to influence an insect herbivore across its ontogeny.

A growing number of studies have manipulated intraspecific plant diversity and found dramatic changes in the densities of associated insect herbivores and their predators. While these studies have been essential for quantifying the net ecological consequences of intraspecific plant diversity, they have been less effective at uncovering the ways in which plant diversity alters trophic interactions within arthropod communities. We manipulated intraspecific plant diversity and predation risk in the field in a factorial design to reveal how a mixture of plant genotypes changes the response of an herbivorous beetle (Leptinotarsa decemlineata) to a common stink bug predator (Podisus maculiventris). We repeated the manipulations twice across the ontogeny of the beetle to examine how the effects of diversity on the predator-prey interaction differ between larval and adult stages. We found that intraspecific plant diversity, mixtures of susceptible and resistant varieties of potato (Solanum tuberosum), reduced larval survival by 20% and adult oviposition by 34%, which surprisingly put survival and oviposition lower in the mixed-genotype plots than in the resistant monocultures. Moreover, we found that predation risk reduced larval survival 25% and 11% in resistant and susceptible monocultures, respectively, but had no effect in the mixture. This result indicated that our genotypic mixing treatment interacted nonadditively with predation risk such that plant diversity altered the predator-prey interaction by changing the responses of the beetles to their stink bug predators. In addition, even though predation risk reduced larval survival, it increased adult overwintering survival by 9%, independently of plant treatment, suggesting that these interactions change through ontogeny. A key implication of our study is that plant diversity influences arthropod communities not only by changing resource quality, as past studies have suggested, but also by changing interactions between species within the arthropod community.

Host-choice reduces, but does not eliminate, the negative effects of a multi-species diet for an herbivorous beetle.

A consequence of plant diversity is that it can allow or force herbivores to consume multiple plant species, which studies indicate can have major effects on herbivore fitness. An underappreciated but potentially important factor modulating the consequences of multi-species diets is the extent to which herbivores can choose their diets versus being forced to consume specific host-plant sequences. We examined how host-selection behavior alters the effects of multi-species diets using the Colorado potato beetle (Leptinotarsa decemlineata) and diets of potato plants (Solanum tuberosum), tomato plants (S. lycopersicum), or both. When we gave beetles simultaneous access to both plants, allowing them to choose their diets, their final mass was within 0.1% of the average mass across both monocultures and 43.6% lower than mass on potato, the superior host in monoculture. This result indicates these beetles do not benefit from a mixed diet, and that the presence of tomato, an inferior but suitable host, makes it difficult to use potato. In contrast, when we forced beetles to switch between host species, their final mass was 37.8% less than the average of beetles fed constant diets of either host species and within 3.5% of the mass on tomato even though they also fed on potato. This indicates preventing host-selection behavior magnified the negative effects of this multi-species diet. Our results imply that ecological contexts that constrain host-selection or force host-switches, such as communities with competition or predation, will lead plant species diversity to reduce the performance of insect herbivores.

The effect of predator presence on the behavioral sequence from host selection to reproduction in an invulnerable stage of insect prey.

Predator-prey interactions primarily focus on prey life-stages that are consumed. However, animals in less vulnerable life-stages might also be influenced by the presence of a predator, making our understanding of predation-related impacts across all life-stages of prey essential. It has been previously demonstrated that Podisus maculiventris is a voracious predator of eggs and larvae of Leptinotarsa decemlineata, and that larvae will alter their behavior to avoid predation. However, the adult beetles are not readily consumed by P. maculiventris, raising the question of whether they will respond to predators to protect themselves or their offspring. Here, we examine the effect of predation risk by P. maculiventris, on three adult behaviors of L. decemlineata; colonization, oviposition, and feeding, and the resulting impact on host plant damage. In an open-field test, there was no difference in natural beetle colonization between plots with predation risk and control treatments. However, subsequent host plant damage by adult beetles was 63.9% less in predation risk treatments. Over the lifetime of adult beetles in field mesocosms, per capita feeding was 23% less in the predation risk treatment. Beetle oviposition was 37% less in the presence of predators in a short-term, greenhouse assay, and marginally reduced in longer term field mesocosms. Our results indicate that predation risk can drive relatively invulnerable adult herbivores to adjust behaviors that affect themselves (feeding) and their offspring (oviposition). Thus, the full impact of predator presence must be considered across the prey life cycle.

Maternally induced intraclutch cannibalism: an adaptive response to predation risk?

