Eric F. LoPresti

Chemicals on plant surfaces as a heretofore unrecognized, but ecologically informative, class for investigations into plant defence

Plants produce and utilize a great diversity of chemicals for a variety of physiological and ecological purposes. Many of these chemicals defend plants against herbivores, pathogens and competitors. The location of these chemicals varies within the plant, some are located entirely within plant tissues, others exist in the air‐ (or water‐) space around plants, and still others are secreted onto plant surfaces as exudates. I argue herein that the location of a given defensive chemical has profound implications for its ecological function; specifically, I focus on the characteristics of chemical defences secreted onto plant surfaces. Drawing from a broad literature encompassing ecology, evolution, taxonomy and physiology, I found that these external chemical defences (ECDs) are common and widespread in plants and algae; hundreds of examples have been detailed, yet they are not delineated as a separate class from internal chemical defences (ICDs). I propose a novel typology for ECDs and, using existing literature, explore the ecological consequences of the hypothesized unique characteristics of ECDs. The axis of total or proportional investment in ECDs versus ICDs should be considered as one axis of investment by a plant, in the same way as quantitative versus qualitative chemical defences or induced versus constitutive defences is considered. The ease of manipulating ECDs in many plant systems presents a powerful tool to help test plant defence theory (e.g. optimal defence). The framework outlined here integrates various disciplines of botany and ecology and suggests a need for further examinations of exudates in a variety of contexts, as well as recognition of the effects of within‐plant localization of defences.

Chenopod salt bladders deter insect herbivores.

Trichomes on leaves and stems of certain chenopods (Chenopodiaceae) are modified with a greatly enlarged apical cell (a salt bladder), containing a huge central vacuole. These structures may aid in the extreme salt tolerance of many species by concentrating salts in the vacuole. Bladders eventually burst, covering the leaf in residue of bladder membranes and solid precipitates. The presence of this system in non-halophytic species suggests additional functions. I tested the novel hypothesis that these bladders have a defensive function against insect herbivores using choice, no choice, and field tests. Generalist insect herbivores preferred to feed on leaves without salt bladders in choice tests. In no choice tests, herbivores consumed less leaf matter with bladders. In a field test, leaves from which I had removed bladders suffered greater herbivory than adjacent leaves with bladders. Solutions containing bladders added to otherwise preferred leaves deterred herbivores, suggesting a water-soluble chemical component to the defense. This bladder system has a defensive function in at least four genera of chenopods. Salt bladders may be a structural defense, like spines or domatia, but also have a chemical defense component.

Chewing sandpaper: grit, plant apparency, and plant defense in sand-entrapping plants.

Sand entrapment on plant surfaces, termed psammophory or sand armor, is a phylogenetically and geographically widespread trait. The functional significance of this phenomenon has been poorly investigated. Sand and soil are nonnutritive and difficult for herbivores to process, as well as visually identical to the background. We experimentally investigated whether this sand coating physically protected the plant from herbivores or increased crypsis (e.g., decreased apparency to herbivores). We tested the former hypothesis by removing entrapped sand from stems, petioles, and leaves of the sand verbena Abronia latifolia and by supplementing natural sand levels in the honeyscented pincushion plant Navarretia mellita. Consistent with a physical defensive function, leaves with sand present or supplemented suffered less chewing herbivory than those with sand removed or left as is. To test a possible crypsis effect, we coated some sand verbena stems with green sand, matching the stem color, as well as others with brown sand to match the background color. Both suffered less chewing herbivory than controls with no sand and herbivory did not significantly differ between the colors, suggesting crypsis was not the driving resistance mechanism. Strong tests of plant apparency are rare; this experimental approach may be possible in other systems and represents one of few manipulative tests of this long-standing hypothesis.

Plant structural complexity and mechanical defenses mediate predator-prey interactions in an odonate-bird system

Abstract Habitat‐forming species provide refuges for a variety of associating species; these refuges may mediate interactions between species differently depending on the functional traits of the habitat‐forming species. We investigated refuge provisioning by plants with different functional traits for dragonfly and damselfly (Odonata: Anisoptera and Zygoptera) nymphs emerging from water bodies to molt into their adult stage. During this period, nymphs experience high levels of predation by birds. On the shores of a small pond, plants with mechanical defenses (e.g., thorns and prickles) and high structural complexity had higher abundances of odonate exuviae than nearby plants which lacked mechanical defenses and exhibited low structural complexity. To disentangle the relative effects of these two potentially important functional traits on nymph emergence‐site preference and survival, we conducted two fully crossed factorial field experiments using artificial plants. Nymphs showed a strong preference for artificial plants with high structural complexity and to a lesser extent, mechanical defenses. Both functional traits increased nymph survival but through different mechanisms. We suggest that future investigations attempt to experimentally separate the elements contributing to structural complexity to elucidate the mechanistic underpinnings of refuge provisioning.

