Self-Medication as Adaptive Plasticity: Increased Ingestion of Plant Toxins by Parasitized Caterpillars

Self-medication is a specific therapeutic behavioral change in response to disease or parasitism. The empirical literature on self-medication has so far focused entirely on identifying cases of self-medication in which particular behaviors are linked to therapeutic outcomes. In this study, we frame self-medication in the broader realm of adaptive plasticity, which provides several testable predictions for verifying self-medication and advancing its conceptual significance. First, self-medication behavior should improve the fitness of animals infected by parasites or pathogens. Second, self-medication behavior in the absence of infection should decrease fitness. Third, infection should induce self-medication behavior. The few rigorous studies of self-medication in non-human animals have not used this theoretical framework and thus have not tested fitness costs of self-medication in the absence of disease or parasitism. Here we use manipulative experiments to test these predictions with the foraging behavior of woolly bear caterpillars (Grammia incorrupta; Lepidoptera: Arctiidae) in response to their lethal endoparasites (tachinid flies). Our experiments show that the ingestion of plant toxins called pyrrolizidine alkaloids improves the survival of parasitized caterpillars by conferring resistance against tachinid flies. Consistent with theoretical prediction, excessive ingestion of these toxins reduces the survival of unparasitized caterpillars. Parasitized caterpillars are more likely than unparasitized caterpillars to specifically ingest large amounts of pyrrolizidine alkaloids. This case challenges the conventional view that self-medication behavior is restricted to animals with advanced cognitive abilities, such as primates, and empowers the science of self-medication by placing it in the domain of adaptive plasticity theory

Crop pests and predators exhibit inconsistent responses to surrounding landscape composition

The idea that noncrop habitat enhances pest control and represents a win–win opportunity to conserve biodiversity and bolster yields has emerged as an agroecological paradigm. However, while noncrop habitat in landscapes surrounding farms sometimes benefits pest predators, natural enemy responses remain heterogeneous across studies and effects on pests are inconclusive. The observed heterogeneity in species responses to noncrop habitat may be biological in origin or could result from variation in how habitat and biocontrol are measured. Here, we use a pest-control database encompassing 132 studies and 6,759 sites worldwide to model natural enemy and pest abundances, predation rates, and crop damage as a function of landscape composition. Our results showed that although landscape composition explained significant variation within studies, pest and enemy abundances, predation rates, crop damage, and yields each exhibited different responses across studies, sometimes increasing and sometimes decreasing in landscapes with more noncrop habitat but overall showing no consistent trend. Thus, models that used landscape-composition variables to predict pest-control dynamics demonstrated little potential to explain variation across studies, though prediction did improve when comparing studies with similar crop and landscape features. Overall, our work shows that surrounding noncrop habitat does not consistently improve pest management, meaning habitat conservation may bolster production in some systems and depress yields in others. Future efforts to develop tools that inform farmers when habitat conservation truly represents a win–win would benefit from increased understanding of how landscape effects are modulated by local farm management and the biology of pests and their enemies

Understanding, using, and promoting biological control: from commercial walnut orchards to school gardens

