Flowers that self-shade reduce heat stress and pollen limitation.

PREMISE: Plants are facing increased risk of heat stress with global climate change. Reproductive tissues are particularly heat-sensitive, which can result in lower plant fitness. Floral shading and closure are possible mechanisms to limit heat stress although most previous work on petal orientation has considered adaptations to raise temperatures. We hypothesized that floral shading could reduce temperature and increase reproductive success. METHODS: We measured floral temperatures of four species that exhibited intraspecific variation in flower closure (Opuntia ficus-indica, Oenothera elata, Convolvulus arvensis, and Romneya coulteri). We also wired newly opened R. coulteri flowers so that they were either permanently open or permanently closed; controls were not wired. RESULTS: Individual flowers of all four species that shaded their pistils were exposed to temperatures 3-8°C lower than those that remained open and unshaded. In our wiring experiment, unencumbered R. coulteri controls were 40% more likely to produce seeds than flowers that were either permanently open or closed. Without added pollen, control flowers produced 2× more seeds than flowers wired open and 8× more than those wired closed. However, pollen addition eliminated the effects of wiring and increased capsule mass and seed production. This effect of pollen addition suggests that pollen limitation was responsible for observed differences in the wiring treatments. Pollinators may prefer control flowers over those that were wired open or closed; petal shading may make flowers cooler and more attractive to pollinators. CONCLUSIONS: Petal shading may be a behavior that allows flowers to reduce heat stress and increases their chances of pollination and seed set.

The consequence of leaf life span to virus infection of herbivorous insects.

Many herbivorous insects die of pathogen infections, though the role of plant traits in promoting the persistence of these pathogens as an indirect interaction is poorly understood. We tested whether winter leaf retention of bush lupines (Lupinus arboreus) promotes the persistence of a nucleopolyhedroviruses, thereby increasing the infection risk of caterpillars (Arctia virginalis) feeding on the foliage during spring. We also investigated whether winter leaf retention reduces viral exposure of younger caterpillars that live on the ground, as leaf retention prevents contaminated leaves from reaching the ground. We surveyed winter leaf retention of 248 lupine bush canopies across twelve sites and examined how it related to caterpillar infection risk, herbivory, and inflorescence density. We also manipulated the amount of lupine litter available to young caterpillars in a feeding experiment to emulate litterfall exposure in the field. Greater retention of contaminated leaves from the previous season increased infection rates of caterpillars in early spring. Higher infection rates reduced herbivory and increased plant inflorescence density by summer. Young caterpillars exposed to less litterfall were more likely to starve to death but less likely to die from infection, further suggesting foliage mediated exposure to viruses. We speculate that longer leaf life span may be an unrecognized trait that indirectly mediates top-down control of herbivores by facilitating epizootics.

Advances in the Evolution and Ecology of 13- and 17-Year Periodical Cicadas.

Apart from model organisms, 13- and 17-year periodical cicadas (Hemiptera: Cicadidae: Magicicada) are among the most studied insects in evolution and ecology. They are attractive subjects because they predictably emerge in large numbers; have a complex biogeography shaped by both spatial and temporal isolation; and include three largely sympatric, parallel species groups that are, in a sense, evolutionary replicates. Magicicada are also relatively easy to capture and manipulate, and their spectacular, synchronized mass emergences facilitate outreach and citizen science opportunities. Since the last major review, studies of Magicicada have revealed insights into reproductive character displacement and the nature of species boundaries, provided additional examples of allochronic speciation, found evidence for repeated and parallel (but noncontemporaneous) evolution of 13- and 17-year life cycles, quantified the amount and direction of gene flow through time, revealed phylogeographic patterning resulting from paleoclimate change, examined the timing of juvenile development, and created hypotheses for the evolution of life-cycle control and the future effects of climate changeon Magicicada life cycles. New ecological studies have supported and questioned the role of prime numbers in Magicicada ecology and evolution, found bidirectional shifts in population size over generations, quantified the contribution of Magicicada to nutrient flow in forest ecosystems, and examined behavioral and biochemical interactions between Magicicada and their fungal parasites and bacterial endosymbionts.

