Density-Dependent Survival in the Larval Stage of an Invasive Insect: Dispersal vs. Predation

1. The success of invasive species is often thought to be due to release from natural enemies. This hypothesis relies on the assumption that species are regulated by top-down forces in their native range and implies that species are likely to be regulated by bottom-up forces in the invasive range. Neither of these assumptions has been consistently supported with insects, a group which include many highly destructive invasive pest species. 2. Winter moth (Operophtera brumata) is an invasive defoliator in North America that appears to be regulated by mortality in the larval stage in its invasive range. To assess whether regulation in the invasive range is caused by top-down or bottom-up forces, we sought to identify the main causes of larval mortality. 3. To measure the importance of different sources of winter moth larval mortality, we used observational and manipulative field studies to measure dispersal, predation, parasitism, disease. We measured the response of larval dispersal in the field to multiple aspects of foliar quality, including total phenolics, pH 10 oxidized phenolics, trichome density, total nitrogen, total carbon, and carbon-nitrogen ration. We also used manipulative laboratory studies to measure the presence of cannibalism and dispersal. 4. Tree-level declines in density were driven by density-dependent larval dispersal of early instars with very little mortality caused by other factors. Later instar larvae dispersed at increased rates from previously damaged vs. undamaged foliage, and field larval dispersal rates were related to proportion of oxidative phenolics in 2015, suggesting that larval dispersal may have been mediated by an induced decline in foliar quality. 5. We conclude that winter moth population densities are regulated in New England by density-dependent larval dispersal possibly mediated by phenolic oxidative capacity. The suggested role of host plant quality in mediating dispersal means that winter moth population densities in New England appear to be regulated by bottom up forces, aligning with the assumptions of the natural enemy release hypothesis. This is the first study known to the authors presenting data showing a negative effect on insect herbivore performance from pH 10 oxidized phenolics

Induction of the sticky plant defense syndrome in wild tobacco.

Many plants engage in protective mutualisms, offering resources such as extrafloral nectar and shelters to predatory arthropods in exchange for protection against herbivores. Recent work indicates that sticky plants catch small insects and provide this carrion to predators who defend the plants against herbivores. In this study, we investigated whether wild tobacco, Nicotiana attenuata, fits this sticky plant defense syndrome that has been described for other sticky plants. We developed a bioassay for stickiness involving the number of flies that adhered to flowers, the stickiest tissues. In surveys conducted over three field seasons at four sites, we found that the number of carrion that adhered to a plant was positively correlated with the number of predators that we observed foraging over its surfaces. The number of predators was positively correlated with the number of seed capsules that the plant produced, a measure of lifetime female reproductive success. Structural equation modeling indicated strong support for the causal path linking carrion numbers to predator numbers to capsule production. We investigated whether stickiness was an inducible trait and examined two potential cues. We found that experimental clipping of rosette leaves induced greater stickiness, although clipping of neighboring sagebrush leaves did not. Damage to leaf tissue is likely to be a more reliable predictor of risk than is damage to a neighboring plant. The sticky plant defense syndrome is a widespread protective mutualism; its strength and ecological relevance can adjust as risk of herbivory changes

Climate Change, Predator-Prey Interactions, and Population Dynamics of the Ranchman’s Tiger Moth (Arctia virginalis)

