skip to main content


The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Friday, July 12 until 9:00 AM ET on Saturday, July 13 due to maintenance. We apologize for the inconvenience.

Title: Sodium addition increases leaf herbivory and fungal damage across four grasslands

Sodium (Na) is an essential element for all animals, but not for plants. Soil Na supplies vary geographically. Animals that primarily consume plants thus have the potential to be Na limited and plants that uptake Na may be subject to higher rates of herbivory, but their high Na content also may attract beneficial partners such as pollinators and seed dispersers.

To test for the effects of Na biogeochemistry on herbivory, we conducted distributed Na press experiments (monthly Na application across the growing season) in four North American grasslands.

Na addition increased soil and plant Na concentrations at all sites. Grasses in Na addition plots had significantly higher herbivore damage by leaf miners and fungal pathogens than those in control plots. Forbs with higher foliar Na concentrations had significantly more chewing insect herbivore and fungal damage.

While no pattern was evident across all species, several forb species had higher Na concentrations in inflorescences compared to leaves, suggesting they may allocate Na to attract beneficial partners.

The uptake of Na by plants, and animal responses, has implications for the salinification in the Anthropocene. Increased use of road salt, irrigation with saline groundwater, rising sea levels and increasing temperatures and evapotranspiration rates with climate change can all increase inputs of Na into terrestrial ecosystems.

Our results suggest increasing terrestrial Na availability will benefit insect herbivores and plant fungal pathogens.

A freePlain Language Summarycan be found within the Supporting Information of this article.

more » « less
Award ID(s):
Author(s) / Creator(s):
Publisher / Repository:
Date Published:
Journal Name:
Functional Ecology
Page Range / eLocation ID:
p. 1212-1221
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Plants face many environmental stresses that can impact their survival, development and fitness. Insects are the most diverse, abundant and threatening herbivores in nature. As a consequence, plants produce direct chemical and physical defences to reduce herbivory. They also release volatiles to recruit natural enemies that indirectly protect them from herbivory. The recruitment of parasitic wasps can benefit plant fitness because they ultimately kill their insect hosts.

    Recently, studies showed that parasitoids can indirectly mediate plant defences by modulating herbivore oral secretions. In addition to the direct benefits of parasitoids in terms of reducing herbivore survival, we tested if the reduction in induced defences by parasitized caterpillars compared to non‐parasitized caterpillars may reduce the costs associated with defence expression.

    We provide evidence that tomato plants treated with saliva from parasitized caterpillars have significantly higher fitness parameters including increased flower numbers (16.3%) and heavier fruit weight (13.5%), compared to plants treated with saliva from non‐parasitized caterpillars. Since plants were grown without actual herbivores, the higher values for these fitness parameters were due to lower costs of induced defences and not due to reduced herbivory by parasitized caterpillars. Furthermore, the resulting seed germination time was shorter and the germination rate was higher when the maternal plants were previously exposed to parasitized herbivore treatment compared to control (non‐treated) plants.

    Overall, application of saliva did not result in transgenerational priming of offspring defence responses. However, offspring of parents exposed to caterpillar saliva had lower constitutive levels and higher induced levels of trypsin inhibitor than offspring from unexposed parents.

    This study shows that the saliva of parasitized caterpillars can modulate plant defences and further demonstrates that the lower induction of plant defences is associated with elevated plant fitness in the absence of herbivore feeding, suggesting that induced plant defences are costly.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

    more » « less
  2. Abstract

    Both theory and prior studies predict that climate warming should increase attack rates by herbivores and pathogens on plants. However, past work has often assumed that variation in abiotic conditions other than temperature (e.g. precipitation) do not alter warming responses of plant damage by natural enemies. Studies over short time periods span low variation in weather, and studies over long time‐scales often neglect to account for fine‐scale weather conditions.

    Here, we used a 20+ year warming experiment to investigate if warming affects on herbivory and pathogen disease are dependent on variation in ambient weather observed over 3 years. We studied three common grass species in a subalpine meadow in the Colorado Rocky Mountains, USA. We visually estimated herbivory and disease every 2 weeks during the growing season and evaluated weather conditions during the previous 2‐ or 4‐week time interval (2‐week average air temperature, 2‐ and 4‐week cumulative precipitation) as predictors of the probability and amount of damage.

    Herbivore attack was 13% more likely and damage amount was 29% greater in warmed plots than controls across the focal species but warming treatment had little affect on plant disease. Herbivory presence and damage increased the most with experimental warming when preceded by wetter, rather than drier, fine‐scale weather, but preceding ambient temperature did not strongly interact with elevated warming to influence herbivory.

    Disease presence and amount increased, on average, with warmer weather and more precipitation regardless of warming.