Hilltopping influences spatial dynamics in a patchy population of tiger moths.

Dispersal is a key driver of spatial population dynamics. Dispersal behaviour may be shaped by many factors, such as mate-finding, the spatial distribution of resources, or wind and currents, yet most models of spatial dynamics assume random dispersal. We examined the spatial dynamics of a day-flying moth species (Arctia virginalis) that forms mating aggregations on hilltops (hilltopping) based on long-term adult and larval population censuses. Using time-series models, we compared spatial population dynamics resulting from empirically founded hilltop-based connectivity indices and modelled the interactive effects of temperature, precipitation and density dependence. Model comparisons supported hilltop-based connectivity metrics including hilltop elevation over random connectivity, suggesting an effect of hilltopping behaviour on dynamics. We also found strong interactive effects of temperature and precipitation on dynamics. Simulations based on fitted time-series models showed lower patch occupancy and regional synchrony, and higher colonization and extinction rates when hilltopping was included, with potential implications for the probability of persistence of the patch network. Overall, our results show the potential for dispersal behaviour to have important effects on spatial population dynamics and persistence, and we advocate the inclusion of such non-random dispersal in metapopulation models.

Influence of delayed density and ultraviolet radiation on caterpillar baculovirus infection and mortality.

Infectious disease is an important potential driver of population cycles but must occur through delayed density-dependent infection and resulting fitness effects. Delayed density-dependent infection by baculoviruses can be caused by environmental persistence of viral occlusion bodies (OBs), which can be influenced by environmental factors. Specifically, ultraviolet radiation is potentially important in reducing the environmental persistence of viruses by inactivating OBs. Delayed density-dependent viral infection has rarely been observed empirically at the population level although theory predicts that it is necessary for pathogens to drive population cycles. Similarly, field studies have not examined the effects of ultraviolet radiation on viral infection rates in natural animal populations. We tested if viral infection is delayed density-dependent with the potential to drive cyclic dynamics and if ultraviolet radiation influences viral infection levels. We censused 18 Ranchman's tiger moth (Arctia virginalis) populations across 9° of latitude over 2 years and quantified the effects of direct and delayed density and ultraviolet radiation on proportion infected by baculovirus, infection severity and survival to adulthood. Caterpillars were collected from field populations and reared in the laboratory. Baculovirus has not previously been described infecting A. virginalis, and we used genetic methods to confirm the identity of the virus. We found that proportion infected, infection severity and survival to adulthood exhibited delayed density dependence. Ultraviolet radiation in the previous summer decreased infection severity, which increased caterpillar survival probability. Structural equation modelling indicated that the effect of lagged density on caterpillar survival was mediated through proportion infected and infection severity and was 2.5-fold stronger than the indirect effect of ultraviolet. We successfully amplified polh, lef-8 and lef-9 viral genes from caterpillars, and BLAST results confirmed that the virus was a nucleopolyhedrovirus. Our findings provide clear evidence that delayed density-dependent mortality can arise through viral infection rate and severity in insects, which supports the role of viral disease as a mechanism, among others, that may drive insect population cycles. Furthermore, our findings support predictions that ultraviolet radiation can modify viral disease dynamics in insect populations, most likely through attenuating viral persistence in the environment.

Consistent individual variation in plant communication: do plants have personalities?

Animal biologists have recently focused on individual variation in behavioral traits and have found that individuals of many species have personalities. These are defined as consistent intraspecific differences in behaviors that are repeatable across different situations and stable over time. When animals sense danger, some individuals will alert neighbors with alarm calls and both calling and responding vary consistently among individuals. Plants, including sagebrush, emit volatile cues when they are attacked by herbivores and neighbors perceive these cues and reduce their own damage. We experimentally transferred volatiles between pairs of sagebrush plants to evaluate whether individuals showed consistent variation in their effectiveness as emitters and as receivers of cues, measured in terms of reduced herbivore damage. We found that 64% of the variance in chewing damage to branches over the growing season was attributable to the identity of the individual receiving the cues. This variation could have been caused by inherent differences in the plants as well as by differences in the environments where they grew and their histories. We found that 5% of the variance in chewing damage was attributable to the identity of the emitter that provided the cue. This fraction of variation was statistically significant and could not be attributed to the environmental conditions of the receiver. Effective receivers were also relatively effective emitters, indicating consistency across different situations. Pairs of receivers and emitters that were effective communicators in 2018 were again relatively effective in 2019, indicating consistency over time. These results suggest that plants have repeatable individual personalities with respect to alarm calls.