In my dissertation, I examined how a changing environment affects Ranchman’s tiger moth (Arctia virginalis) population dynamics via predator-prey and host-pathogen interactions. I also examined the complex ways in which biotic drivers of population dynamics interact with climate forcing.In Chapter 1, I examined how body size mediates the effect of warming on the interaction between Arctia virginalis and an ant predator (Formica lasioides). I also developed a general framework for understanding warming effects on stage or size-dependent predator-prey interactions. Specifically, I showed through experiments and modelling that A. virginalis is only vulnerable to predation by F. lasioides when small. This window of vulnerability narrows as the development rate of A. virginalis increases with warming. However, the attack rate of F. lasioides also increases with warming and overcompensates for the decreasing window of prey vulnerability. We therefore project warming to favor the predator in this case, in contrast to the results of previous related work in other systems. In Chapter 2, I expanded upon Chapter 1 by examining the effects of warming on predator-prey interactions in multi-predator communities. In Chapter 1, I showed that asymmetries in predator-prey thermal response rates can result in changing interactions, constituting an important indirect effect of warming. In demographic models using simulated and empirically informed parameters from a natural community of ant predators, I showed that greater predator diversity paired with sufficient thermal niche diversity attenuates these indirect effects of warming, leaving only direct, physiological effects. This result depends on predator diversity and thermal niche diversity and complementarity, which has significant implications for how we might expect warming to affect predator-prey interactions in different communities dependent on traits of the community thermal niche. In Chapter 3, I examined viral disease as a mechanism for delayed density-dependent dynamics in A. virginalis populations and the role of ultraviolet radiation in reducing viral infection through attenuating virions persisting in the environment. I censused 18 populations across 9° of latitude and a gradient of ultraviolet radiation intensity for two years and measured viral infection rate, severity, and survival of lab-reared caterpillars. I found that caterpillar density in the previous year led to a higher infection rate and severity and lower survival and that ultraviolet radiation led to lower infection severity and higher survival. This suggested that virus is the main mechanism for cyclic dynamics in this species, which has been proposed theoretically but rarely shown empirically. I also found a population-level effect of ultraviolet radiation on viral infection severity, which had not been shown previously. In Chapter 4, I analyzed long-term A. virginalis census data, finding that changing precipitation patterns due to changes in large-scale climate led to qualitative changes in population dynamics. Using change-point analysis and state-space models, I showed that caterpillar dynamics transitioned from short to long-period dynamics concurrent with a change in precipitation dynamics. Using deterministic simulations, I showed that shifting dynamics were likely due to resonance: precipitation patterns interfered with cycles initially and later amplified cycles

Climate Change, Predator-Prey Interactions, and Population Dynamics of the Ranchman’s Tiger Moth (Arctia virginalis)

In my dissertation, I examined how a changing environment affects Ranchman’s tiger moth (Arctia virginalis) population dynamics via predator-prey and host-pathogen interactions. I also examined the complex ways in which biotic drivers of population dynamics interact with climate forcing.In Chapter 1, I examined how body size mediates the effect of warming on the interaction between Arctia virginalis and an ant predator (Formica lasioides). I also developed a general framework for understanding warming effects on stage or size-dependent predator-prey interactions. Specifically, I showed through experiments and modelling that A. virginalis is only vulnerable to predation by F. lasioides when small. This window of vulnerability narrows as the development rate of A. virginalis increases with warming. However, the attack rate of F. lasioides also increases with warming and overcompensates for the decreasing window of prey vulnerability. We therefore project warming to favor the predator in this case, in contrast to the results of previous related work in other systems. In Chapter 2, I expanded upon Chapter 1 by examining the effects of warming on predator-prey interactions in multi-predator communities. In Chapter 1, I showed that asymmetries in predator-prey thermal response rates can result in changing interactions, constituting an important indirect effect of warming. In demographic models using simulated and empirically informed parameters from a natural community of ant predators, I showed that greater predator diversity paired with sufficient thermal niche diversity attenuates these indirect effects of warming, leaving only direct, physiological effects. This result depends on predator diversity and thermal niche diversity and complementarity, which has significant implications for how we might expect warming to affect predator-prey interactions in different communities dependent on traits of the community thermal niche. In Chapter 3, I examined viral disease as a mechanism for delayed density-dependent dynamics in A. virginalis populations and the role of ultraviolet radiation in reducing viral infection through attenuating virions persisting in the environment. I censused 18 populations across 9° of latitude and a gradient of ultraviolet radiation intensity for two years and measured viral infection rate, severity, and survival of lab-reared caterpillars. I found that caterpillar density in the previous year led to a higher infection rate and severity and lower survival and that ultraviolet radiation led to lower infection severity and higher survival. This suggested that virus is the main mechanism for cyclic dynamics in this species, which has been proposed theoretically but rarely shown empirically. I also found a population-level effect of ultraviolet radiation on viral infection severity, which had not been shown previously. In Chapter 4, I analyzed long-term A. virginalis census data, finding that changing precipitation patterns due to changes in large-scale climate led to qualitative changes in population dynamics. Using change-point analysis and state-space models, I showed that caterpillar dynamics transitioned from short to long-period dynamics concurrent with a change in precipitation dynamics. Using deterministic simulations, I showed that shifting dynamics were likely due to resonance: precipitation patterns interfered with cycles initially and later amplified cycles

Effects of experimental watering but not warming on herbivory vary across a gradient of precipitation.

