Lynn S. Adler

Induced plant responses and information content about risk of herbivory

Plant defenses are plastic when a single genotype can produce different phenotypes depending upon the environment. Plastic responses might be favored by selection only if plants can respond appropriately to reliable information in their environments. Recent findings indicate that when information is accurate, plants can benefit by changing their defenses appropriately but, when information is inaccurate they produce inappropriate defenses and have lower fitness. Plants can potentially use a variety of cues to adjust their defensive phenotypes appropriately. The relationship between the information about risk of herbivory and plant defense can be evaluated by determining if the information available to plants is reliable enough to support the evolution of plastic-induced defenses.

The Dual Role of Floral Traits: Pollinator Attraction and Plant Defense

Plants are under siege from a diversity of enemies that consume both leaf and floral parts. Plants resist damage to leaves in a variety of ways, and we now have a rich literature documenting how plants defend themselves against herbivore attack. In con- trast, the mechanisms by which plants resist enemies that consume floral parts or resources are much less known, even though damage to floral tissue usually has tighter links to plant fitness than damage to leaf tissue. Many plants experience nectar robbing, whereby floral visitors remove nectar from flowers, often without pollinating. Nectar robbers can reduce plant fitness to degrees comparable to, or even surpassing, reduction by herbivores. How- ever, because nectar attracts both pollinators and nectar robbers, plants face a dilemma in defending against nectar robbers without also deterring pollinators. Here, we extend the conceptual framework of resistance to herbivores to include resistance to nectar robbers, focusing on nectar traits. We review published data and find that an array of nectar traits may deter robbers without deterring pollinators. Although resistance traits against robbers have been broadly identified, the costs and benefits of these traits in terms of plant fitness remain poorly understood. We present data showing that a nectar trait (dilute nectar) might directly, as well as indirectly, benefit plant fitness by deterring nectar-robbing bumble bees of Ipomopsis aggregata without deterring hummingbird pollinators. However, the magni- tude of any plant fitness benefit will depend on the degree to which plants are pollen- vs. resource-limited in a given year. The results of our work offer both conceptual and empirical insight into how plants cope with attack by nonpollinating floral visitors through a relatively unexplored trait, nectar.

ECOLOGICAL COSTS AND BENEFITS OF DEFENSES IN NECTAR

The nectar of many plant species contains defensive compounds that have been hypothesized to benefit plants through a variety of mechanisms. However, the rela- tionship between nectar defenses and plant fitness has not been established for any species. We experimentally manipulated gelsemine, the principal alkaloid of Carolina jessamine (Gelsemium sempervirens ), in nectar to determine its effect on pollinator visitation, nectar robber visitation, and male and female plant reproduction. We found that nectar robbers and most pollinators probed fewer flowers and spent less time per flower on plants with high compared to low nectar alkaloids. High alkaloids decreased the donation of fluorescent dye, an analogue of pollen used to estimate male plant reproduction, to neighboring plants by one-third to one-half. However, nectar alkaloids did not affect female plant reproduction, measured as pollen receipt, fruit set, seed set, and seed mass. The weak effects of nectar alkaloids on female reproduction could represent a balance between the altered behavior of nectar robbers and pollinators, or it could be that neither of these interactions affected plant reproduction. Taken together, these results suggest that secondary compounds in nectar may have more costs than benefits for plants.

DIRECT AND INDIRECT EFFECTS OF ALKALOIDS ON PLANT FITNESS VIA HERBIVORY AND POLLINATION

Herbivores and pollinators can simultaneously exert selective pressures on plant traits via direct and indirect effects. Net selection on plant traits, such as defensive chemistry, may be difficult to predict from studying either of these interactions in isolation. In this study, alkaloids were manipulated experimentally in the hemiparasitic annual plant Castilleja indivisa (Scrophulariaceae; Indian paintbrush) by growing these parasites with bitter (high-alkaloid) or sweet (low-alkaloid) near-isogenic lines of the host Lupinus albus (Fabaceae) in the field. To evaluate the effect of herbivores, half of the Indian paintbrush plants were randomly assigned to a reduced-herbivory treatment using insecticide, and the other half to a natural-herbivory treatment. Floral traits, bud and fruit herbivory, pollination, alkaloids, and plant performance were measured. These variables were used in a path analysis to dissect the direct and indirect effects of herbivory and pollination on lifetime seed set, and the direct and indirect effects of alkaloids on seed set via herbivory and pollination. Bud herbivory and fruit herbivory directly decreased seed production, whereas polli- nation had a direct positive effect. In addition, bud herbivory had negative indirect effects on seed set by reducing the number of open flowers, which reduced pollinator visits. Alkaloids directly reduced bud herbivory but did not significantly affect pollination or fruit herbivory directly. However, because bud herbivory indirectly reduced seed set by reducing pollinator visits to flowers, alkaloids also had additional indirect benefits for plants by increasing pollination. Overall, the net benefit of alkaloid uptake was due to both reduction in herbivory and an increase in pollinator visits to flowers. This study demonstrates the importance of considering multiple interactions simultaneously when attempting to under- stand the mechanisms underlying correlations between plant traits and fitness.

ATTRACTING ANTAGONISTS: DOES FLORAL NECTAR INCREASE LEAF HERBIVORY?

Traits that are attractive to mutualists may also attract antagonists, resulting in conflicting selection pressures. Here we develop the idea that increased floral nectar production can, in some cases, increase herbivory. In these situations, selection for increased nectar production to attract pollinators may be constrained by a linked cost of herbivore attraction. In support of this hypothesis, we report that experimentally supplementing nectar rewards in Datura stramonium led to increased oviposition by Manduca sexta, a sphingid moth that pollinates flowers, but whose larvae feed on leaf tissue. We speculate that nectar composition may provide information about plant nutritional status or defense that floral visitors could use to make oviposition decisions. Thus, selection by floral visitors and leaf herbivores may be inextricably intertwined, and herbivores may represent a relatively unexplored agent of selection on nectar traits.