Plant induced defenses that promote cannibalism reduce herbivory as effectively as highly pathogenic herbivore pathogens.

Plant induced defenses may benefit plants by increasing cannibalism among insect herbivores. However, the general efficacy of plant defenses that promote cannibalism remains unclear. Using a generalist Lepidopteran herbivore (Helicoverpa zea), we examined whether plant induced defenses in Solanum lycopersicum increased cannibalism among H. zea and whether defense-mediated cannibalism benefits both the plant and the cannibal. In a separate experiment, we also examined whether defense-mediated cannibalism has effects on H. zea herbivory that are comparable to the effects of pathogenic virus of H. zea (HzSNPV) and whether defense-mediated cannibalism modified pathogen efficacy. We found that both plant defenses and cannibalism decreased herbivory: H. zea consumed less plant material if plants were induced, if dead conspecifics were provided, or both. Cannibalism increased cannibal growth rate: cannibals effectively overcome the costs of plant defenses by eating conspecifics. Inoculating half of H. zea with virus strongly reduced caterpillar survival. Cannibalism occurred sooner among virus-inoculated groups of H. zea, and all caterpillars in virus-inoculated treatments died before the end of the 7-day experiment. Although the rise in mortality caused by HzSNPV occurred more rapidly than the rise in mortality due to defense-mediated cannibalism, overall H. zea mortality at the end of the experiment was equal among virus-inoculated and induced-defense groups. Defense-mediated cannibalism and viral inoculation equally reduced herbivory on S. lycopersicum. Our results provide evidence that defense-mediated increases in cannibalism can be as effective as other forms of classic herbivore population regulation, and that both viral pathogens and defense-induced cannibalism can have significant benefits for plants.

Variability in plant nutrients reduces insect herbivore performance.

The performance and population dynamics of insect herbivores depend on the nutritive and defensive traits of their host plants. The literature on plant-herbivore interactions focuses on plant trait mean values, but recent studies showing the importance of plant genetic diversity for herbivores suggest that plant trait variance may be equally important. The consequences of plant trait variance for herbivore performance, however, have been largely overlooked. Here we report an extensive assessment of the effects of within-population plant trait variance on herbivore performance using 457 performance datasets from 53 species of insect herbivores. We show that variance in plant nutritive traits substantially reduces mean herbivore performance via non-linear averaging of performance relationships that were overwhelmingly concave down. By contrast, relationships between herbivore performance and plant defence levels were typically linear, with variance in plant defence not affecting herbivore performance via non-linear averaging. Our results demonstrate that plants contribute to the suppression of herbivore populations through variable nutrient levels, not just by having low average quality as is typically thought. We propose that this phenomenon could play a key role in the suppression of herbivore populations in natural systems, and that increased nutrient heterogeneity within agricultural crops could contribute to the sustainable control of insect pests in agroecosystems.

Altered precipitation dynamics lead to a shift in herbivore dynamical regime.

The interaction between endogenous dynamics and exogenous environmental variation is central to population dynamics. Although investigations into the effects of changing mean climate are widespread, changing patterns of variation in environmental forcing also affect dynamics in complex ways. Using wavelet and time series analyses, we identify a regime shift in the dynamics of a moth species in California from shorter to longer period oscillations over a 34-year census, and contemporaneous changes in regional precipitation dynamics. Simulations support the hypothesis that shifting precipitation dynamics drove changes in moth dynamics, possibly due to stochastic resonance with delayed density-dependence. The observed shift in climate dynamics and the interaction with endogenous dynamics mean that predicting future population dynamics will require information on both climatic shifts and their interaction with endogenous density-dependence, a combination that is rarely available. Consequently, models based on historical data may be unable to predict future population dynamics.

