Species-specific, age-varying plant traits affect herbivore growth and survival

Louie H. Yang, Meredith L. Cenzer, Laura J. Morgan, and Griffin W. Hall


Seasonal windows of opportunity represent intervals of time within a year during which organisms have improved prospects of achieving life history aims such as growth or reproduction, and may be commonly structured by temporal variation in abiotic factors, bottom-up factors, and top-down factors. Although seasonal windows of opportunity are likely to be common, few studies have examined the factors that structure seasonal windows of opportunity in time. Here, we experimentally manipulated host plant age in two milkweed species (Asclepias fascicularis and Asclepias speciosa) in order to investigate the role of plant species-specific and plant age-varying traits on the survival and growth of monarch caterpillars (Danaus plexippus). We show that the two plant species showed diverging trajectories of defense traits with increasing age. These species-specific and age-varying host plant traits significantly affected the growth and survival of monarch caterpillars through both resource quality- and resource quantity-based constraints. The effects of plant age on monarch developmental success were comparable to and sometimes larger than those of plant species identity. We conclude that species-specific and age-varying plant traits are likely to be important factors with the potential to structure seasonal windows of opportunity for monarch development, and examine the implications of these findings for both broader patterns in the ontogeny of plant defense traits and the specific ecology of milkweed-monarch interactions in a changing world.



Toward a more temporally explicit framework for community ecology (Open Access)

Louie H. Yang


Although ecologists have long understood the fundamentally dynamic nature of communities, ecology has until recently seemed to emphasize other aspects of ecological complexity, such as diversity and spatial structure, ahead of temporal variation. Climate change has made studies into the temporal dimensions of community ecology more immediate and urgent, and has exposed the limits of our general understanding about how species interactions change over time. Here, I suggest four specific ways to continue building towards a more temporally explicit understanding of community ecology: 1) by increasing the representation of temporal change in interaction networks, 2) by developing both specific and general insights into event-driven dynamics, 3) by developing and testing sequential hypotheses to describe proposed explanations that unfold over time, and 4) by characterizing seasonal windows of opportunity. A great deal about the temporal dynamics of communities remains uncertain, but temporally explicit studies have the potential to improve our fundamental understanding of how communities function.

Ecological Research


Open Access PDF

Seasonal windows of opportunity in milkweed-monarch interactions

Louie H. Yang and Meredith L. Cenzer


Many organisms experience seasonal windows of opportunity for growth and reproduction. These windows represent intervals in time when organisms experience improved prospects for advancing their life history objectives, constrained by the combined effects of seasonally variable biotic and abiotic conditions acting independently or in combination. While seasonal windows of opportunity are likely to be widespread in nature, relatively few studies have conducted the repeated observations necessary to identify them or suggest the factors that structure them in time. Here, we present the results of three experimental studies conducted at different field sites in three different years in which we manipulated the phenology of monarch caterpillars (Danaus plexippus) throughout the growing season. The primary aims of these experiments were to a) identify seasonal windows of opportunity for successful larval development on milkweed (Asclepias spp.), and b) to suggest which factors are most likely to constrain these windows of opportunity in time. We found strong seasonal windows of opportunity in the developmental success of monarchs, with distinct periods of higher developmental prospects during each study year. We evaluated the role of seasonal variation in abiotic thermal stress, host plant density, host plant defensive traits, and natural enemy risk as potential factors that may limit seasonal windows of opportunity. By comparing the seasonal patterns of larval success and potential explanatory factors across all three years, we find patterns that are consistent with seasonally variable abiotic conditions, host plant availability, host plant traits, and natural enemy risk factors.  These results suggest the potential for seasonal variation in the factors that limit monarch larval development and population growth. More generally, this study also highlights the value of temporally explicit experimental studies that can identify and examine seasonal patterns in species interactions.



