John L. Maron

Plants with large geographic distributions experience varying biotic and abiotic conditions across their range that can influence plant defence traits among populations. Whether populations inhabiting warmer, wetter, and more productive regions face greater pressure and results in higher investment in defence compared with populations from cooler, drier, and less productive regions remains uncertain. Here, we quantified defence traits and herbivory on Solanum carolinense L . across a large climate and productivity gradient. We sampled populations spanning the entire north–south range (29–44° N) of S. carolinense (33 populations; ~15 plants per population) and employed a common garden experiment (15 populations; ~5 plants per population). We examined whether climate predicts (1) plant defence traits (specific leaf area, trichome density and glycoalkaloid concentration), (2) herbivore damage, and (3) the correlation of traits and herbivore damage in field and common garden plants. Trichome density and herbivore damage were higher for S. carolinense at the centre of its range, while glycoalkaloid concentrations were negatively associated with warmer, wetter climates both in the field and in the common garden. In the field, plants with higher glycoalkaloid production experienced reduced herbivory, while in the common garden plants with greater SLA received more damage. Synthesis. Overall, these findings suggest that different types of defensive traits within a single species may follow different ecological and evolutionary trends and highlight the need for trait‐specific considerations when applying plant defence hypotheses at the intraspecific level.

Plants with large geographic distributions experience varying biotic and abiotic conditions across their range that can influence plant defense traits among populations. Whether populations inhabiting warmer, wetter and more productive regions face greater pressure and results in higher investment in defense compared to populations from cooler, drier, and less productive regions remains uncertain. Here we quantified defense traits and herbivory on Solanum carolinense L. across a large climate and productivity gradient. We sampled populations spanning the entire north-south range (29–44° N) of S. carolinense , (33 populations; ∼15 plants per population) and employed a common garden experiment (15 populations; ∼5 plants per population). We examined whether climate predicts 1) plant defense traits (specific leaf area, trichome density and glycoalkaloid concentration), 2) herbivore damage, and 3) the correlation of traits and herbivore damage in field and common garden plants. Trichome density and herbivore damage were higher for S. carolinense at the center of its range, while glycoalkaloid concentrations were negatively associated with warmer, wetter climates both in the field and in the common garden. In the field, plants with higher glycoalkaloid production experienced reduced herbivory, while in the common garden plants with greater SLA received more damage. Overall, these findings suggest that different types of defensive traits within a single species may follow different ecological and evolutionary trends and highlight the need for trait-specific considerations when applying plant defense hypotheses at the intraspecific level.

Resources play an important role in shaping the evolution of plant defensive strategies. How resource availability influences overall phytochemical diversity within species, and how this in‐turn affects herbivore damage is not well understood. Using Monarda fistulosa, a species that produces diverse terpene compounds and distinct chemotypes (i.e. thymol or carvacrol), we addressed three questions: 1) how do phytochemical components (i.e. total concentration, Shannon diversity, and chemotypes) vary between distinct populations from two large, widely separated regions that differ in climate and productivity? 2) How do these components influence attack by different herbivore species? 3) What are the growth costs of higher phytochemical levels in different chemotypes? Seeds were collected from 12 populations spread across two regions that differ in precipitation‐driven productivity, six from a low‐productivity environment in Montana and six from a high‐productivity environment in Wisconsin, and grown in a common garden in Wisconsin. We analyzed terpene concentrations, quantified the number of herbivores and damage, and measured plant above‐ground biomass. Plants from Montana exhibited higher terpene concentrations but lower diversity, whereas those from Wisconsin displayed lower terpene concentrations but higher diversity. Plants from Wisconsin received more damage from a specialist seed predator and leaf‐chewing herbivores, although abundance of a specialist aphid was lower, compared to plants from Montana. Total terpene concentration emerged as the primary predictor of herbivore damage, although some differences were observed between region of origin and with terpene richness. Herbivores exhibited mixed responses to phytochemistry; some herbivores were negatively affected, while a specialized leaf galler responded positively. Costs of producing defenses were evident by negative correlations between plant biomass and total terpene concentration (but not chemical richness or Shannon diversity). Our study revealed that regional differences in productivity can influence the evolution of phytochemical concentration and diversity, which, in turn, affects plant damage and incurs growth‐related costs.

