Amy M. Trowbridge

Consequences of Climate Warming and Altered Precipitation Patterns for Plant-Insect and Multitrophic Interactions

Understanding and predicting the impacts of anthropogenically driven climate change on species interactions and ecosystem processes is a critical scientific and societal challenge. Climate change has important ecological consequences for species interactions that occur across multiple trophic levels

Contribution of various carbon sources toward isoprene biosynthesis in poplar leaves mediated by altered atmospheric CO2 concentrations.

Biogenically released isoprene plays important roles in both tropospheric photochemistry and plant metabolism. We performed a 13CO2-labeling study using proton-transfer-reaction mass spectrometry (PTR-MS) to examine the kinetics of recently assimilated photosynthate into isoprene emitted from poplar (Populus × canescens) trees grown and measured at different atmospheric CO2 concentrations. This is the first study to explicitly consider the effects of altered atmospheric CO2 concentration on carbon partitioning to isoprene biosynthesis. We studied changes in the proportion of labeled carbon as a function of time in two mass fragments, M41+, which represents, in part, substrate derived from pyruvate, and M69+, which represents the whole unlabeled isoprene molecule. We observed a trend of slower 13C incorporation into isoprene carbon derived from pyruvate, consistent with the previously hypothesized origin of chloroplastic pyruvate from cytosolic phosphenolpyruvate (PEP). Trees grown under sub-ambient CO2 (190 ppmv) had rates of isoprene emission and rates of labeling of M41+ and M69+ that were nearly twice those observed in trees grown under elevated CO2 (590 ppmv). However, they also demonstrated the lowest proportion of completely labeled isoprene molecules. These results suggest that under reduced atmospheric CO2 availability, more carbon from stored/older carbon sources is involved in isoprene biosynthesis, and this carbon most likely enters the isoprene biosynthesis pathway through the pyruvate substrate. We offer direct evidence that extra-chloroplastic rather than chloroplastic carbon sources are mobilized to increase the availability of pyruvate required to up-regulate the isoprene biosynthesis pathway when trees are grown under sub-ambient CO2.

BVOC-Mediated Plant-Herbivore Interactions

Plants release unique blends of biogenic volatile organic compounds (BVOCs) into the atmosphere, part of a silent language used to communicate with other organisms in their community. Within this high traffic chemical environment, plants and insects, among other organisms, are receiving, processing, modifying, and responding to information conveyed through varying suites of molecules. Because plants and insects are part of an integrative complex of food web relationships, one common topic of conversation is defence. Plants maintain a baseline level of BVOC emissions as a bottom-up constitutive defence, emitting compounds that act as repellents or deterrents to feeding and/or egg deposition by herbivores. Due to the autonomy of their attackers, plants can also employ an indirect top-down defence strategy, releasing induced volatiles in response to feeding that attract the natural enemies of their herbivore attackers, such as predators and parasitoids. Both bottom-up and top-down BVOC-mediated strategies have important consequences for herbivore preference, performance, and survival with even broader ecological and evolutionary consequences for tritrophic interactions. In this chapter we discuss how constitutive BVOCs mediate aspects of plant defence within a hierarchical spatiotemporal framework. Next we bring to light some of the most recent research on oviposition- and herbivore-induced BVOC synthesis and subsequent effects on the recruitment of natural enemies. We follow up by discussing the ecological effects of induced BVOCs in the context of multiple herbivores, expression from various plant organs, time-lags associated with BVOC induction, and heterogeneity within the infochemical environment. The critical feature of insect learning is described and we highlight some of the major evolutionary implications of BVOC-mediated plant defence syndromes that rely on the unique timing of events at the biochemical, atmospheric, organismal, and community scales.

Herbivory and climate interact serially to control monoterpene emissions from pinyon pine forests

