Episodic defoliation rapidly reduces starch but not soluble sugars in an invasive shrub, Tamarix spp.

PREMISE: Plants rely on pools of internal nonstructural carbohydrates (NSCs: soluble sugars plus starch) to support metabolism, growth, and regrowth of tissues damaged from disturbance such as foliage herbivory. However, impacts of foliage herbivory on the quantity and composition of NSC pools in long-lived woody plants are currently unclear. We implemented a controlled defoliation experiment on mature Tamarix spp.-a dominant riparian woody shrub/tree that has evolved with intense herbivory pressure-to test two interrelated hypotheses: (1) Repeated defoliation disproportionately impacts aboveground versus belowground NSC storage. (2) Defoliation disproportionately impacts starch versus soluble sugar storage. METHODS: Hypotheses were tested by transplanting six Tamarix seedlings into each of eight cylinder mesocosms (2 m diameter, 1 m in depth). After 2.5 years, plants in four of the eight mesocosms were mechanically defoliated repeatedly over a single growing season, and all plants were harvested in the following spring. RESULTS: Defoliation had no impact on either above- or belowground soluble sugar pools. However, starch in defoliated plants dropped to 55% and 26% in stems and roots, respectively, relative to control plants, resulting in an over 2-fold higher soluble sugar to starch ratio in defoliated plants. CONCLUSIONS: The results suggest that defoliation occurring over a single growing season does not impact immediate plant functions such as osmoregulation, but depleted starch could limit future fitness, particularly where defoliation occurs over multiple years. These results improve our understanding of how woody plants cope with episodic defoliation caused by foliage herbivory and other disturbances.

Establishing Diorhabda carinulata: Impact of Release Disturbances on Pheromone Emission and Influence of Pheromone Lures on Establishment.

Before weed biocontrol insects are transported and released in a new area, they are commonly collected into small paper containers, chilled, and kept under dark conditions. This process can be termed a pre-release protocol. The influence of a pre-release protocol on establishment success of a gregarious biological control agent was assessed using the northern tamarisk beetle, Diorhabda carinulata (Desbrochers), and its exotic, invasive host plant saltcedar (Tamarix spp.). Pre-release protocol impacts on aggregation pheromone production by D. carinulata were characterized under controlled conditions. Additional experiments were undertaken to determine if deployment of aggregation pheromone lures might enhance the agent's persistence at release sites. Adults that experienced the pre-release protocol produced less aggregation pheromone compared to undisturbed adults. Olfactometer bioassays indicated that a cohort of adults subjected to the pre-release protocol were less attractive to other adults than a control cohort. Efficacy of aggregation pheromone-based lures to retain adults at release sites was evaluated by comparing capture numbers of adult beetles at paired treatment and control release sites, 10-14 days after the release of 300, 500, or 1000 individuals. A greater number of adult D. carinulata were captured where the pheromone lures had been deployed compared to control release sites. Application of aggregation pheromone when a new release of D. carinulata is planned should allow biological control practitioners to increase retention of beetles at a release site.

Early impacts of biological control on canopy cover and water use of the invasive saltcedar tree (Tamarix spp.) in western Nevada, USA.

The success of biological control programs is rarely assessed beyond population level impacts on the target organism. The question of whether a biological control agent can either partially or completely restore ecosystem services independent of population level control is therefore still open to discussion. Using observational and experimental approaches, we investigated the ability of the saltcedar leaf beetle [Diorhabda carinulata (Brullé) (Coleoptera: Chrysomelidae)] to reduce the water use of saltcedar trees (Tamarix ramosissima Ledeb.) in two sites (Humboldt and Walker Rivers) in Nevada, USA. At these sites D. carinulata defoliated the majority of trees within 25 and 9 km, respectively, of the release location within 3 years. At the Humboldt site, D. carinulata reduced the canopy cover of trees adjacent to the release location by >90%. At a location 4 km away during the first year of defoliation, D. carinulata reduced peak (August) stem water use by 50-70% and stand transpiration (July to late September) by 75% (P = 0.052). There was, however, no reduction in stem water use and stand transpiration during the second year of defoliation due to reduced beetle abundances at that location. At the Walker site, we measured stand evapotranspiration (ET) in the center of a large saltcedar stand and found that ET was highest immediately prior to D. carinulata arrival, dropped dramatically with defoliation, and remained low through the subsequent 2 years of the study. In contrast, near the perimeter of the stand, D. carinulata did not reduce sap flow, partly because of low rates of defoliation but also because of increased water use per unit leaf area in response to defoliation. Taken together, our results provide evidence that in the early stages of population expansion D. carinulata can lead to substantial declines in saltcedar water use. The extent of these declines varies spatially and temporally and is dependent on saltcedar compensatory responses along with D. carinulata population dynamics and patterns of dispersal.