Herbivores often have highly variable impacts on plant fecundity. The relative contribution of different environmental factors operating at varying spatial scales in affecting this variability is often unclear. We examined how density‐dependent seed predation at local scales and regional differences in primary productivity are associated with variation in the magnitude of pre‐dispersal seed predation on Monarda fistulosa (Lamiaceae). Within M. fistulosa populations growing in a low‐productivity region (LPR), Montana, USA, and a high‐productivity region (HPR), Wisconsin, USA, we quantified the magnitude of pre‐dispersal seed predation among individual plants differing in seed head densities. Out of a total of 303 M. fistulosa plants that were surveyed, we found half as many herbivores in seed heads in the LPR (n = 133 herbivores) compared to the HPR (n = 316). In the LPR, 30% of the seed heads were damaged in plants with low seed head density, while 61% of seed heads were damaged in plants with high seed head density. Seed head damage was consistently high in the HPR (about 49% across the range of seed head density) compared to the LPR (45% across a range of seed head density). However, the proportion of seeds per seed head that were destroyed by herbivores was nearly two times higher (~38% loss) in the LPR compared to HPR (22% loss). Considering the combined effects of probability of damage and seed loss per seed head, the proportion seed loss per plant was consistently higher in the HPR regardless of seed head density. Nevertheless, because of greater seed head production, the total number of viable seeds produced per plant was higher in HPR and high‐density plants, despite being exposed to greater herbivore pressure. These findings show how large‐scale factors can interact with local‐scale factors to influence how strongly herbivores suppress plant fecundity.

As major consumers of plants, insect herbivores have strong potential to influence long‐term patterns of plant abundance and community structure. Nonetheless, remarkably few manipulative experiments exclude insects for three or more years. Thus, how often, and under what conditions insects have enduring impacts remains unclear. Here we summarize the key conceptual issues and evidence from long‐term studies on the impact of insects on plant populations and communities. Models that project effects of herbivores on plant population growth, based on demographic study, suggest that insects often limit plant asymptotic population growth. However, empirical estimations of insect impacts on plant abundance based on long‐term experimental studies are few. As such, the strength and conditionality of compensatory mechanisms (such as density dependence and seedbanks) that may dampen (or exacerbate) the negative effects of insects on plant populations remains unclear. The influences of insects on plant range size and limits, invasion success and biocontrol are well‐established research areas, but are also underexplored in long‐term experiments. Insect herbivores can influence plant community structure and diversity, and change successional trajectories, often through modification of plant competitive ability. Nonetheless, effects are mostly known from mesic grasslands, take years to manifest and the extent of insect damage does not always predict their impact. The relative importance of specialist versus generalist herbivores is unclear, as is how feedbacks between plant productivity, herbivory and plant species richness contribute to community dynamics over time. Synthesis. The few existing long‐term insect suppression experiments, and many short‐term studies, suggest that insect herbivores can importantly affect plant populations and communities. Although challenging, experimental studies spanning multiple plant generations could greatly enhance our ability to develop a more predictive framework for how insect herbivores influence plant populations and communities.

In many invaded grasslands, dominant exotic species can produce large amounts of litter that modify local abiotic conditions and species' interactions. These novel conditions can reduce native species abundance and promote the persistence of exotic species, yet the strength of this disparity may be influenced by how consumer pressure interacts with litter accumulation. Consumers may exacerbate this disparity by preferentially targeting native species or by promoting heterogeneity in microhabitats due to their movement and small‐scale ground disturbances that favours fast growing exotic species. How species respond to litter accumulation and consumer pressure may depend on either evolutionary differences, whereby exotics species may benefit from a lack natural predators, or by functional differences, in which species' physiological traits may confer fitness advantages to low‐light conditions or herbivory or granivory pressure. We examined the impact of litter presence and small mammal herbivory on the establishment and reproduction of functionally diverse exotic versus native species seeded across sites that naturally vary in resource availability in an annual invaded California grassland. We assessed whether seed mass and leaf nitrogen content (LNC) were predictive of successful establishment and reproduction. Litter accumulation affected exotic and native species differently, with litter significantly decreasing native recruitment and reproduction, while exotics were largely unaffected. Small mammals had a slight positive effect on the establishment of native species when litter was present but did not influence exotic species. Regardless of species provenance, larger seeded species established at a higher density while species with lower leaf nitrogen content had a higher density of reproductive individuals. Native species that successfully established and reproduced were functionally different in LNC than the resident community, while successful exotic species were functionally more similar to the resident community in LNC. Our study demonstrates that exotic species outperformed native species regardless of the presence of litter or herbivory pressure. Without the removal or thinning of litter, it is likely that exotic species will continue to dominate, resulting in positive feedback that further favours the persistence of exotic species within this invaded grassland system. Read the free Plain Language Summary for this article on the Journal blog.

