An official website of the United States government
Abstract Plants have evolved multiple defensive traits in response to herbivory; in turn, herbivore specialists evolved adaptive behaviours to avoid or tolerate such defences. Here, we employ milkweeds (Asclepiasspp.) to test two defences, latex and trichomes, for their independent and interactive effects on behaviour and performance of monarch caterpillars (Danaus plexippus).Latex exuded upon damage and the density of leaf trichomes positively correlate across milkweed species, suggesting they may have evolved together as synergistic defences. Nonetheless, the complementary roles of these two traits have been little‐studied. We focus on two behaviours: shaving, or the removal of trichomes, and chewing, which encompasses both deactivation of latex and leaf consumption.In an experiment with seven milkweed species, with and without manipulated latex flow, we found latex to be the primary determinant of reducing chewing, while both defences positively predicted shaving behaviour in the first instar. Next, we conducted a factorial experiment throughout the first three instars, manipulating latex and trichomes on a high‐latex, high‐trichome species, the woolly milkweedAsclepias vestita. On plants with latex and trichomes intact, caterpillars spent the most time shaving and least time chewing of all treatment groups, suggesting a possible synergism. These defence‐driven behavioural effects decreased later in larval development.Latex and trichomes both impacted monarch performance, additively increasing mortality and reducing growth of survivors. Thus, latex and trichomes represent two important plant defences with effects on specialist herbivore behaviour and implications for insect fitness.
more »
« less
Heat waves induce milkweed resistance to a specialist herbivore via increased toxicity and reduced nutrient content
Abstract Over the last decade, a large effort has been made to understand how extreme climate events disrupt species interactions. Yet, it is unclear how these events affect plants and herbivores directly, via metabolic changes, and indirectly, via their subsequent altered interaction. We exposed common milkweed (Asclepias syriaca) and monarch caterpillars (Danaus plexippus) to control (26:14°C, day:night) or heat wave (HW) conditions (36:24°C, day:night) for 4 days and then moved each organism to a new control or HW partner to disentangle the direct and indirect effects of heat exposure on each organism. We found that the HW directly benefited plants in terms of growth and defence expression (increased latex exudation and total cardenolides) and insect her'bivores through faster larval development. Conversely, indirect HW effects caused both plant latex and total cardenolides to decrease after subsequent herbivory. Nonetheless, increasing trends of more toxic cardenolides and lower leaf nutritional quality after herbivory by HW caterpillars likely led to reduced plant damage compared to controls. Our findings reveal that indirect impacts of HWs may play a greater role in shaping plant‐herbivore interactions via changes in key physiological traits, providing valuable understanding of how ecological interactions may proceed in a changing world.
more »
« less
- Award ID(s):
- 2209762
- PAR ID:
- 10575549
- Publisher / Repository:
- plant cell and environment
- Date Published:
- Journal Name:
- Plant, Cell & Environment
- Volume:
- 47
- Issue:
- 12
- ISSN:
- 0140-7791
- Page Range / eLocation ID:
- 4530 to 4542
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Extreme heat events are becoming more frequent and intense as climate variability increases, and these events inherently vary in their timing. We predicted that the timing of a heat wave would determine its consequences for insect communities owing to temporal variation in the susceptibility of host plants to heat stress. We subjected common milkweed (Asclepias syriaca) plants to in‐field experimental heat waves to investigate how the timing of heat waves, both seasonally and relative to a biotic stressor (experimental herbivory), affected their ecological consequences. We found that heat waves had multiyear, timing‐specific effects on plant–insect communities. Early‐season heat waves led to greater and more persistent effects on plants and herbivore communities than late‐season heat waves. Heat waves following experimental herbivory had reduced consequences. Our results show that extreme climate events can have complex, lasting ecological effects beyond the year of the event—and that timing is key to understanding those effects.more » « less
-
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
-
For highly specialized insect herbivores, plant chemical defenses are often co-opted as cues for oviposition and sequestration. In such interactions, can plants evolve novel defenses, pushing herbivores to trade off benefits of specialization with costs of coping with toxins? We tested how variation in milkweed toxins (cardenolides) impacted monarch butterfly (Danaus plexippus) growth, sequestration, and oviposition when consuming tropical milkweed (Asclepias curassavica), one of two critical host plants worldwide. The most abundant leaf toxin, highly apolar and thiazolidine ring–containing voruscharin, accounted for 40% of leaf cardenolides, negatively predicted caterpillar growth, and was not sequestered. Using whole plants and purified voruscharin, we show that monarch caterpillars convert voruscharin to calotropin and calactin in vivo, imposing a burden on growth. As shown by in vitro experiments, this conversion is facilitated by temperature and alkaline pH. We next employed toxin-target site experiments with isolated cardenolides and the monarch’s neural Na+/K+-ATPase, revealing that voruscharin is highly inhibitory compared with several standards and sequestered cardenolides. The monarch’s typical >50-fold enhanced resistance to cardenolides compared with sensitive animals was absent for voruscharin, suggesting highly specific plant defense. Finally, oviposition was greatest on intermediate cardenolide plants, supporting the notion of a trade-off between benefits and costs of sequestration for this highly specialized herbivore. There is apparently ample opportunity for continued coevolution between monarchs and milkweeds, although the diffuse nature of the interaction, due to migration and interaction with multiple milkweeds, may limit the ability of monarchs to counteradapt.more » « less
-
Semi‐arid grasslands on the Mongolian Plateau are expected to experience high inputs of anthropogenic reactive nitrogen in this century. It remains unclear, however, how soil organisms and nutrient cycling are directly affected by N enrichment (i.e., without mediation by plant input to soil) vs. indirectly affected via changes in plant‐related inputs to soils resulting from N enrichment. To test the direct and indirect effects of N enrichment on soil organisms (bacteria, fungi and nematodes) and their associated C and N mineralization, in 2010, we designated two subplots (with plants and without plants) in every plot of a six‐level N‐enrichment experiment established in 1999 in a semi‐arid grassland. In 2014, 4 years after subplots with and without plant were established, N enrichment had substantially altered the soil bacterial, fungal and nematode community structures due to declines in biomass or abundance whether plants had been removed or not. N enrichment also reduced the diversity of these groups (except for fungi) and the soil C mineralization rate and induced a hump‐shaped response of soil N mineralization. As expected, plant removal decreased the biomass or abundance of soil organisms and C and N mineralization rates due to declines in soil substrates or food resources. Analyses of plant‐removal‐induced changes (ratios of without‐ to with‐plant subplots) showed that micro‐organisms and C and N mineralization rates were not enhanced as N enrichment increased but that nematodes were enhanced as N enrichment increased, indicating that the effects of plant removal on soil organisms and mineralization depended on trophic level and nutrient status. Surprisingly, there was no statistical interaction between N enrichment and plant removal for most variables, indicating that plant‐related inputs did not qualitatively change the effects of N enrichment on soil organisms or mineralization. Structural equation modelling confirmed that changes in soil communities and mineralization rates were more affected by the direct effects of N enrichment (via soil acidification and increased N availability) than by plant‐related indirect effects. Our results provide insight into how future changes in N deposition and vegetation may modify below‐ground communities and processes in grassland ecosystems.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1111/pce.15040