Risk of herbivory negatively correlates with the diversity of volatile emissions involved in plant communication.

Plant-to-plant volatile-mediated communication and subsequent induced resistance to insect herbivores is common. Less clear is the adaptive significance of these interactions; what selective mechanisms favour plant communication and what conditions allow individuals to benefit by both emitting and responding to cues? We explored the predictions of two non-exclusive hypotheses to explain why plants might emit cues, the kin selection hypothesis (KSH) and the mutual benefit hypothesis (MBH). We examined 15 populations of sagebrush that experience a range of naturally occurring herbivory along a 300 km latitudinal transect. As predicted by the KSH, we found several uncommon chemotypes with some chemotypes occurring only within a single population. Consistent with the MBH, chemotypic diversity was negatively correlated with herbivore pressure; sites with higher levels of herbivory were associated with a few common cues broadly recognized by most individuals. These cues varied among different populations. Our results are similar to those reported for anti-predator signalling in vertebrates.

Loss of branches due to winter storms could favor deciduousness in oaks.

PREMISE: Ecologists have an incomplete understanding of the factors that select for deciduous, evergreen, and marcescent leaf habits. Evergreens have more opportunities for photosynthesis but may experience costs when abiotic conditions are unfavorable such as during ice and windstorms. METHODS: We documented branch loss for species of oaks (Quercus spp.) in a common garden in California during an unusual windstorm. RESULTS: Branches of marcescent trees were more likely to break during the storm, and this pattern had a negligible phylogenetic signature. Branches of evergreen and marcescent species were mostly alive before breaking, which likely accrued a fitness cost, while those of deciduous species were mostly already dead. One explanation for the overrepresentation of broken branches from marcescent species is that their petioles are inflexible and have greater wind loading compared to the flexible petioles of evergreen leaves and the leafless condition of deciduous branches. CONCLUSIONS: These results suggest that branch loss during unusual winter storms may be an important cost of a marcescent leaf habit.

Feeding and damage-induced volatile cues make beetles disperse and produce a more even distribution of damage for sagebrush.

Induced plant responses to herbivory are common, and we have learned a lot about the mechanisms of induced resistance and their effects on herbivore performance. We know less about their effects on herbivore behaviour and especially on spatial patterns of damage. Theoretical models predict that induced responses can cause patterns of damage to become aggregated, random or even. A recent model predicted that informed herbivore movement coupled with communication between plants would make damage more even within individual plants. We tested these predictions in the field using a specialist beetle Trirhabda pilosa that feeds on sagebrush Artemisia tridentata. Both the beetle and the plant are well-documented to respond to damage-induced volatile cues. Beetle larvae were more likely to move from damaged leaves and leaves that had been exposed to volatiles from nearby damaged leaves compared to undamaged control leaves. Previous laboratory results indicated that beetles were more likely to choose undamaged leaves compared to damaged leaves or those exposed to volatile cues of damage. A comparison of damage patterns early in the season and after completion of beetle feeding revealed that variance in damage among branches decreased as the season progressed; that is, damage became more evenly distributed among the branches within a plant. Larvae damaged many leaves on a plant but removed relatively little tissue from each leaf. Herbivore movement and the spatial patterns of damage that it creates can be important in determining effects on plant fitness and other population processes. Dispersion of damage deserves more consideration in plant-herbivore studies.

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.

Unidirectional grass hairs usher insects away from meristems.