Artificial light increases local predator abundance, predation rates, and herbivory

Marshall McMunn, Louie H. Yang, Amy Ansalmo, Keatyn Bucknam, Miles Claret, Cameron Clay, Kyle Cox, Darian Dungey, Asia Jones, Ashley Kim, Robert Kubacki, Rachel Le, Deniss Martinez, Brian Reynolds, John Schroder, and Emily Wood


Human activity is rapidly increasing the radiance and geographic extent of artificial light at night (ALAN). The timing and characteristics of light affect the development, behavior, and physiological state of many organisms. Depending on the ecological context, plants and animals respond to artificial lights in both adaptive and maladaptive ways. Mesocosm experiments have demonstrated both top-down and bottom-up control of populations under ALAN, but there have been few community-scale studies that allow for spatial aggregation through positive phototaxis, a common phenomenon among arthropods. We performed a field study to determine the effects of ALAN on arthropod communities, plant traits, and local herbivory and predation rates. We found strong positive phototaxis in 10 orders of arthropods, with increased (159% higher) overall arthropod abundance under ALAN compared to unlit controls. The arthropod community under ALAN was more diverse and contained a higher proportion of predaceous arthropods (15% vs 8%).  Predation of immobilized flies occurred more 3.6 times faster under ALAN; this effect was not observed during the day. Contrary to expectations, we also observed a 6% increase in herbivory under ALAN. Our results highlight the importance of open experimental field studies for determining the community-level effects of ALAN.

Environmental Entomology


Pulsed seaweed subsidies drive sequential shifts in the effects of lizard predators on island food webs

Jonah Piovia-Scott, Louie H. Yang, Amber N. Wright, David Spiller, Thomas Schoener


Most prominent theories of food-web dynamics imply the simultaneous action of bottom-up and top-down forces. However, transient bottom-up effects resulting from resource pulses can lead to sequential shifts in the strength of top-down predator effects. We used a large-scale field experiment (32 small islands sampled over 5 years) to probe how the frequency and magnitude of pulsed seaweed inputs drives temporal variation in the top-down effects of lizard predators. Short-term weakening of lizard effects on spiders and plants (the latter via a trophic cascade) were associated with lizard diet shifts, and were more pronounced with larger seaweed inputs. Long-term strengthening of lizard effects was associated with lizard numerical responses and plant fertilization. Increased pulse frequency reinforced the strengthening of lizard effects on spiders and plants. These results underscore the temporally variable nature of top-down effects and highlight the role of resource pulses in driving this variation.

Ecology Letters


Vectors with autonomy: what distinguishes animal‐mediated nutrient transport from abiotic vectors?

Alexandra G. McInturf, Lea Pollack, Louie H. Yang and Orr Spiegel


Animal movements are important drivers of nutrient redistribution that can affect primary productivity and biodiversity across various spatial scales. Recent work indicates that incorporating these movements into ecosystem models can enhance our ability to predict the spatio‐temporal distribution of nutrients. However, the role of animal behaviour in animal‐mediated nutrient transport (i.e. active subsidies) remains under‐explored. Here we review the current literature on active subsidies to show how the behaviour of active subsidy agents makes them both ecologically important and qualitatively distinct from abiotic processes (i.e. passive subsidies). We first propose that animal movement patterns can create similar ecological effects (i.e. press and pulse disturbances) in recipient ecosystems, which can be equal in magnitude to or greater than those of passive subsidies. We then highlight three key behavioural features distinguishing active subsidies. First, organisms can transport nutrients counter‐directionally to abiotic forces and potential energy gradients (e.g. upstream). Second, unlike passive subsidies, organisms respond to the patterns of nutrients that they generate. Third, animal agents interact with each other. The latter two features can form positive‐ or negative‐feedback loops, creating patterns in space or time that can reinforce nutrient hotspots in places of mass aggregations and/or create lasting impacts within ecosystems. Because human‐driven changes can affect both the space‐use of active subsidy species and their composition at both population (i.e. individual variation) and community levels (i.e. species interactions), predicting patterns in nutrient flows under future modified environmental conditions depends on understanding the behavioural mechanisms that underlie active subsidies and variation among agents’ contributions. We conclude by advocating for the integration of animal behaviour, animal movement data, and individual variation into future conservation efforts in order to provide more accurate and realistic assessments of changing ecosystem function.

Biological Reviews


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

Louie H. Yang and Richard Karban


While 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 cicadas (Magicicada spp.) adults represent a pulsed detrital subsidy that fertilizes plants, while 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 multi-year timescale. Here we describe the results of a three-year 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 two years 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.