Using Chemical Ecology to Enhance Weed Biological Control.

In agricultural systems, chemical ecology and the use of semiochemicals have become critical components of integrated pest management. The categories of semiochemicals that have been used include sex pheromones, aggregation pheromones, and plant volatile compounds used as attractants as well as repellents. In contrast, semiochemicals are rarely utilized for management of insects used in weed biological control. Here, we advocate for the benefit of chemical ecology principles in the implementation of weed biocontrol by describing successful utilization of semiochemicals for release, monitoring and manipulation of weed biocontrol agent populations. The potential for more widespread adoption and successful implementation of semiochemicals justifies multidisciplinary collaborations and increased research on how semiochemicals and chemical ecology can enhance weed biocontrol programs.

An Herbivore-Induced Plant Volatile From Saltcedar (Tamarix spp.) Is Repellent to Diorhabda carinulata (Coleoptera: Chrysomelidae).

The leaf beetle Diorhabda carinulata Desbrochers (Coleoptera: Chrysomelidae) was introduced into the United States in 1999 for classical biological control of the exotic woody invader saltcedar (Tamarix spp. L. [Caryophyllales: Tamaricaceae]). The recent southern expansion of the range of D. carinulata in the United States has precipitated conflict between proponents of biological control of Tamarix and those with concerns over habitat conservation for avian species. Several semiochemicals that mediate aggregations by this species have been reported, but no repellent compounds have been recorded thus far. We now report a repellent compound, 4-oxo-(E)-2-hexenal, induced by adult D. carinulata feeding on saltcedar foliage. Collection of headspace volatiles, gas chromatography mass spectrometry, and electroantennographic analyses identified 4-oxo-(E)-2-hexenal as an insect-induced compound that is antennally active. Behavioral and exposure assays were conducted to test for repellency and toxicity in adults and larvae. Headspace volatiles were also collected from adult males exposed to 4-oxo-(E)-2-hexenal to determine the impact exposure might have on the emission of the aggregation pheromone. 4-Oxo-(E)-2-hexenal elicited electrophysiological responses in adults of both sexes. Behavioral responses indicated repellency across multiple doses for reproductive D. carinulata adults but not in nonreproductive adults. Exposure assays indicated altered behaviors in first instar larvae and adults, but not in third instar larvae. Collection of headspace volatiles indicated that exposure to 4-oxo-(E)-2-hexenal did not alter emission of the D. carinulata aggregation pheromone by adult males. The continued development and field deployment of this repellent compound may provide a new tool for the management of D. carinulata.

Field demonstration of a semiochemical treatment that enhances Diorhabda carinulata biological control of Tamarix spp.

The northern tamarisk beetle Diorhabda carinulata (Desbrochers) was approved for release in the United States for classical biological control of a complex of invasive saltcedar species and their hybrids (Tamarix spp.). An aggregation pheromone used by D. carinulata to locate conspecifics is fundamental to colonization and reproductive success. A specialized matrix formulated for controlled release of this aggregation pheromone was developed as a lure to manipulate adult densities in the field. One application of the lure at onset of adult emergence for each generation provided long term attraction and retention of D. carinulata adults on treated Tamarix spp. plants. Treated plants exhibited greater levels of defoliation, dieback and canopy reduction. Application of a single, well-timed aggregation pheromone treatment per generation increased the efficacy of this classical weed biological control agent.

Invasive African clawed frogs in California: A reservoir for or predator against the chytrid fungus?