Grasses are major agricultural products worldwide and they are critical to ecosystem function in many terrestrial habitats. Despite their global importance, we know relatively little about their defenses against herbivory. Grasses tend to be tolerant of leaf loss because their valuable meristems are located underground, out of reach for above ground herbivores. Many grasses have unidirectional leaf hairs, prickles, and spines that make moving up the leaf blade easy, but make moving down, toward the meristem, difficult. We tested the hypothesis that unidirectional grass hairs direct small arthropod herbivores away from the meristems. In a field survey of the distribution of herbivore damage, we found that leaf tips received five times more damage than leaf bases for Avena barbata. Early-instar grasshoppers fed three times as often on leaf tops as on leaf bases of pubescent individuals in a common garden laboratory experiment. This effect was not observed for glabrous individuals where grasshoppers damaged leaf bases as often as leaf tops. A common generalist caterpillar, Heliothus virescens, was more than twice as likely to turn in the direction of the hairs, away from the meristems, when it encountered pubescent leaves of A. barbata. However, larger caterpillars of the generalist feeder Arctia virginalis showed no directional bias when they encountered pubescent leaves. In common garden experiments, selection on pubescence was weak and inconsistent over space and time. Under some circumstances, individuals of A. barbata with pubescent leaves were more likely to produce seeds than were individuals with fewer hairs. The surveys, behavioral experiments with small insects, and estimates of lifetime reproduction all support the hypothesis that unidirectional leaf hairs on A. barbata, and perhaps other grasses, serve as an unstudied defense that direct small herbivores away from the meristems.

A judgment and decision-making model for plant behavior.

Recently plant biologists have documented that plants, like animals, engage in many activities that can be considered as behaviors, although plant biologists currently lack a conceptual framework to understand these processes. Borrowing the well-established framework developed by psychologists, we propose that plant behaviors can be constructively modeled by identifying four distinct components: (1) a cue or stimulus that provides information, (2) a judgment whereby the plant perceives and processes this informative cue, (3) a decision whereby the plant chooses among several options based on their relative costs and benefits, and (4) action. Judgment for plants can be determined empirically by monitoring signaling associated with electrical, calcium, or hormonal fluxes. Decision-making can be evaluated empirically by monitoring gene expression or differential allocation of resources. We provide examples of the utility of this judgment and decision-making framework by considering cases in which plants either successfully or unsuccessfully induced resistance against attacking herbivores. Separating judgment from decision-making suggests new analytical paradigms (i.e., Bayesian methods for judgment and economic utility models for decision-making). Following this framework, we propose an experimental approach to plant behavior that explicitly manipulates the stimuli provided to plants, uses plants that vary in sensory abilities, and examines how environmental context affects plant responses. The concepts and approaches that follow from the judgment and decision-making framework can shape how we study and understand plant-herbivore interactions, biological invasions, plant responses to climate change, and the susceptibility of plants to evolutionary traps.

As temperature increases, predator attack rate is more important to survival than a smaller window of prey vulnerability.

Climate change can have strong effects on species interactions and community structure. Temperature-dependent effects on predator-prey interactions are a major mechanism through which these effects occur. To understand the net effects of predator attack rates and dynamic windows of prey vulnerability, we examined the impacts of temperature on the interaction of a caterpillar (Arctia virginalis) and its ant predator (Formica lasioides). We conducted field experiments to examine attack rates on caterpillars relative to temperature, ant abundance, and body size, and laboratory experiments to determine the effects of temperature on caterpillar growth. We modeled temperature-dependent survival based on the integrated effects of temperature-dependent growth and temperature- and size-dependent predation. Attack rates on caterpillars increased with warming and ant recruitment, but decreased with caterpillar size. Caterpillar growth rates increased with temperature, narrowing the window of vulnerability. The model predicted that net caterpillar survival would decrease with temperature, suggesting that A. virginalis populations could be depressed with future climate warming. Theoretical work suggests that the net outcome of predator-prey interactions with increasing temperature depends on the respective responses of interacting species in terms of velocity across space, whereas the present study suggests the importance of effects of temperature on prey window of vulnerability, or "velocity" across time.

Precipitation affects plant communication and defense.