Seasonal assembly of arthropod communities on milkweeds experiencing simulated herbivory

Ian Pearse, Marshall McMunn, and Louie H. Yang


The seasonal assembly of arthropod communities is shaped by biotic and abiotic aspects of the habitat that limit the appearance or activity phenology of potential community members. In addition, previous interactions within the community, such as herbivore-induced plant defensive responses, aggregation, and predator avoidance likely affect the assembly of arthropod communities on individual plants. We observed the phenology of arthropod communities and defensive plant traits on 100 milkweed (Asclepias eriocarpa) individuals at monthly intervals over a growing season. We experimentally wounded a subset of plants each month (April–August) to observe the effect of simulated added herbivore damage on the seasonal assembly of these arthropod communities. All plant traits and measures of arthropod communities changed over the season. The observed response to experimental leaf damage suggested a trend of induced susceptibility in early months, but not late months. Plants receiving early-season simulated herbivory experienced more subsequent leaf damage than unmanipulated plants. We observed several lagged correlations in our study indicating that blue milkweed beetle (Chrysochus cobaltinus) abundance was lower in months following high natural leaf damage, and that the abundance of a secondary omnivore (Lygaeus kalmii) and total predator abundance tended to follow months with high C. cobaltinus abundance. Ahistorical habitat factors determined much of the observed seasonality of arthropod communities, but induced responses to simulated herbivory also contributed historical effects that influenced arthropod community assembly.

Arthropod-Plant Interactions. 13:99–108

doi: 10.1007/s11829-018-9660-7

The mechanisms of phenology: the patterns and processes of phenological shifts

Helen E. Chmura, Heather M. Kharouba, Jaime Ashander, Sean M. Ehlman, Emily B. Rivest and Louie H. Yang


Species across a wide‐range of taxa and habitats are shifting phenological events in response to climate change. While advances are common, shifts vary in magnitude and direction within and among species, and the basis for this variation is relatively unknown. We examine previously suggested patterns of variation in phenological shifts in order to understand the cue‐response mechanisms that underlie phenological change. Here, we review what is known about the mechanistic basis for nine factors proposed to predict phenological change (latitude, elevation, habitat type, trophic level, migratory strategy, ecological specialization, species’ seasonality, thermoregulatory mode, and generation time). We find that many studies either do not identify a specific underlying mechanism or do not evaluate alternative mechanistic hypotheses, limiting the ability of scientists to predict future responses to global change with accuracy. We present a conceptual framework that emphasizes a critical distinction between environmental (cue‐driven) and organismal (response‐driven) mechanisms causing variation in phenological shifts and discuss how this distinction can reduce confusion in the field and improve predictions of future phenological change.

Ecological Monographs


Experimental shifts in phenology affect fitness, foraging, and parasitism in a native solitary bee

Shahla Farzan  and Louie H. Yang


Phenological shifts have been observed in a wide range of taxa, but the fitness consequences of these shifts are largely unknown, and we often lack experimental studies to assess their population‐level and evolutionary consequences. Here, we describe an experimental study to determine the fitness consequences of phenological shifts in blue orchard bee (Osmia lignaria) emergence, compare the measured seasonal fitness landscape with observed phenology in the unmanipulated population, and assess seasonal variation in key factors related to reproduction, foraging, and brood parasitism that were expected to affect the shape of the fitness landscape. By tracking individually marked females, we were able to estimate the lifetime fitness impacts of phenological advances and delays. We also measured parasitism risk, floral resource use, and nesting behavior to understand how each varies seasonally, and their combined effects on realized fitness. Survival to nesting decreased non‐monotonically throughout the season, with a 20.4% decline in survival rates between the first and second cohorts. The total reproductive output per maternal bee was 14.9% higher in the second cohort compared the first, and 161% higher in the second cohort compared to the third. Combining seasonal patterns in survival and reproductive output, experimentally advanced females showed 30.6% higher fitness than bees released at the historic peak. In contrast, the nesting phenology of unmanipulated bees showed nearly equal numbers of nesting attempts in the first two cohorts. Both increased resource availability and reduced parasitism risk favored earlier emergence. These results are consistent with a population experiencing directional selection for earlier emergence, adaptive bet‐hedging, or developmental constraints. Our study offers insight into the fitness consequences of phenological shifts, the mechanisms affecting the fitness consequences of phenological shifts in a community context, and the potential for adaptive responses to climate change.

Ecology; Accepted Articles; July 31, 2018