The three criteria for resistance by plant carrion-provisioning: insect entrapment and predator enrichment on Mimulus bolanderi

1. Many sticky plants provision mutualistic scavenging arthropod predators with carrion, which in turn protect the plant from insect herbivores. While insect entrapment is a common trait across plants, which plants attract these predators and may derive protection is still largely unknown.

Entrapped sand as a plant defence: effects on herbivore performance and preference: Entrapped sand and caterpillar performance

1. Abrasive material in the diet of herbivorous organisms comes from a variety of sources, including crystalline silica or calcium in plant tissues, accidentally ingested soil while digging or grazing, and entrapped substrate on the surfaces of plants. A wide variety of plants entrap substrate, usually with glandular trichomes.

Polyphagy by omnivory: scavenging improves performance of a polyphagous caterpillar on marginal hosts

Few species of insect herbivores are highly polyphagous, but those few species are disproportionately ecologically and economically important and include many of the most destructive crop pests. Common correlates of extreme polyphagy across insects include the related behaviors of cannibalism and omnivory, though any functional consequences of these behaviors on the host range are unknown. I hypothesized that omnivory may allow these insects to exploit marginal hosts successfully (an expansion of realized niche). Using the polyphagous pest caterpillar, Heliothis virescens, I tested the polyphagy by omnivory hypothesis using ten host plants of varying suitability and small quantities of insect carrion. Caterpillars which were allowed omnivory had increased performance on lower-quality hosts; this treatment raised survival, growth rate, and pupal mass over controls on a strictly plant diet. Omnivory allowed successful development on two plants that caterpillars could not exploit alone a potential niche expansion. This effect was limited, however: (1) on high-quality hosts, omnivory did not improve performance, and (2) omnivory on poor hosts did not increase growth rate or pupal mass to levels matching the most suitable hosts and it could not permit exploitation of a completely unpalatable plant. Omnivory may therefore be an important (and overlooked) factor in determining the success of generalist insect herbivores in a variety of ecological settings.

Artificial rainfall increases herbivory on an externally defended forb

Plants have a variety of herbivore resistance traits, including a diverse array of chemicals, either inside plant tissues or on plant surfaces. External chemical defenses are common and widespread, though understudied as a class. One potential selective force on these defenses is their potential for abiotic dislodgement given their exposed position. I tested whether abiotic removal (artificial rainfall) leads to increased herbivory in the annual chenopod Atriplex rosea. This plant, like other chenopods, has specialized secretory trichomes, which secrete water-soluble herbivore resistance compounds onto the plant’s surfaces. Consistent with this hypothesis, I found significantly greater chewing herbivory in plants which received artificial rainfall compared to no-rainfall controls and a below-leaf water control. This simple experiment demonstrates that abiotic factors can directly change the efficacy of a resistance trait.

Breaking Barriers in Evolutionary Biology: A Pioneering Woman in Science and Her Early Theory of Plant Chemical Macroevolution

Plant secondary chemistry is now a paradigmatic example of adaptation. However, more than 120 years ago (70 years before the oft-cited works of Fraenkel or Ehrlich and Raven ignited the field of chemical ecology), a female scientist named Helen Cecilia de Silver Abbott (1857–1904) published an article in The American Naturalist introducing the radical idea that plant chemistry should be considered in light of macroevolution. Here we revisit the groundbreaking but largely overlooked contribution of Abbott’s (1887) “Comparative Chemistry of Higher and Lower Plants.” Our goal is to spotlight Abbott’s important contribution to the field of chemical ecology and to honor her life as a pioneering woman in science.

Measuring success of a reintroduced population of the American burying beetle (Nicrophorus americanus Olivier) to Nantucket Island, MA

The American burying beetle (Nicrophorus americanus) is a federally listed endangered beetle and since 1993 multiple organizations have collaborated to reintroduce this species to Nantucket Island, Massachusetts, USA. We present evidence that despite very successful reintroduction methods, the reintroduced population is not self-sustaining and requires human assistance for long term maintenance. Beetles were reintroduced from captive stock and each year we augmented the population by trapping wild beetles, pairing males and females, and supplying the pairs with carrion. Long term monitoring of this population has shown that, when provided with carrion, N. americanus on Nantucket have an over winter survival rate of 15 % and a reproductive success rate of 54 %. After seeing the number of beetles captured between 2007 and 2011 double, we modified protocols to determine if the established population would be self-sustaining and we have seen a drastic decline. We suggest that a lack of natural carrion is the main reason for this decline.