The emission of volatile monoterpenes from coniferous trees impacts the oxidative state of the troposphere and multi-trophic signaling between plants and animals. Previous laboratory studies have revealed that climate anomalies and herbivory alter the rate of tree monoterpene emissions. However, no studies to date have been conducted to test these relations in situ. We conducted a two-year field experiment at two semiarid sites dominated by pinyon pine (Pinus edulis) during outbreaks of a specialist herbivore, the southwestern tiger moth (Lophocampa ingens: Arctiidae). We discovered that during the early spring, when herbivory rates were highest, monoterpene emission rates were approximately two to six times higher from undamaged needles on damaged trees, with this increase in emissions due to alpha-pinene, beta-pinene, and camphene at both sites. During mid-summer, emission rates did not differ between previously damaged and undamaged trees at the site on the Western Slope of the Rocky Mountains, but rather tracked changes in the temperature and precipitation regime characteristic of the region. As the mid-summer drought progressed at the Eastern Slope site, emission rates were low, but differences between previously damaged and undamaged trees were not statistically significant. Despite no difference in emissions, mid-summer tissue monoterpene concentrations were significantly lower in previously damaged trees at both sites. With the onset of monsoon rains during late summer, emission rates from previously damaged trees increased to levels higher than those of undamaged trees despite the lack of herbivory. We conclude that (1) herbivory systemically increases the flux of terpenes to the atmosphere during the spring, (2) drought overrides the effect of past herbivory as the primary control over emissions during the mid-summer, and (3) a release from drought and the onset of late-summer rains is correlated with a secondary increase in emissions, particularly from herbivore-damaged trees, possibly due to a drought-delayed stimulation of induced monoterpene synthesis and/or increases in stomatal conductance. A greater understanding of the interactive effects of seasonality and herbivory on monoterpene emissions provides much needed information regarding the atmospheric and ecological consequences that these compounds will have for semiarid ecosystems.

Linking meteorology, turbulence, and air chemistry in the Amazon Rain Forest

AbstractWe describe the salient features of a field study whose goals are to quantify the vertical distribution of plant-emitted hydrocarbons and their contribution to aerosol and cloud condensation nuclei production above a central Amazonian rain forest. Using observing systems deployed on a 50-m meteorological tower, complemented with tethered balloon deployments, the vertical distribution of hydrocarbons and aerosols was determined under different boundary layer thermodynamic states. The rain forest emits sufficient reactive hydrocarbons, such as isoprene and monoterpenes, to provide precursors of secondary organic aerosols and cloud condensation nuclei. Mesoscale convective systems transport ozone from the middle troposphere, enriching the atmospheric boundary layer as well as the forest canopy and surface layer. Through multiple chemical transformations, the ozone-enriched atmospheric surface layer can oxidize rain forest–emitted hydrocarbons. One conclusion derived from the field studies is that the...

Global change effects on plant–insect interactions: the role of phytochemistry

Natural and managed ecosystems are undergoing rapid environmental change due to a growing human population and associated increases in industrial and agricultural activity. Global environmental change directly and indirectly impacts insect herbivores and pollinators. In this review, we highlight recent research examining how environmental change factors affect plant chemistry and, in turn, ecological interactions among plants, herbivores, and pollinators. Recent studies reveal the complex nature of understanding global change effects on plant secondary metabolites and plant-insect interactions. Nonetheless, these studies indicate that phytochemistry mediates insect responses to environmental change. Future research on the chemical ecology of plant-insect interactions will provide critical insight into the ecological effects of climate change and other anthropogenic disturbances. We recommend greater attention to investigations examining interactive effects of multiple environmental change factors in addition to chemically mediated plant-pollinator interactions, given limited research in these areas.

Conifer Monoterpene Chemistry during an Outbreak Enhances Consumption and Immune Response of an Eruptive Folivore

Changes in the chemical composition of plant defense compounds during herbivory can impact herbivore resource allocation patterns and thereby herbivore survival, growth, and immune response against endoparasitoid infection. Few studies have investigated folivore responses to changes in plant chemistry that occur under outbreak conditions in mature conifer systems. Using data from an earlier observational field study, we carried out laboratory bioassays to test how variation in monoterpenes in piñon pine trees (Pinus edulis, Pinaceae) during an outbreak affects growth, consumption, and immune response of a specialist herbivore, the Southwestern tiger moth (Lophocampa ingens, Arctiidae). Larvae were fed on artificial diets containing four monoterpenes at concentrations that mimicked those observed in undamaged and herbivore-damaged trees in situ during an outbreak. Damaged trees contained 30% lower total monoterpene concentrations, likely reflecting volatile losses as observed in a previous field study Trowbridge et al. (Ecology 95:1591–1603, Trowbridge et al. 2014). Herbivores reared on diets mimicking terpene concentrations in the needles of damaged trees exhibited an approximately 60% increase in consumption relative to larvae reared on diets characteristic of trees without herbivore damage. Higher consumption was accompanied by a 40% increase in immune response with no change in growth rate. These observations suggest preferential resource allocation towards immunity and/or a strong genetic component that determines growth under these conditions. These outcomes, which favor the herbivore, point to: (i) a potential positive feedback mechanism that may increase L. ingens’s chance of escaping parasitism during the early phases of an outbreak; and (ii) the important role of monoterpenes in mediating conifer-folivore interactions specifically for P. edulis, which has suffered large-scale drought-induced mortality events exacerbated by the presence of insects.