Anti-herbivore defense shows high levels of both inter- and intraspecific variability. Defending against herbivores may be costly to the plant when it requires a tradeoff in allocation between defense and other missed opportunities, such as reproduction. Indeed, the plastic expression of defensive traits allows the plant to invest resources in defense only when the risk of being damaged actually increases, avoiding wasted resources. Plants may assess risk by responding to volatile cues emitted by neighbors that are under attack. Most plastic responses likely depend on environmental conditions. In this experiment, we investigated the effect of water availability on resistance induced by volatile cues in sagebrush. We found that plants receiving additional water over summer and/or volatile cues from neighbor donor plants showed reduced herbivore damage compared to control plants. Interestingly, we found no evidence of interactions between additional water and volatile cues. We performed an inferential analysis comparing historical records of the levels of herbivore damage during different years that had different temperature and precipitation accumulations. Results confirmed findings from the experiment, as the regression model indicated that sagebrush was better defended during wetter and hotter seasons. Reports from the literature indicated that sagebrush is extremely sensitive to water availability in the soil. We suggest that water availability may directly affect resistance of herbivory as well as sensitivity to cues of damage. Costs and benefits of allocating resources to defensive traits may vary with environmental conditions.

Wet years have more caterpillars: interacting roles of plant litter and predation by ants.

Climate is widely recognized as an important factor that affects temporal and spatial patterns of occurrence and abundance of herbivorous insects, although the ecological mechanisms responsible are poorly understood. We found that precipitation and standing water were positively correlated with locations and years of high abundance of caterpillars of the ranchman's tiger moth, Platyprepia virginalis. We analyzed 30 years of survey data and found that the number of large rainfall events was a better predictor of caterpillar abundance than total annual accumulation. We considered three ecological mechanisms that could drive this relationship and conducted observations and manipulative experiments to evaluate these mechanisms. (1) Rainfall facilitates more plant growth, although we found no evidence that increased food quality or quantity was causing the positive association between precipitation and caterpillar abundance. (2) Large rainfall events cause predatory ground-nesting ants to be less abundant and we found that the number of ants that recruited to local sites was negatively associated with survival and abundance of caterpillars. (3) We found that litter from wet sites provided a refuge from ant predation; litter from wet sites was not beneficial to caterpillars in the absence of ants. Both abiotic factors (precipitation) and biotic factors (predatory ants) affected the temporal and spatial abundance of caterpillars directly and interactively. Climate models predict that rainfall will become more variable, suggesting that populations of this caterpillar may also become more variable in the future.

Chewing sandpaper: grit, plant apparency, and plant defense in sand-entrapping plants.

Sand entrapment on plant surfaces, termed psammophory or sand armor, is a phylogenetically and geographically widespread trait. The functional significance of this phenomenon has been poorly investigated. Sand and soil are nonnutritive and difficult for herbivores to process, as well as visually identical to the background. We experimentally investigated whether this sand coating physically protected the plant from herbivores or increased crypsis (e.g., decreased apparency to herbivores). We tested the former hypothesis by removing entrapped sand from stems, petioles, and leaves of the sand verbena Abronia latifolia and by supplementing natural sand levels in the honeyscented pincushion plant Navarretia mellita. Consistent with a physical defensive function, leaves with sand present or supplemented suffered less chewing herbivory than those with sand removed or left as is. To test a possible crypsis effect, we coated some sand verbena stems with green sand, matching the stem color, as well as others with brown sand to match the background color. Both suffered less chewing herbivory than controls with no sand and herbivory did not significantly differ between the colors, suggesting crypsis was not the driving resistance mechanism. Strong tests of plant apparency are rare; this experimental approach may be possible in other systems and represents one of few manipulative tests of this long-standing hypothesis.

Geographic dialects in volatile communication between sagebrush individuals.

Plants respond to volatile cues emitted by damaged neighbors to increase their defenses against herbivores. We examined whether plants communicated more effectively with local neighbors than distant neighbors in a reciprocal experiment at two sites. Three branches on focal plants were incubated with air from (1) a control, (2) an experimentally clipped "foreign" plant from 230 km away, or (3) an experimentally clipped "local" plant from the same population as the focal plant. Branches incubated with air from the controls experienced 50-80% more leaf damage than those receiving air from experimentally clipped plants. Of more interest, branches receiving volatiles from experimentally clipped "local" plants received 50-65% of the leaf damage as those receiving volatiles from experimentally clipped "foreign" plants. Sabinyl compounds and related terpinenes were found to differ consistently for plants from southern and northern sites. These results indicate that cues vary geographically in their effectiveness and suggest that sagebrush responds more strongly to local than foreign dialects.