Growing populations and changing diets have put great pressure on food systems throughout the world and have lead to increasing agricultural intensification including the greater use of pesticides and fertilizers. Given the associated human and environmental health costs of intensification, the development of more sustainable practices is imperative. One such avenue is to make better use of natural ecosystem services, such as the use of conservation biological control to reduce reliance on pesticide. However, there are logistical and educational impediments to the more effective use of resident natural enemies through conservation biological control that need to be addressed. These include how other agricultural management practices impact biological control, and how managers can tell if it is working or when it will work. Along with pesticides, fertilizers are a defining aspect of modern agriculture, but their effect on biological control services has seldom been evaluated. The effects of plant quality on natural enemies are often overlooked developing biological control programs for insect pests in agriculture. An enhanced nutritional status of plants can fuel insect population growth because nitrogen is an important component of proteins that are known to be limiting for phytophagous insects. Additionally, nitrogen fertilizers directly and indirectly affect plant defenses. In this dissertation I used walnuts to address the effect of increased nitrogen availability to the host plant on walnut aphid \textit{Chromaphis juglandicola} and on parasitism by the specialist parasitoid \textit{Trioxys pallidus}. From laboratory experiments and field sampling, nitrogen content of foliage did not change aphid population growth rate or aphid size. However, in laboratory experiments added nitrogen decreased the number of mummies produced by female parasitoids over a 24 h period, but increased the proportion and the size of female offspring. Field sampling of walnut orchards showed no relationship between the percent parasitism of walnut aphids by \textit{T. pallidus} and nitrogen content of foliage. Although nitrogen fertilizer and plant quality can affect biological control in other crops, it did not appear to be a problem for biological control of walnut aphids.Biological control in action is often hard to visualize and even more difficult to quantify in the context of pest population management. Readily measured metrics are needed to accurately predict the effectiveness of biological control services: this would then allow managers to say, given this set of measurements, control of an insect pest can be expected today or at some point in the near future. Using walnuts and walnut aphids as a model system, I investigated whether activity measurements and diversity indices for the natural enemy assemblages present in walnut orchards would be good indicators of current and future biological control. While percent parasitism, predator:prey ratio, and natural enemy evenness were good indicators of current biological control, there were no good indicators of future biological control. An increase in natural enemy units, a measure of abundance weighted by the feeding or parasitism capacities of individual species, was correlated with a decrease in aphids over the season, but, as there was also a strong effect of within-season density dependence in the walnut aphid populations, the correlation is more likely to be an artifact rather than a causal relationship. The composition of a local natural enemy assemblage depends on both the local environment, which acts as a filter, and the surrounding landscape, which serves as a regional pool of natural enemy species. When the surrounding landscape is the dominant factor, measures of landscape complexity can be used to predict the composition of the local natural enemy community. For more urbanized environments, however, local factors can be as important as landscape factors. Urban gardens are an ideal study system to address such questions as they are often spread along an urbanization gradient and yet differ considerably in local composition. For home and school gardens in the South Peninsula of the San Francisco Bay, urbanization had a non-linear effect on natural enemy richness with greater richness in both the most urban and most rural gardens. Moreover, urbanization was also positively related to natural enemy abundance on tomato plants, a key urban garden crop. In addition, the use of natural enemy exclosures showed that natural enemy richness was significantly related to the degree of suppression of aphids on fava bean plants, suggesting that increasing natural enemy richness could improve biological control. However, I found no clear elements of the local composition of gardens that could be modified to increase natural enemy richness. The best indicators and economic incentives do not ensure that farmers and gardeners will use biological control instead of pesticides if they are not comfortable with the idea. In this context, Cooperative Extension (CE) provides an effective means to accomplish the successful transfer of new research information on biological control to the farmers and gardeners who could put it into practice. While outreach from CE to large agricultural industries has been well established, urban gardeners represent a relatively new audience for the transfer of research knowledge. As many gardeners in urban and school gardens include children, education about insects and natural enemies could start with very young audiences. A combined scientific and outreach event put on by San Mateo Cooperative Extension demonstrated the significance of early education on this topic. Using pre and post-participation surveys I was able to show that children felt more positively about insects and were even more likely to eat insects after the event. Making research knowledge available and accessible to all ages involved in food production may help to increase the level of adoption of biological control in the future. Biological control is a valuable ecosystem service that could help reduce the negative impacts of the intensification of agriculture. However, more effective ways to visualize, quantify and predict the action of natural enemies are needed to make conservation biological control an essential part of the pest management tool kit for farmers and gardeners

Cosmetic pesticide use: quantifying use and its policy implications in California, USA

Pesticide use is increasingly under scrutiny for its environmental and human health impacts. While government leaders promote sustainable pest management, including reductions in pesticide usage, growers face pressure to produce agricultural commodities at high cosmetic standards, which often requires the use of pesticides. California (United States) has a productive agricultural industry, many sustainability initiatives and a government that actively regulates pesticide use. We identified two cases where it was possible to quantify cosmetic pesticide use in California: stink bug control in processing tomato and red colour and large size in table grape. Between 2009 and 2019, 1.47% and 7.7% of total hectares treated with pesticides were treated with the subset of cosmetic pesticides examined in this study in processing tomato, and table and raisin grape, respectively. Individual hectares can be treated with multiple pesticides that each adds to the total hectares. We identified unique hectares treated with cosmetic pesticides: 8.14% and 57.1% of harvested hectares received at least one application of a cosmetic pesticide in processing tomato, and table and raisin grape, respectively. The current food system that supports high cosmetic standards, and thus demands pesticide usage, can inhibit the adoption of and transition to sustainable agricultural systems

Proactive biological control: A cost-effective management option for invasive pests

Proactive biocontrol could accelerate responses to invasive pests in urban areas — where pesticide use may be unpopular — before they spread to agricultural areas

Least square mean (±1 SE) of the total amount of the food block eaten by <i>G. incorrupta</i> caterpillars over 5 days in the feeding choice experiment according to parasitism treatment (0–3 <i>E. mella</i> eggs) and post-assay survival to adulthood (survived, died).

<p>Asterisks denote significant differences among means of survivors and victims within each treatment from a Tukey-Kramer test (see text for statistics).</p

Least square mean (±1 SE) of the total amount of the PA block eaten by <i>G. incorrupta</i> caterpillars over 5 days in the feeding choice experiment according to parasitism treatment (0–3 <i>E. mella</i> eggs) and post-assay survival to adulthood (survived, died).

<p>Asterisks denote significant differences among means of survivors and victims within each treatment from a Tukey-Kramer test (see text for statistics).</p

Univariate (ANCOVA) responses of feeding intake by caterpillars in the choice experiment, quantified in terms of i) the angularly transformed percentage of overall intake from the PA block, ii) the log transformed absolute intake of the PA block, and iii) the log transformed absolute intake of the food block over five days.

<p>Significant <i>P</i> values are marked by boldface type.</p

ANCOVA responses of feeding intake by caterpillars in the choice experiment, quantified in terms of i) the angularly transformed percentage of overall intake from the PA block, ii) the log transformed absolute intake of the PA block, and iii) the log transformed overall intake (PA+food block) over five days.

<p>Significant <i>P</i> values are marked by boldface type.</p