    Synthesis. The effect of warming over reference climate on herbivore damage is dependent on and amplified by fine‐scale weather variation, suggesting more boom‐and‐bust damage dynamics with increasing climate variability. However, the mean effect of regional climate change is likely reduced monsoon rainfall, for which we predict a reduction in insect herbivore damage. Plant disease was generally unresponsive to warming, which may be a consequence of our coarse disease estimates that did not track specific pathogen species or guilds. The results point towards temperature as an important but not sufficient determinant and regulator of species interactions, where precipitation and other constraints may determine the affect of warming.

    more » « less
  3. Abstract

    Global climate change and shifting land‐use are increasing plant stress due to abiotic factors such as drought, heat, salinity and cold, as well as via the intensification of biotic stressors such as herbivores and pathogens. The ability of plants to tolerate such stresses is modulated by the bacteria and fungi that live on or inside of plant tissues and comprise the plant microbiome. However, the impacts of diverse classes of beneficial members of the microbiome and the contrasting stresses that impact plants are most commonly studied independently of each other.

    Our meta‐analysis of 288 experiments across 89 studies moves beyond previous studies in that we simultaneously compare the roles of bacterial versus fungal microbiome members that live within plant tissues and colonize plant surfaces in ameliorating biotic versus abiotic sources of plant stress.

    The magnitude of microbial stress amelioration can be measured as the greater proportional impact of beneficial microbes on plant performance in more stressful environments. In the plant experiments we examine, the magnitude of microbial stress amelioration is substantial: it is 23% of the effect size of the typical impact of stress and 56% of the effect size of beneficial microbiome members in the absence of stress.

    The amount of benefit microbiome members confer to plants differs among classes of microbes, depending on whether plants are grown in stressful or non‐stressful environments. In the absence of stress, beneficial bacteria tend to confer greater plant benefits than do fungi. However, symbiotic fungi, especially arbuscular mycorrhizal fungi, more strongly ameliorate plant stress than do bacteria. In particular, beneficial microbes ameliorate salinity, foliar herbivory and fungal pathogen stress.

    These results highlight the fact that the impacts of beneficial and antagonistic components of the microbiome on plant performance depend on biotic and abiotic environmental contexts. Furthermore, beneficial microbes are especially critical for plant health in stressful environments and thus present opportunities to mitigate negative consequences of global change.

    A freeplain language summarycan be found within the Supporting Information of this article.

    more » « less
  4. Abstract

    Species interactions are expected to change in myriad ways as the frequency and magnitude of extreme temperature events increase with anthropogenic climate change.

    The relationships between endosymbionts, parasites and their hosts are particularly sensitive to thermal stress, which can have cascading effects on other trophic levels.

    We investigate the interactive effects of heat stress and parasitism on a terrestrial tritrophic system consisting of two host plants (one common, high‐quality plant and one novel, low‐quality plant), a caterpillar herbivore and a specialist parasitoid wasp.

    We used a fully factorial experiment to determine the bottom‐up effects of the novel host plant on both the caterpillars' life history traits and the wasps' survival, and the top‐down effects of parasitism and heat shock on caterpillar developmental outcomes and herbivory levels.

    Host plant identity interacted with thermal stress to affect wasp success, with wasps performing better on the low‐quality host plant under constant temperatures but worse under heat‐shock conditions.

    Surprisingly, caterpillars consumed less leaf material from the low‐quality host plant to reach the same final mass across developmental outcomes.

    In parasitized caterpillars, heat shock reduced parasitoid survival and increased both caterpillar final mass and development time on both host plants.

    These findings highlight the importance of studying community‐level responses to climate change from a holistic and integrative perspective and provide insight into potential substantial interactions between thermal stress and diet quality in plant–insect systems.

    Read the freePlain Language Summaryfor this article on the Journal blog.

    more » « less
  5. Abstract

    Conspecific plant density and heterospecific frequency are key drivers of herbivore damage. However, most studies have investigated their effects separately and for single (rather than multiple) focal plant species.

    We conducted an experiment involving three tree species, namely:Cordia dodecandra(Boraginaceae),Manilkara zapota(Zapotaceae), andPiscidia piscipula(Fabaceae). We manipulated understory densities ofM. zapotaandC. dodecandra(focal species) and their frequency relative toP. piscipula.Three months after planting, we surveyed insect leaf chewer and sucking damage on the former two. Because these species are attacked by different herbivores, we predicted a negative effect of heterospecific frequency on herbivory.

    Density and frequency varied in the direction and function of their effects on herbivory depending on the plant species and attacking herbivore. As expected,Piscidia piscipulafrequency had a negative linear effect onM. zapotaleaf‐chewer damage, whereas conspecific density did not affect chewer damage on this species. In contrast, density and frequency had non‐linear effects onC. dodecandrachewer damage, namely positive (hump‐shaped) and negative (U‐shaped) relationships, respectively. In addition, density and frequency had positive linear effects onC. dondecandradamage by leafhoppers.

    These findings call for more work jointly assessing plant inter‐specific variation in density‐ and frequency‐dependent variation in herbivory and its underlying drivers.

    more » « less