Home on the (expanding) range: evaluating the effectiveness of a novel host's induced defenses against the mountain pine beetle-fungal complex.

The mountain pine beetle (MPB; Dendroctonus ponderosae) is one of the most destructive forest pests, responsible for the death of billions of coniferous trees from Mexico to Alaska (Bentz et al. 2009). Behavioral plasticity helps the beetle sustain endemic levels until the right conditions are met, thus releasing constraints on population growth and resulting in a population eruption (Raffa et al. 2008). These large-scale outbreak events have resulted in significant impacts on ecosystem function and negative effects on local and regional economies (Ayres and Lombardero 2000, Kurz et al. 2008, Edburg et al. 2012). While the mechanisms contributing to bark beetle outbreaks are complex (Raffa et al. 2008, Bleiker et al. 2014), predicted increases in mean annual global temperatures will influence insect population success and expansion both directly via changes in development (Parmesan 2006, Jamieson et al. 2012) and indirectly via altered host defenses (Lusebrink et al. 2016, Erbilgin et al. 2017, Jamieson et al. 2017). The role that plant secondary compounds play during an insect host expansion, however, is unclear, especially for insects that rely on associated symbionts, as is the case for the MPB and its associated blue stain fungi. Phloem-feeding bark beetles are intimately linked to the defensive chemicals of their hosts, particularly monoterpenes (C10). Monoterpenes play a critical role in beetle behavior, physiology, reproduction and survival by serving as precursors to aggregation pheromones, synergists of pheromones, as well as lethal defenses depending on the composition and vapor concentrations (Seybold et al. 2006). During outbreaks, MPB attack en masse to surpass both physical and constitutive chemical defenses of healthy well-defended trees, as well as the induced changes in the quantity and quality of a host’s terpene and phenolic chemistry (Franceschi et al. 2005). This means that a rapid induced chemical response can mean life or death for both the tree and MPB (Raffa et al. 2008, Boone et al. 2011, KeefoverRing et al. 2016). Thus, understanding how MPB attack induces changes in defensive chemistry provides important insights into successful beetle colonization and the propagation of mass attacks (Raffa et al. 2005). Just as individual monoterpenes can have varying effects on MPB, they can also differentially affect the fungal symbionts of MPB. Some host monoterpenes can impede the growth of fungi, which MPB relies on for nutrition, development and survival (Bleiker and Six 2007). Fungi not only provide a nutrient rich food source for bark beetles (Bentz and Six 2006, Adams and Six 2007, Bleiker and Six 2007, Cook et al. 2010, Goodsman et al. 2012), but can aid in overcoming tree defense (Klepzig and Six 2004, Hammerbacher et al. 2013) and metabolizing toxic monoterpenes (Wang et al. 2013, 2014). While the failure of the fungi would result in the demise of the beetle, the effect of rapidly induced monoterpene production on fungal function during colonization of novel hosts and its effect on the success and spread of the MPB into new habitats remains to be elucidated. In Canada, the MPB has expanded its range from lodgepoledominated forests through a lodgepole-jack pine (Pinus banksiana Lambert) hybrid zone into jack pine forests (Cullingham et al. 2011). The ecological and economical impacts of this range expansion have the potential to be disastrous (Ono 2003).

RELATIONSHIP BETWEEN CANOPY TURBULENCE AND VERTICAL DISTRIBUTION OF REACTIVE GASES IN THE CENTRAL AMAZON RAINFOREST

Ozone plays a crucial role in the chemistry of the tropical atmospheric boundary layer. In the rainforest, ozone sources and sinks are complex due to numerous chemical reactions and surface deposition. Turbulent transport controls the vertical distribution of ozone. A field study in the Amazonia, near Manaus, Brazil during 2014 shows different shapes of ozone profiles as a response to changes in air turbulence during night-to-day and day-to-night transitions. During the night-to-day transition following sunrise ozone levels increase within the canopy due to photochemical production and increased vertical mixing. The vertical transport of ozone to the lower layers of the canopy is enhanced after the thermal inversion in the canopy disappears. At night, the ozone deposition to the ground and the foliage in the lower canopy is strong. After midnight, the lower canopy is devoid of ozone. Relatively high gradients of ozone levels within the forest during the nighttime also result from the decoupling between the in- and above-canopy environment that limits the forest-atmosphere ozone exchange. Processes responsible for the vertical distribution ozone are necessary to estimate the oxidation of the plant-emitted gases whose reaction products are aerosol precursors.