Amphibian species are experiencing population declines due to infection by the fungal pathogen, Batrachochytrium dendrobatidis (Bd). The African clawed frog (Xenopus laevis), an asymptomatic carrier of Bd, has been implicated in the spread of this pathogen through global trade and established invasive populations on several continents. However, research has not explored the relationships of both life stages of this amphibian with Bd. While the post-metamorphic individuals may act as a reservoir, spreading the infection to susceptible species, the filter-feeding larvae may consume the motile Bd zoospores from the water column, potentially reducing pathogen abundance and thus the likelihood of infection. We explore these contrasting processes by assessing Bd prevalence and infection intensities in field populations of post-metamorphic individuals, and performing laboratory experiments to determine if larval X. laevis preyed upon Bd zoospores. The water flea, Daphnia magna, was included in the Bd consumption trials to compare consumption rates and to explore whether intraguild predation between the larval X. laevis and Daphnia may occur, potentially interfering with control of Bd zoospores by Daphnia. Field surveys of three X. laevis populations in southern California, in which 70 post-metamorphic individuals were tested for Bd, found 10% infection prevalence. All infected individuals had very low infection loads (all Bd loads were below 5 zoospore equivalents). Laboratory experiments found that larval X. laevis consume Bd zoospores and therefore may reduce Bd abundance and transmission between amphibians. However, metamorphic and juvenile X. laevis exhibited intraguild predation by consuming Daphnia, which also prey upon Bd zoospores. The results suggest that X laevis is not a large reservoir for Bd and its larval stage may offer some reduction of Bd transmission through direct predation.

Semiochemicals to enhance herbivory by Diorhabda carinulata aggregations in saltcedar (Tamarix spp.) infestations.

BACKGROUND: Semiochemicals for monitoring, attracting or repelling pest and beneficial organisms are increasingly deployed in agricultural and forest systems for pest management. However, the use of aggregation pheromones and host-plant attractants for the express purpose of increasing the efficacy of classical biological control agents of weeds has not been widely reported. Therefore, we conducted field-based assays to determine if a specialized wax-based matrix impregnated with an aggregation pheromone of the northern tamarisk beetle Diorhabda carinulata (Desbrochers) or host-plant volatiles could increase the efficacy of D. carinulata. RESULTS: The aggregation pheromone and host-plant volatiles were formulated for field application using a wax-based matrix. Reported release rates suggest that this matrix is a viable formulation for enhancing D. carinulata aggregations under field conditions. Pheromone-treated saltcedar plants (Tamarix spp.) not only had higher densities of adult and larval D. carinulata, but also sustained greater levels of foliar damage than control plants. Increased damage from the focused feeding of D. carinulata caused an increase in foliar dieback and decrease in live canopy volume of semiochemical-treated plants. CONCLUSION: Field deployment of these semiochemical formulations could be useful in directing populations of D. carinulata for increased impact on Tamarix spp. © 2018 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Seasonal timing of diapause induction limits the effective range of Diorhabda elongata deserticola (Coleoptera: Chrysomelidae) as a biological control agent for tamarisk (Tamarix spp.).

The leaf beetle Diorhabda elongata Brullé subspecies deserticola Chen, collected in northwestern China, has been released in the western United States to control tamarisk (Tamarix spp.). While beetle establishment and saltcedar defoliation have been noted at northern study sites, this species has not established at latitudes south of the 38th parallel. Critical daylength for diapause induction was measured in the laboratory and ranged between 14 h 50 min to 15 h 08 min, depending on temperature, and adults were shown to cease reproduction and enter diapause at daylengths of 14 h 30 min or less. Critical daylength in the field was measured at approximately 14 h 39 min and occurred 13 d before 50% of the population reached diapause. South of 36 degrees 20' N, the longest days of the year are shorter than 14 h 39 min, making the beetles univoltine in the southern United States. North of 36 degrees 20' N, a window of reproductive activity opens 13 d after the critical daylength is reached in the spring and closes 13 d after it is passed in the summer, allowing at least a partial second summer generation. It is predicted that south of the 38th parallel, premature diapause will increase mortality and disrupt synchrony between the life cycle of the beetle and host plant availability. This could hinder establishment and help explain the failure of this population south of the 38th parallel, providing a rationale for testing other populations of D. elongata in the southern range of Tamarix in North America.

Can local adaptation explain varying patterns of herbivory tolerance in a recently introduced woody plant in North America?