Pollinator and Herbivore Attraction to Cucurbita Floral Volatiles

Mutualists and antagonists may place conflicting selection pressures on plant traits. For example, the evolution of floral traits is typically studied in the context of attracting pollinators, but traits may incur fitness costs if they are also attractive to antagonists. Striped cucumber beetles (Acalymma vittatum) feed on cucurbits and are attracted to several volatiles emitted by Cucurbita blossoms. However, the effect of these volatiles on pollinator attraction is unknown. Our goal was to determine whether pollinators were attracted to the same or different floral volatiles as herbivorous cucumber beetles. We tested three volatiles previously found to attract cucumber beetles in a factorial design to determine attraction of squash bees (Peponapis pruinosa), the specialist pollinators of cucurbita species, as well as the specialist herbivore A. vittatum. We found that 1,2,4-trimethoxybenzene was attractive to both the pollinator and the herbivore, indole was attractive only to the herbivore, and (E)-cinnamaldehyde was attractive only to the pollinator. There were no interactions among volatiles on attraction of squash bees or cucumber beetles. Our results suggest that reduced indole emission could benefit plants by reducing herbivore attraction without loss of pollination, and that 1,2,4-trimethoxybenzene might be under conflicting selection pressure from mutualists and antagonists. By examining the attraction of both mutualists and antagonists to Cucurbita floral volatiles, we have demonstrated the potential for some compounds to influence only one type of interaction, while others may affect both interactions and possibly result in tradeoffs. These results shed light on the potential evolution of fragrance in native Cucurbita, and may have consequences for yield in agricultural settings.

Alkaloid Uptake Increases Fitness in a Hemiparasitic Plant via Reduced Herbivory and Increased Pollination

It has been historically difficult to manipulate secondary compounds in living plants to assess how these compounds influence plant‐herbivore and plant‐pollinator interactions. Using a hemiparasitic plant that takes up secondary compounds from host plants, I experimentally manipulated secondary compounds in planta and assessed their effects on herbivores and pollinators in the field. Here, I show that the uptake of alkaloids in the annual hemiparasite Castilleja indivisa resulted in decreased herbivory, increased visitation by pollinators, and increased lifetime seed production. These results indicate that resistance traits such as alkaloids can increase plant fitness directly by reducing herbivore attack and indirectly by increasing pollinator visitation to defended plants. Thus, selection for production of secondary compounds may be underestimated by considering only the direct effect of herbivores on plant fitness.

Reliance on pollinators predicts defensive chemistry across tobacco species

Defensive traits are typically studied in the context of avoiding antagonists, but may also mediate key interactions with mutualists. Plant chemical defences occur in flowers, suggesting pollinators may be agents of selection on defence. We hypothesised that floral defences would deter pollinators, and therefore, pollinators would select for lower defences in outcrossing than self-pollinating species. We measured pollinator reliance and alkaloid levels in 32 greenhouse-grown Nicotiana species. Using a comparative phylogenetic approach, we found significantly lower nectar, floral and leaf nicotine concentrations in outcrossing than selfing species, with a 15-fold decrease in leaf nicotine levels. Nicotine concentrations were positively correlated across tissues, suggesting that selection against floral defences could constrain the evolution of leaf defences. Thus, pollinators could shape the evolution not only of floral defences but also of defences in other tissues where herbivores have traditionally been considered the dominant agent of selection.

Secondary metabolites in floral nectar reduce parasite infections in bumblebees

The synthesis of secondary metabolites is a hallmark of plant defence against herbivores. These compounds may be detrimental to consumers, but can also protect herbivores against parasites. Floral nectar commonly contains secondary metabolites, but little is known about the impacts of nectar chemistry on pollinators, including bees. We hypothesized that nectar secondary metabolites could reduce bee parasite infection. We inoculated individual bumblebees with Crithidia bombi, an intestinal parasite, and tested effects of eight naturally occurring nectar chemicals on parasite population growth. Secondary metabolites strongly reduced parasite load, with significant effects of alkaloids, terpenoids and iridoid glycosides ranging from 61 to 81%. Using microcolonies, we also investigated costs and benefits of consuming anabasine, the compound with the strongest effect on parasites, in infected and uninfected bees. Anabasine increased time to egg laying, and Crithidia reduced bee survival. However, anabasine consumption did not mitigate the negative effects of Crithidia, and Crithidia infection did not alter anabasine consumption. Our novel results highlight that although secondary metabolites may not rescue survival in infected bees, they may play a vital role in mediating Crithidia transmission within and between colonies by reducing Crithidia infection intensities.

Advertising to the enemy: enhanced floral fragrance increases beetle attraction and reduces plant reproduction

Many organisms face challenges in avoiding predation while searching for mates. For plants, emitting floral fragrances to advertise reproductive structures could increase the attraction of detrimental insects along with pollinators. Very few studies have experimentally evaluated the costs and benefits of fragrance emission with explicit consideration of how plant fitness is affected by both pollinators and florivores. To determine the reproductive consequences of increasing the apparency of reproductive parts, we manipulated fragrance, pollination, and florivores in the wild Texas gourd, Cucurbita pepo var. texana. With enhanced fragrance we found an increase in the attraction of florivores, rather than pollinators, and a decrease in seed production. This study is the first to demonstrate that enhanced floral fragrance can increase the attraction of detrimental florivores and decrease plant reproduction, suggesting that florivory as well as pollination has shaped the evolution of floral scent.