Theory on condition-dependent risk-taking indicates that when prey are in poor condition, their anti-predator responses should be weak. However, variation in responses resulting from differences in condition is generally considered an incidental by-product of organisms living in a heterogeneous environment. Using Leptinotarsa decemlineata beetles and stinkbug (Podisus maculiventris) predators, we hypothesised that in response to predation risk, parents improve larval nutritional condition and expression of anti-predator responses by promoting intraclutch cannibalism. We showed that mothers experiencing predation risk increase production of unviable trophic eggs, which assures provisioning of an egg meal to the newly hatched offspring. Next, we experimentally demonstrated that egg cannibalism reduces L. decemlineata vulnerability to predation by improving larval nutritional condition and expression of anti-predator responses. Intraclutch cannibalism in herbivorous insects might be a ubiquitous strategy, aimed to overcome the dual challenge of feeding on protein-limited diets while living under constant predation threat.

Plant defences limit herbivore population growth by changing predator-prey interactions.

Plant quality and predators are important factors affecting herbivore population growth, but how they interact to regulate herbivore populations is not well understood. We manipulated jasmonate-induced plant resistance, exposure to the natural predator community and herbivore density to test how these factors jointly and independently affect herbivore population growth. On low-resistance plants, the predator community was diverse and abundant, promoting high predator consumption rates. On high-resistance plants, the predator community was less diverse and abundant, resulting in low predator consumption rate. Plant resistance only directly regulated aphid population growth on predator-excluded plants. When predators were present, plant resistance indirectly regulated herbivore population growth by changing the impact of predators on the herbivorous prey. A possible mechanism for the interaction between plant resistance and predation is that methyl salicylate, a herbivore-induced plant volatile attractive to predators, was more strongly induced in low-resistance plants. Increased plant resistance reduced predator attractant lures, preventing predators from locating their prey. Low-resistance plants may regulate herbivore populations via predators by providing reliable information on prey availability and increasing the effectiveness of predators.

Plant mating systems affect adaptive plasticity in response to herbivory.

The fitness consequences of mating system variation (e.g. inbreeding) have been studied for at least 200 years, yet the ecological consequences of this variation remain poorly understood. Most plants are capable of inbreeding, and also exhibit a remarkable suite of adaptive phenotypic responses to ecological stresses such as herbivory. We tested the consequences of experimental inbreeding on phenotypic plasticity in resistance and growth (tolerance) traits in Solanum carolinense (Solanaceae). Inbreeding reduced the ability of plants to up-regulate resistance traits following damage. Moreover, inbreeding disrupted growth trait responses to damage, indicating the presence of deleterious mutations at loci regulating growth under stress. Production of the phytohormones abscisic and indole acetic acid, and wounding-induced up-regulation of the defence signalling phytohormone jasmonic acid were all significantly reduced under inbreeding, indicating a phytohormonal basis for inbreeding effects on growth and defence trait regulation. We conclude that the plasticity of induced responses is negatively affected by inbreeding, with implications for fragmented populations facing mate limitation and stress as a consequence of environmental change.

The raison d'être of chemical ecology.

Chemical ecology is a mechanistic approach to understanding the causes and consequences of species interactions, distribution, abundance, and diversity. The promise of chemical ecology stems from its potential to provide causal mechanisms that further our understanding of ecological interactions and allow us to more effectively manipulate managed systems. Founded on the notion that all organisms use endogenous hormones and chemical compounds that mediate interactions, chemical ecology has flourished over the past 50 years since its origin. In this essay we highlight the breadth of chemical ecology, from its historical focus on pheromonal communication, plant-insect interactions, and coevolution to frontier themes including community and ecosystem effects of chemically mediated species interactions. Emerging approaches including the -omics, phylogenetic ecology, the form and function of microbiomes, and network analysis, as well as emerging challenges (e.g., sustainable agriculture and public health) are guiding current growth of this field. Nonetheless, the directions and approaches we advocate for the future are grounded in classic ecological theories and hypotheses that continue to motivate our broader discipline.

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.

Compensatory mechanisms for ameliorating the fundamental trade-off between predator avoidance and foraging.

Most organisms face the problem of foraging and maintaining growth while avoiding predators. Typical animal responses to predator exposure include reduced feeding, elevated metabolism, and altered development rate, all of which can be beneficial in the presence of predators but detrimental in their absence. How then do animals balance growth and predator avoidance? In a series of field and greenhouse experiments, we document that the tobacco hornworm caterpillar, Manduca sexta, reduced feeding by 30-40% owing to the risk of predation by stink bugs, but developed more rapidly and gained the same mass as unthreatened caterpillars. Assimilation efficiency, extraction of nitrogen from food, and percent body lipid content all increased during the initial phase (1-3 d) of predation risk, indicating that enhanced nutritional physiology allows caterpillars to compensate when threatened. However, we report physiological costs of predation risk, including altered body composition (decreased glycogen) and reductions in assimilation efficiency later in development. Our findings indicate that hornworm caterpillars use temporally dynamic compensatory mechanisms that ameliorate the trade-off between predator avoidance and growth in the short term, deferring costs to a period when they are less vulnerable to predation.

Prey perception of predation risk: volatile chemical cues mediate non-consumptive effects of a predator on a herbivorous insect.