Patterns of woody-plant mortality have been linked to global-scale environmental changes, such as extreme drought, heat stress, more frequent and intense fires, and episodic outbreaks of insects and pathogens. Although many studies have focussed on survival and mortality in response to specific physiological stresses, little attention has been paid to the role of genetic heritability of traits and local adaptation in influencing patterns of plant mortality, especially in non-native species. Tamarix spp. is a dominant, non-native riparian tree in western North America that is experiencing dieback in some areas of its range due to episodic herbivory by the recently introduced northern tamarisk leaf beetle (Diorhabda carinulata). We propose that genotype × environment interactions largely underpin current and future patterns of Tamarix mortality. We anticipate that (i) despite its recent introduction, and the potential for significant gene flow, Tamarix in western North America is generally adapted to local environmental conditions across its current range in part due to hybridization of two species; (ii) local adaptation to specific climate, soil and resource availability will yield predictable responses to episodic herbivory; and (iii) the ability to cope with a combination of episodic herbivory and increased aridity associated with climate change will be largely based on functional tradeoffs in resource allocation. This review focusses on the potential heritability of plant carbon allocation patterns in Tamarix, focussing on the relative contribution of acquired carbon to non-structural carbohydrate (NSC) pools versus other sinks as the basis for surviving episodic disturbance. Where high aridity and/or poor edaphic position lead to chronic stress, NSC pools may fall below a minimum threshold because of an imbalance between the supply of carbon and its demand by various sinks. Identifying patterns of local adaptation of traits related to resource allocation will improve forecasting of Tamarix population susceptibility to episodic herbivory.

Species Introductions and Their Cascading Impacts on Biotic Interactions in desert riparian ecosystems.

Desert riparian ecosystems of North America are hotspots of biodiversity that support many sensitive species, and are in a region experiencing some of the highest rates of climatic alteration in North America. Fremont cottonwood, Populus fremontii, is a foundation tree species of this critical habitat, but it is threatened by global warming and regional drying, and by a non-native tree/shrub, Tamarix spp., all of which can disrupt the mutualism between P. fremontii and its beneficial mycorrhizal fungal communities. Specialist herbivorous leaf beetles (Diorhabda spp.) introduced for biocontrol of Tamarix are altering the relationship between this shrub and its environment. Repeated episodic feeding on Tamarix foliage by Diorhabda results in varying rates of dieback and mortality, depending on genetic variation in allocation of resources, growing conditions, and phenological synchrony between herbivore and host plant. In this article, we review the complex interaction between climatic change and species introductions and their combined impacts on P. fremontii and their associated communities. We anticipate that (1) certain genotypes of P. fremontii will respond more favorably to the presence of Tamarix and to climatic change due to varying selection pressures to cope with competition and stress; (2) the ongoing evolution of Diorhabda's life cycle timing will continue to facilitate its expansion in North America, and will over time enhance herbivore impact to Tamarix; (3) defoliation by Diorhabda will reduce the negative impact of Tamarix on P. fremontii associations with mycorrhizal fungi; and (4) spatial variability in climate and climatic change will modify the capacity for Tamarix to survive episodic defoliation by Diorhabda, thereby altering the relationship between Tamarix and P. fremontii, and its associated mycorrhizal fungal communities. Given the complex biotic/abiotic interactions outlined in this review, conservation biologists and riparian ecosystem managers should strive to identify and conserve the phenotypic traits that underpin tolerance and resistance to stressors such as climate change and species invasion. Such efforts will greatly enhance conservation restoration efficacy for protecting P. fremontii forests and their associated communities.

Life history characteristics of diorhabda carinulata under various temperatures.

Tamarisk leaf beetles, Diorhabda spp., have been released in the western United States as a biological control agent for the invasive weed Tamarix spp. There have been a few studies on the life cycle, host preferences, and field observations of Diorhabda; however, their ecophysiological characteristics under various temperature regimes are not clearly understood. In this study, life history characteristics such as growth, fecundity, and mortality of Diorhabda Carinulata (Desbrochers), the species established in the Colorado River basin, were investigated under various temperatures. Beetles were housed at various temperatures (room, constant high, and variable high) and their life cycle from eggs to reproductive adult was observed. Body size at various larval and adult stages, as well as their developmental time decreased with increasing temperature. Between the two temperature treatments, beetles at diurnally fluctuating temperature (variable high treatment) grew slower and produced fewer eggs per clutch when compared with the constant high treatment. Despite smaller in size, beetles grew fastest at the constant high temperature and produced most eggs per clutch compared with the other two treatments. Overall, severely high temperatures seem to have a debilitating effect on Diorhabda at early larval stages with nearly 50% mortality. The study has potential implications for the tamarisk beetle biocontrol program in the southwestern United States.

