Evolution of sensitivity to warning cues from kin in plants with a structured population.

Plants exchange a variety of information intra- and interspecifically by using various mediating cues. For example, plant individuals that are injured by herbivores release volatile chemicals, which induce receiver plants to express anti-herbivore resistance. Remarkably, some plant species were known to represent kin specificity in the response, where cues from a damaged individual induce a higher level of resistance in a kin receiver than in a non-kin receiver. Such higher sensitivity to warning cues from kin could be advantageous via two mechanisms. If each herbivore tends to attack plants with a certain genotype, plants should be more sensitive to warning cues from kin that share genetic properties. In addition, if herbivores successively attack the neighboring plant with a high probability, and if related plants tend to grow in close proximity, plants may be more sensitive to warning cues from neighboring kin under the presence of a trade-off between sensitivity to kin and non-kin. In the present study, we constructed a mathematical model including those mechanisms to investigate the evolutionary process of the higher sensitivity to warning cues from kin than sensitivities to cues from non-kin. According to the analysis of evolutionary dynamics, we revealed that both mechanisms could contribute, although higher sensitivity to cues from kin is more likely to evolve when the spatial range of competition is greater than the range of effective alarm cues. This result highlights the importance of the competition regime in the evolution of signaling among kin.

Spatial habitat heterogeneity influences host-pathogen dynamics in a patchy population of Ranchman's tiger moth.

Host-pathogen dynamics are influenced by many factors that vary locally, but models of disease rarely consider dynamics across spatially heterogeneous environments. In addition, theory predicts that dispersal will influence host-pathogen dynamics of populations that are linked, although this has not been examined empirically in natural systems. We examined the spatial dynamics of a patchy population of tiger moths and its baculovirus pathogen, in which habitat type and weather influence dynamics. Theoretical models of host-baculovirus dynamics predict that such variation in dynamics between habitat types could be driven by a range of factors, of which we predict two are likely to be operating in this system: (1) differences in the environmental persistence of pathogens or (2) differences in host intrinsic rates of increase. We used time series models and monitored infection rates of hosts to characterize population and disease dynamics and distinguish between these possibilities. We also examined the role of host dispersal (connectivity) and weather as important contributors to dynamics, using time series models and experiments. We found that the population growth rate was higher, delayed density dependence was weaker, and long-period oscillations had lower amplitudes in high-quality habitat patches. The infection rate was higher on average in high-quality habitat, and this was likely to have been driven by higher mean population densities and no differences in pathogen persistence in different habitats (delayed density dependence). Time series modeling and experiments also showed an interactive effect of temperature and precipitation on moth population growth rates (likely caused by variation in host plant quality and quantity), and an effect of connectivity. Our results showed that spatial heterogeneity, connectivity, climate, and their interactions were important in driving host-baculovirus dynamics. In particular, our study found that connected patches and spatial heterogeneity generated differences in dynamics that only partially aligned with theoretical predictions.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Effects of experimental watering but not warming on herbivory vary across a gradient of precipitation.

Climate change can affect biotic interactions, and the impacts of climate on biotic interactions may vary across climate gradients. Climate affects biotic interactions through multiple drivers, although few studies have investigated multiple climate drivers in experiments. We examined the effects of experimental watering, warming, and predator access on leaf water content and herbivory rates of woolly bear caterpillars (Arctia virginalis) on a native perennial plant, pacific silverweed (Argentina anserina ssp. pacifica), at two sites across a gradient of precipitation in coastal California. Based on theory, we predicted that watering should increase herbivory at the drier end of the gradient, predation should decrease herbivory, and watering and warming should have positive interacting effects on herbivory. Consistent with our predictions, we found that watering only increased herbivory under drier conditions. However, watering increased leaf water content at both wetter and drier sites. Warming increased herbivory irrespective of local climate and did not interact with watering. Predation did not affect herbivory rates. Given predictions that the study locales will become warmer and drier with climate change, our results suggest that the effects of future warming and drying on herbivory may counteract each other in drier regions of the range of Argentina anserina. Our findings suggest a useful role for range-limit theory and the stress-gradient hypothesis in predicting climate change effects on herbivory across stress gradients. Specifically, if climate change decreases stress, herbivory may increase, and vice versa for increasing stress. In addition, our work supports previous suggestions that multiple climate drivers are likely to have dampening effects on biotic interactions due to effects in different directions, though this is context-dependent.

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.

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.

Induction of the sticky plant defense syndrome in wild tobacco.

Many plants engage in protective mutualisms, offering resources such as extrafloral nectar and shelters to predatory arthropods in exchange for protection against herbivores. Recent work indicates that sticky plants catch small insects and provide this carrion to predators who defend the plants against herbivores. In this study, we investigated whether wild tobacco, Nicotiana attenuata, fits this sticky plant defense syndrome that has been described for other sticky plants. We developed a bioassay for stickiness involving the number of flies that adhered to flowers, the stickiest tissues. In surveys conducted over three field seasons at four sites, we found that the number of carrion that adhered to a plant was positively correlated with the number of predators that we observed foraging over its surfaces. The number of predators was positively correlated with the number of seed capsules that the plant produced, a measure of lifetime female reproductive success. Structural equation modeling indicated strong support for the causal path linking carrion numbers to predator numbers to capsule production. We investigated whether stickiness was an inducible trait and examined two potential cues. We found that experimental clipping of rosette leaves induced greater stickiness, although clipping of neighboring sagebrush leaves did not. Damage to leaf tissue is likely to be a more reliable predictor of risk than is damage to a neighboring plant. The sticky plant defense syndrome is a widespread protective mutualism; its strength and ecological relevance can adjust as risk of herbivory changes.

The effects of pulsed fertilization and chronic herbivory by periodical cicadas on tree growth.

Although many studies have investigated plant growth in the context of episodic herbivory and pressed resource availability, relatively few have examined how plant growth is affected by pulsed resources and chronic herbivory. Periodical cicada (Magicicada spp.) adults represent a pulsed detrital subsidy that fertilizes plants, and live cicada nymphs are long-lived root-feeding herbivores. Previous studies of cicada herbivory effects have been inconclusive, and previous studies of cicada-mediated fertilization did not examine effects on trees, or on a multiyear timescale. Here, we describe the results of a 3-yr experiment that factorially manipulated the presence and absence of cicada fertilization and herbivory in a population of 100 American sycamore (Platanus occidentalis) trees. We found that cicada fertilization strongly increased tree growth in the year of emergence, creating differences in tree size that persisted at least 2 yr later. By comparison, we did not detect reductions in tree growth associated with cicada herbivory in any year of this experiment. However, cicada herbivory reduced the densities of, and damage from, other aboveground herbivores. These results suggest that cicadas affect the size structure of forests over multiple years, and raise questions about how cicada-mediated fertilization and herbivory will affect tree growth over longer timescales.

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.