Plants often face chronic seed loss from predispersal seed predation by insects. Although many studies have documented the rates of seed loss for single species in different communities, it is unclear how rates of predispersal seed predation vary among co‐occurring species within the same community. If interspecific asymmetries in seed loss are great, this common interaction could have important implications for coexistence. Species traits, such as seed size or seed nitrogen and carbon, might correlate with interspecific variation in predispersal seed predation among co‐occurring grassland forb species. We collected infructescences from 13 co‐occurring forb species from each of four western Montana grasslands over 2 years. We quantified the magnitude of seed loss due to predispersal seed predation by insects. The average level of seed loss was 15.8%. Larger seeded species suffered significantly higher levels of predispersal seed predation than smaller seeded species, and seed size predicted seed loss more than seed nitrogen or carbon. Although large‐seeded species often have greater proportional recruitment and early survival than small‐seeded species, our study suggests that these advantages are partially counterbalanced by greater predispersal seed loss for larger versus smaller seeded species. Asymmetries in predispersal seed predation may importantly affect coexistence among these species.

Determining how climate affects biotic interactions can improve understanding of drivers of context‐dependence and inform predictions of how interactions may influence plants under future climates. In arid environments, the community‐level impacts of seed predators may depend strongly on aridity; yet, long‐term studies documenting impacts of granivores on plant communities over variable climate conditions remain scarce. We evaluated how rodent exclusion interacted with climate to influence grassland and shrubland forb communities and the community‐scale distribution of seed mass over 15 years in the climatically variable northern Chihuahuan Desert. In this dynamic system, two seasonally distinct plant community phases occur annually, one in spring and the other during the summer monsoon. Rodent exclusion significantly altered the community composition of monsoon season plant communities in both grassland and shrubland, but did not affect spring plant composition. Rodents suppressed the abundance of larger‐seeded forb species and promoted smaller‐seeded species. As a consequence, rodent exclusion increased community seed mass (CWM) in monsoon forb communities, most strongly in grassland. The magnitude of impacts of rodents on seed mass varied substantially from year‐to‐year, tracking variation in climate. Specifically, rodent exclusion increased community mean seed mass the most in dry years (grassland) or in years following dry years (shrubland). Rodent exclusion had relatively weak effects on plant species diversity and richness. Our results indicate that climate interacts with the presence of rodents to structure not only the composition but also the traits of desert plant communities.

Dormancy has repeatedly evolved in plants, animals, and microbes and is hypothesized to facilitate persistence in the face of environmental change. Yet previous experiments have not tracked demography and trait evolution spanning a full successional cycle to ask whether early bouts of natural selection are later reinforced or erased during periods of population dormancy. In addition, it is unclear how well short-term measures of fitness predict long-term genotypic success for species with dormancy. Here, we address these issues using experimental field populations of the plant Oenothera biennis, which evolved over five generations in plots exposed to or protected from insect herbivory. While populations existed above ground, there was rapid evolution of defensive and life-history traits, but populations lost genetic diversity and crashed as succession proceeded. After >5 y of seed dormancy, we triggered germination from the seedbank and genotyped >3,000 colonizers. Resurrected populations showed restored genetic diversity that reduced earlier responses to selection and pushed population phenotypes toward the starting conditions of a decade earlier. Nonetheless, four defense and life-history traits remained differentiated in populations with insect suppression compared with controls. These findings capture key missing elements of evolution during ecological cycles and demonstrate the impact of dormancy on future evolutionary responses to environmental change. Significance Studies that experimentally examine evolution have provided critical insight in biology. Indeed, rigorous and replicated laboratory experiments have revealed parallel evolution and have proved essential to understanding evolutionary processes. Nonetheless, a typical limitation of such work is the lack of ecological realism. We report on a decade-long field experiment with a native plant (common evening primrose) that advances our understanding of how populations adapt to environmental change. In particular, we address whether the common strategy of seed dormancy significantly alters the evolutionary trajectory of populations. We find that population genetic diversity is restored following a period of sustained dormancy. Nonetheless, the impact of past natural selection persisted under some conditions.

A paradigm in the plant defence literature is that defending against herbivores comes at a cost to growth, resulting in a growth–defence trade‐off. However, while there is strong evidence for growth–defence trade‐offs across species, evidence is mixed within species. Several mechanisms can account for this equivocal support within species, but teasing them apart requires examining growth–defence relationships both within and among populations, an approach seldom employed. We examined correlations between plant biomass (growth) and terpene production (defence) within and among populations of Monarda fistulosa, a perennial herb. We sampled populations from Montana and Wisconsin, regions that differ in resource availability characterized by different summer precipitation and associated abiotic conditions that influence plant productivity. We found negative, neutral and positive growth–defence correlations, depending on the scale examined. Negative correlations occurred across populations originating from divergent regions, positive correlations occurred across populations originating from within the high‐resource region and neutral correlations were found within single populations. Collectively, these results challenge the general expectation of ubiquitous trade‐offs and support emerging views that resource availability (as it affects productivity) shapes the evolution of defence at different scales. A free Plain Language Summary can be found within the Supporting Information of this article.