Evolution of critical day length for diapause induction enables range expansion of Diorhabda carinulata, a biological control agent against tamarisk (Tamarix spp.).

In classical weed biological control, small collections of arthropods are made from one or a few sites in the native range of the target plant and are introduced to suppress the plant where it has become invasive, often across a wide geographic range. Ecological mismatches in the new range are likely, and success using the biocontrol agent may depend on postrelease evolution of beneficial life history traits. In this study, we measure the evolution of critical day length for diapause induction (day length at which 50% of the population enters dormancy), in a beetle (Diorhabda carinulata) introduced into North America from China to control an exotic shrub, Tamarix spp. Beetle populations were sampled from four sites in North America 7 years after introduction, and critical day length was shown to have declined, forming a cline over a latitudinal gradient At one field site, decreased critical day length was correlated with 16 additional days of reproductive activity, resulting in a closer match between beetle life history and the phenology of Tamarix. These findings indicate an enhanced efficacy and an increasingly wider range for D. carinulata in Tamarix control.

Seasonal adaptations to day length in ecotypes of Diorhabda spp. (Coleoptera: Chrysomelidae) inform selection of agents against saltcedars (Tamarix spp.).

Seasonal adaptations to daylength often limit the effective range of insects used in biological control of weeds. The leaf beetle Diorhabda carinulata (Desbrochers) was introduced into North America from Fukang, China (latitude 44° N) to control saltcedars (Tamarix spp.), but failed to establish south of 38° N latitude because of a mismatched critical daylength response for diapause induction. The daylength response caused beetles to enter diapause too early in the season to survive the duration of winter at southern latitudes. Using climate chambers, we characterized the critical daylength response for diapause induction (CDL) in three ecotypes of Diorhabda beetles originating from 36, 38, and 43° N latitudes in Eurasia. In a field experiment, the timing of reproductive diapause and voltinism were compared among ecotypes by rearing the insects on plants in the field. CDL declined with latitude of origin among Diorhabda ecotypes. Moreover, CDL in southern (<39° N latitude) ecotypes was shortened by more than an hour when the insects were reared under a fluctuating 35-15°C thermoperiod than at a constant 25°C. In the northern (>42° N latitude) ecotypes, however, CDL was relatively insensitive to temperature. The southern ecotypes produced up to four generations when reared on plants in the field at sites south of 38° N, whereas northern ecotypes produced only one or two generations. The study reveals latitudinal variation in how Diorhabda ecotypes respond to daylength for diapause induction and how these responses affect insect voltinism across the introduced range.

Control of Tamarix in the Western United States: implications for water salvage, wildlife use, and riparian restoration.

Non-native shrub species in the genus Tamarix (saltcedar, tamarisk) have colonized hundreds of thousands of hectares of floodplains, reservoir margins, and other wetlands in western North America. Many resource managers seek to reduce saltcedar abundance and control its spread to increase the flow of water in streams that might otherwise be lost to evapotranspiration, to restore native riparian (streamside) vegetation, and to improve wildlife habitat. However, increased water yield might not always occur and has been substantially lower than expected in water salvage experiments, the potential for successful revegetation is variable, and not all wildlife taxa clearly prefer native plant habitats over saltcedar. As a result, there is considerable debate surrounding saltcedar control efforts. We review the literature on saltcedar control, water use, wildlife use, and riparian restoration to provide resource managers, researchers, and policy-makers with a balanced summary of the state of the science. To best ensure that the desired outcomes of removal programs are met, scientists and resource managers should use existing information and methodologies to carefully select and prioritize sites for removal, apply the most appropriate and cost-effective control methods, and then rigorously monitor control efficacy, revegetation success, water yield changes, and wildlife use.