Disentangling the direct, indirect, and combined effects of experimental warming on a plant–insect herbivore interaction

Heather M. Kharouba and Louie H. Yang

Abstract

There is increasing evidence that climate warming will have both direct and indirect effects on species. Whereas the direct effects of climate warming represent the proximate physiological consequences of changing abiotic conditions, the indirect effects of climate change reflect changes mediated by at least one other interacting species. The relative importance of these two kinds of effects has been unclear, limiting our ability to generalize the response of different species to climate change. Here, we used a series of experiments to disentangle some of the key direct and indirect effects of warming on the growth of monarch butterfly caterpillars (Danaus plexippus) and showy milkweed plants (Asclepias speciosa) during a window of rapid growth for both species. The effects of warming differed between direct, indirect, and combined effect experiments. Warming from 26°C to 30°C directly increased the growth of both monarch larvae and milkweeds, with monarch and milkweed growth rates showing similar sensitivity to warming. However, in a subsequent experiment, we did not observe significantly increased growth when comparing caterpillars and plants reared at 27°C and 31°C, suggesting that small differences can change the direct effects of warming. When caterpillars that were maintained at laboratory temperatures were fed leaves from host plants that were exposed to warmer temperatures, warming had a negative indirect effect on larval growth rates likely mediated by decreases in milkweed leaf quality. In experiments combining direct and indirect effects, we observed a net positive effect of warming on larval growth rates. Warming had no combined effects on milkweed growth, potentially due to opposing positive direct and negative indirect effects on growth mediated via increased monarch herbivory. These results show how variability among the direct, indirect, and combined effects of even relatively simple, short-term climatic perturbations can present challenges for predicting the broader effects of climatic warming in multispecies communities.

Ecosphere

https://doi.org/10.1002/ecs2.3778

A meta-analysis of single visit pollination effectiveness comparing honeybees and other floral visitors

M.L. Page, C.C. Nicholson, R.M. Brennan, A.T. Britzman, J. Greer, J. Hemberger, H. Kahl, U. Müller, Y. Peng, N.M. Rosenberger, C. Stuligross, L. Wang, L.H. Yang, N.M. Williams

Abstract

Premise
Many animals provide ecosystem services in the form of pollination, including honeybees which have become globally dominant floral visitors. A rich literature documents considerable variation in single visit pollination effectiveness, but this literature has yet to be extensively synthesized to address whether honeybees are effective pollinators.

Methods
We conducted a hierarchical meta-analysis of 168 studies and extracted 1564 single visit effectiveness (SVE) measures for 240 plant species. We paired SVE data with visitation frequency data for 69 of these studies. We used these data to ask: 1) Do honeybees (Apis mellifera) and other floral visitors differ in their SVE?; 2) To what extent do plant and pollinator attributes predict differences in SVE between honeybees and other visitors?; and 3) Is there a correlation between visitation frequency and SVE?

Key results
Honeybees were significantly less effective than the most effective non-honeybee pollinators but as effective as the average pollinator. The type of pollinator moderated these effects. Honeybees were less effective compared to the most effective and average bird and bee pollinators but were as effective as other taxa. Visitation frequency and SVE were positively correlated, but this trend was largely driven by data from communities where honeybees were absent.

Conclusions
Although high visitation frequencies make honeybees important pollinators, they were less effective than the average bee and rarely the most effective pollinator of the plants they visit. As such, honeybees may be imperfect substitutes for the loss of wild pollinators and safeguarding pollination will benefit from conservation of non-honeybee taxa.

American Journal of Botany

https://doi.org/10.1002/ajb2.1764

The effectiveness of eyespots and masquerade in protecting artificial prey across ontogenetic and seasonal shifts

Elizabeth G. Postema

Abstract

When constraints on antipredator coloration shift over the course of development, it can be advantageous for animals to adopt different color strategies for each life stage. Many caterpillars in the genus Papilio exhibit unique ontogenetic color sequences: e.g., early instars that masquerade as bird feces, with later instars possessing eyespots. I hypothesize that larvae abandon feces masquerade in lieu of eyespots due to ontogenetic changes in signaler size. This ontogenetic pattern also occurs within broader seasonal shifts in background color and predator activity. I conducted predation experiments with artificial prey to determine how potential signaling constraints (specifically size and season) shape predation risk, and consequently the expression of ontogenetic color change in Papilio larvae. Seasonally, both predation and background greenness declined significantly from July to September, though there was little evidence that these patterns impacted the effectiveness of either color strategy. Caterpillar size and color strongly affected the attack rate of avian predators: attacks increased with prey size regardless of color, and eyespotted prey were attacked more than masquerading prey overall. These results may reflect a key size-mediated tradeoff between conspicuousness and intimidation in eyespotted prey, and raise questions about how interwoven aspects of behavior and signal environment might maintain the prevalence of large, eyespotted larvae in nature.

Current Zoology

https://doi.org/10.1093/cz/zoab082

Tree preference and temporal activity patterns for a native ant community in an urbanized California woodland

Dylan J. MacArthur-Waltz, Rebecca A. Nelson, Gail Lee and Deborah M. Gordon

Abstract

Anthropogenic disturbances, including land use change and exotic species, can alter the diversity and dynamics of ant communities. To examine foraging behavior in an urbanized habitat in northern California, we surveyed the presence of 9 ant species on 876 trees across 4 seasons during both day and night in a 9.5-hectare urbanized oak-exotic woodland. Ants were more likely to be observed on native, evergreen trees, suggesting that native evergreen species may help maintain ant diversity. Species showed clear patterns of temporal partitioning of foraging activity. Ant species varied in their use of native evergreen Quercus agrifolia trees across season and day/night axes. Of the 3 ant species most frequently observed, Camponotus semitestaceus was most active during spring and summer nights, Formica moki was most active during spring and summer days, and Prenolepis imparis was most active during both day and night during fall and winter. Liometopum occidentale was the second most active species during summer day and night, and winter day. Our findings demonstrate that an oak-exotic urban woodland in Northern California was able to maintain a native ant community, and strong temporal partitioning within that community.