Predators can affect prey in two ways-by reducing their density (consumptive effects) or by changing their behavior, physiology or other phenotypic traits (non-consumptive effects). Understanding the cues and sensory modalities prey use to detect predators is critical for predicting the strength of non-consumptive effects and the outcome of predator-prey encounters. While predator-associated cues have been well studied in aquatic systems, less is known about how terrestrial prey, particularly insect larvae, detect their predators. We evaluated how Colorado potato beetle, Leptinotarsa decemlineata, larvae perceive predation risk by isolating cues from its stink bug predator, the spined soldier bug, Podisus maculiventris. When exposed to male "risk" predators that were surgically manipulated so they could hunt but not kill, beetles reduced feeding 29% compared to controls. Exposure to risk females caused an intermediate response. Beetles ate 24% less on leaves pre-exposed to predators compared to leaves never exposed to predators, indicating that tactile and visual cues are not required for the prey's response. Volatile odor cues from predators reduced beetle feeding by 10% overall, although male predators caused a stronger reduction than females. Finally, visual cues from the predator had a weak effect on beetle feeding. Because multiple cues appear to be involved in prey perception of risk, and because male and female predators have differential effects, beetle larvae likely experience tremendous variation in the information about risk from their local environment.

Virus strains differentially induce plant susceptibility to aphid vectors and chewing herbivores.

Plants are frequently attacked by both pathogens and insects, and an attack from one can induce plant responses that affect resistance to the other. However, we currently lack a predictive framework for understanding how pathogens, their vectors, and other herbivores interact. To address this gap, we have investigated the effects of a viral infection in the host plant on both its aphid vector and non-vector herbivores. We tested whether the infection by three different strains of Potato virus Y (PVY(NTN), PVY(NO) and PVY(O)) on tomato plants affected: (1) the induced plant defense pathways; (2) the abundance and fecundity of the aphid vector (Macrosiphum euphorbiae); and (3) the performance of two non-vector species: a caterpillar (Trichoplusia ni) and a beetle (Leptinotarsa decemlineata). While infection by all three strains of PVY induced the salicylate pathway, PVY(NTN) induced a stronger and longer response. Fecundity and density of aphids increased on all PVY-infected plants, suggesting that the aphid response is not negatively associated with salicylate induction. In contrast, the performance of non-vector herbivores positively correlated with the strength of salicylate induction. PVY(NTN) infection decreased plant resistance to both non-vector herbivores, increasing their growth rates. We also demonstrated that the impact of host plant viral infection on the caterpillar results from host plant responses and not the effects of aphid vector feeding. We propose that pathogens chemically mediate insect-plant interactions by activating the salicylate pathway and decreasing plant resistance to chewing insects, which has implications for both disease transmission and insect community structure.

Plant chemistry underlies herbivore-mediated inbreeding depression in nature.

The cost of inbreeding (inbreeding depression, ID) is an important variable in the maintenance of reproductive variation. Ecological interactions such as herbivory could modulate this cost, provided that defence traits harbour deleterious mutations and herbivores are responsible for differences in fitness. In the field, we manipulated the presence of herbivores on experimentally inbred and outcrossed plants of Solanum carolinense (horsenettle) for three years. Damage was greater on inbred plants, and ID for growth and fitness was significantly greater under herbivory. Inbreeding reduced phenolic expression both qualitatively (phytochemical diversity) and quantitatively, indicating deleterious load at loci related to the biosynthesis of defence compounds. Our results indicate that inbreeding effects on plant-herbivore interactions are mediated by changes to functional plant metabolites, suggesting that variation in inbreeding could be a predictor of defence trait variation. The magnitude of herbivore-mediated, ecological ID indicates that herbivores could maintain outcrossing mating systems in nature.

Plant genotypic diversity reduces the rate of consumer resource utilization.

While plant species diversity can reduce herbivore densities and herbivory, little is known regarding how plant genotypic diversity alters resource utilization by herbivores. Here, we show that an invasive folivore--the Japanese beetle (Popillia japonica)--increases 28 per cent in abundance, but consumes 24 per cent less foliage in genotypic polycultures compared with monocultures of the common evening primrose (Oenothera biennis). We found strong complementarity for reduced herbivore damage among plant genotypes growing in polycultures and a weak dominance effect of particularly resistant genotypes. Sequential feeding by P. japonica on different genotypes from polycultures resulted in reduced consumption compared with feeding on different plants of the same genotype from monocultures. Thus, diet mixing among plant genotypes reduced herbivore consumption efficiency. Despite positive complementarity driving an increase in fruit production in polycultures, we observed a trade-off between complementarity for increased plant productivity and resistance to herbivory, suggesting costs in the complementary use of resources by plant genotypes may manifest across trophic levels. These results elucidate mechanisms for how plant genotypic diversity simultaneously alters resource utilization by both producers and consumers, and show that population genotypic diversity can increase the resistance of a native plant to an invasive herbivore.