Climate change can affect biotic interactions, and the impacts of climate on biotic interactions may vary across climate gradients. Climate affects biotic interactions through multiple drivers, although few studies have investigated multiple climate drivers in experiments. We examined the effects of experimental watering, warming, and predator access on leaf water content and herbivory rates of woolly bear caterpillars (Arctia virginalis) on a native perennial plant, pacific silverweed (Argentina anserina ssp. pacifica), at two sites across a gradient of precipitation in coastal California. Based on theory, we predicted that watering should increase herbivory at the drier end of the gradient, predation should decrease herbivory, and watering and warming should have positive interacting effects on herbivory. Consistent with our predictions, we found that watering only increased herbivory under drier conditions. However, watering increased leaf water content at both wetter and drier sites. Warming increased herbivory irrespective of local climate and did not interact with watering. Predation did not affect herbivory rates. Given predictions that the study locales will become warmer and drier with climate change, our results suggest that the effects of future warming and drying on herbivory may counteract each other in drier regions of the range of Argentina anserina. Our findings suggest a useful role for range-limit theory and the stress-gradient hypothesis in predicting climate change effects on herbivory across stress gradients. Specifically, if climate change decreases stress, herbivory may increase, and vice versa for increasing stress. In addition, our work supports previous suggestions that multiple climate drivers are likely to have dampening effects on biotic interactions due to effects in different directions, though this is context-dependent

Hilltopping influences spatial dynamics in a patchy population of tiger moths.

Dispersal is a key driver of spatial population dynamics. Dispersal behaviour may be shaped by many factors, such as mate-finding, the spatial distribution of resources, or wind and currents, yet most models of spatial dynamics assume random dispersal. We examined the spatial dynamics of a day-flying moth species (Arctia virginalis) that forms mating aggregations on hilltops (hilltopping) based on long-term adult and larval population censuses. Using time-series models, we compared spatial population dynamics resulting from empirically founded hilltop-based connectivity indices and modelled the interactive effects of temperature, precipitation and density dependence. Model comparisons supported hilltop-based connectivity metrics including hilltop elevation over random connectivity, suggesting an effect of hilltopping behaviour on dynamics. We also found strong interactive effects of temperature and precipitation on dynamics. Simulations based on fitted time-series models showed lower patch occupancy and regional synchrony, and higher colonization and extinction rates when hilltopping was included, with potential implications for the probability of persistence of the patch network. Overall, our results show the potential for dispersal behaviour to have important effects on spatial population dynamics and persistence, and we advocate the inclusion of such non-random dispersal in metapopulation models

Induction of the sticky plant defense syndrome in wild tobacco.

Many plants engage in protective mutualisms, offering resources such as extrafloral nectar and shelters to predatory arthropods in exchange for protection against herbivores. Recent work indicates that sticky plants catch small insects and provide this carrion to predators who defend the plants against herbivores. In this study, we investigated whether wild tobacco, Nicotiana attenuata, fits this sticky plant defense syndrome that has been described for other sticky plants. We developed a bioassay for stickiness involving the number of flies that adhered to flowers, the stickiest tissues. In surveys conducted over three field seasons at four sites, we found that the number of carrion that adhered to a plant was positively correlated with the number of predators that we observed foraging over its surfaces. The number of predators was positively correlated with the number of seed capsules that the plant produced, a measure of lifetime female reproductive success. Structural equation modeling indicated strong support for the causal path linking carrion numbers to predator numbers to capsule production. We investigated whether stickiness was an inducible trait and examined two potential cues. We found that experimental clipping of rosette leaves induced greater stickiness, although clipping of neighboring sagebrush leaves did not. Damage to leaf tissue is likely to be a more reliable predictor of risk than is damage to a neighboring plant. The sticky plant defense syndrome is a widespread protective mutualism; its strength and ecological relevance can adjust as risk of herbivory changes