Journal of Insect Behavior

https://doi.org/10.1007/s10905-021-09778-w

Welcome, Ana!

We are glad to welcome Ana Gomez Ramirez to the lab! Ana is a Ph.D. student at San Diego State University where she is co-advised by Rulon Clark and Jeremy Long, but will at UC Davis for the second year of her Ph.D. in the UCD-SDSU Joint Doctoral Program. Ana is studying the effects of tuna aquaculture as a marine subsidy to the terrestrial community of an island chain in Mexico.

The complexity of global change and its effects on insects

Louie H. Yang, Elizabeth G. Postema, Tracie E. Hayes, Mia K. Lippey, Dylan J. MacArthur-Waltz

Abstract

Global change includes multiple overlapping and interacting drivers: 1) climate change, 2) land use change, 3) novel chemicals, and 4) the increased global transport of organisms. Recent studies have documented the complex and counterintuitive effects of these drivers on the behavior, life histories, distributions, and abundances of insects. This complexity arises from the indeterminacy of indirect, non-additive and combined effects. While there is wide consensus that global change is reorganizing communities, the available data are limited. As the pace of anthropogenic changes outstrips our ability to document its impacts, ongoing change may lead to increasingly unpredictable outcomes. This complexity and uncertainty argue for renewed efforts to address the fundamental drivers of global change.

Current Opinion in Insect Science

https://doi.org/10.1016/j.cois.2021.05.001

Open Access PDF available before July 30, 2021

Competition for pollination and isolation from mates differentially impact four stages of pollination in a model grassland perennial

Lea K. Richardson, M. Kate Gallagher, Tracie E. Hayes, Amanda S. Gallinat, Gretel Kiefer, Kristen Manion, Miriam Jenkins, Greg Diersen, Stuart Wagenius

Abstract

  1. Species that persist in small populations isolated by habitat destruction may experience reproductive failure. Self‐incompatible plants face dual threats of mate‐limitation and competition with co‐flowering plants for pollination services. Such competition may lower pollinator visitation, increase heterospecific pollen transfer and reduce the likelihood that a visit results in successful pollination.
  2. To understand how isolation from mates and competition with co‐flowering species contribute to reproductive failure in fragmented habitat, we conducted an observational study of a tallgrass prairie perennial Echinacea angustifolia. We quantified the isolation of focal individuals from mates, characterized species richness and counted inflorescences within 1 m radius, observed pollinator visitation, collected pollinators, quantified pollen loads on pollinators and on Echinacea stigmas, and measured pollination success. Throughout the season, we sampled 223 focal plants across 10 remnant prairie sites.
  3. We present evidence that both co‐flowering species and isolation from mates substantially limit reproduction in Echinacea. As the flowering season progressed, the probability of pollinator visitation to focal plants decreased and evidence for pollen‐limited reproduction increased. Pollinators were most likely to visit Echinacea plants from low‐richness floral neighbourhoods with close potential mates, or plants from high‐richness neighbourhoods with distant potential mates. Frequent visitation only increased pollination success in the former case, likely because Echinacea in high‐richness floral neighbourhoods received low‐quality visits.
  4. Synthesis. In Echinacea, reproduction was limited by isolation from potential mates and the richness of co‐flowering species. These aspects of the floral neighbourhood influenced pollinator visitation and pollination success, although conditions that predicted high visitation did not always lead to high pollination success. These results reveal how habitat modification and destruction, which influence floral neighbourhood and isolation from conspecific mates, can differentially affect various stages of reproductive biology in self‐incompatible plants. Our results suggest that prairie conservation and restoration efforts that promote patches of greater floral diversity may improve reproductive outcomes in fragmented habitats.

Journal of Ecology

https://doi.org/10.1111/1365-2745.13562

Evolved phenological cueing strategies show variable responses to climate change

Collin B. Edwards and Louie H. Yang

Abstract

Several studies have documented a global pattern of phenological advancement that is consistent with ongoing climate change. However, the magnitude of these phenological shifts is highly variable across taxa and locations. This variability of phenological responses has been difficult to explain mechanistically. To examine how the evolution of multi-trait cueing strategies could produce variable responses to climate change, we constructed a model in which organisms evolve strategies that integrate multiple environmental cues to inform anticipatory phenological decisions. We simulated the evolution of phenological cueing strategies in multiple environments, using historic climate data from 78 locations in North America and Hawaii to capture features of climatic correlation structures in the real world. Organisms in our model evolved diverse strategies that were spatially autocorrelated across locations on a continental scale, showing that similar strategies tend to evolve in similar climates. Within locations, organisms often evolved a wide range of strategies that showed similar response phenotypes and fitness outcomes under historical conditions. However, these strategies responded differently to novel climatic conditions, with variable fitness consequences. Our model shows how the evolution of phenological cueing strategies can explain observed variation in phenological shifts and unexpected responses to climate change.

The American Naturalist

https://doi.org/10.1086/711650