Recovery of A Native Tree Following Removal of An Invasive Competitor In The Context of Potential Endangered Bird Habitat

Invasive species removal is a common focus in restoration ecology, but the ultimate goal of native plant species recovery and habitat recovery is often elusive. Control of invasive Tamarix spp. shrubs in the American Southwest has only sometimes led to increased native species cover; this is of particular concern for the protection of the endangered Southwestern willow flycatcher (Empidonax extimus trailii, abbr. SWFL) that nests readily in Tamarix when native Salix canopy is absent. If we can identify the conditions that lead to more native trees as well as habitat protection for the SWFL, we can prioritize restoration efforts more effectively and reduce conflict between conservation goals. To determine whether reduction in the invasive Tamarix led to more Salix cover (and thus no net loss in SWFL habitat), we compiled data on vegetation, soils, and geographic conditions in 260 sites where Tamarix had been subject to control efforts and 132 positive and negative reference sites. We found that (1) reduction in Tamarix only increased Salix cover in wetter sites, and was greater when a particular, low-disturbance removal method was used; however the increase did not typically compensate for the overall losses in canopy cover, and (2) Salix cover was generally highest in locations with low drought stress, as reflected by soil properties, distance to water, and climate. These results suggest that the presence and recovery of Salix is dependent on its relatively narrow environmental niche, in contrast with Tamarix’s broader one. Thus, although abundance of Salix and Tamarix was negatively correlated, this is likely because of Salix’s different niche, as much as or more than direct interspecific competition. Our findings demonstrate that removal of an invasive species does not necessarily lead to reestablishment of the native species they appeared to displace. We suggest that in the case of promoting habitat for SWFL and other birds, outcomes of restoration activity can be improved by focusing Tamarix removal efforts on sites more likely to promote Salix growth based on environmental characteristics.

Hybridization and range expansion in tamarisk beetles (Diorhabda spp.) introduced to North America for classical biological control

With the global rise of human-mediated translocations and invasions, it is critical to understand the genomic consequences of hybridization and mechanisms of range expansion. Conventional wisdom is that high genetic drift and loss of genetic diversity due to repeated founder effects will constrain introduced species. However, reduced genetic variation can be countered by behavioral aspects and admixture with other distinct populations. As planned invasions, classical biological control (biocontrol) agents present important opportunities to understand the mechanisms of establishment and spread in a novel environment. The ability of biocontrol agents to spread and adapt, and their effects on local ecosystems, depends on genomic variation and the consequences of admixture in novel environments. Here we use a biocontrol system to examine the genome-wide outcomes of introduction, spread, and hybridization in four cryptic species of a biocontrol agent, the tamarisk beetle (Diorhabda carinata, D. carinulata, D. elongata, and D. sublineata), introduced from six localities across Eurasia to control the invasive shrub tamarisk (Tamarix spp.) in western North America. We assembled a de novo draft reference genome and applied RADseq to over 500 individuals from laboratory cultures, the native ranges, and across the introduced range. Despite evidence of a substantial genetic bottleneck among D. carinulata in N. America, populations continue to establish and spread, possibly due to aggregation behavior. We found that D. carinata, D. elongata, and D. sublineata hybridize in the field to varying extents, with D. carinata x D. sublineata hybrids being the most abundant. Genetic diversity was greater at sites with hybrids, highlighting potential for increased ability to adapt and expand. Our results demonstrate the complex patterns of genomic variation that can result from introduction of multiple ecotypes or species for biocontrol, and the importance of understanding them to predict and manage the effects of biocontrol agents in novel ecosystems.

Monitoring Tamarix Changes Using WorldView-2 Satellite Imagery in Grand Canyon National Park, Arizona

Remote sensing methods are commonly used to monitor the invasive riparian shrub tamarisk (Tamarix spp.) and its response to the northern tamarisk beetle (D. carinulata), a specialized herbivore introduced as a biocontrol agent to control tamarisk in the Southwest USA in 2001. We use a Spectral Angle Mapper (SAM) supervised classification method with WorldView-2 (2 m spatial resolution) multispectral images from May and August of 2019 to map healthy tamarisk, canopy dieback, and defoliated tamarisk over a 48 km segment of the Colorado River in the topographically complex Grand Canyon National Park, where coarse-resolution satellite images are of limited use. The classifications in May and August produced overall accuracies of 80.0% and 83.1%, respectively. Seasonal change detection between May and August 2019 indicated that 47.5% of the healthy tamarisk detected in May 2019 had been defoliated by August 2019 within the WorldView-2 image extent. When compared to a previously published tamarisk map from 2009, derived from multispectral aerial imagery, we found that 29.5% of healthy tamarisk canopy declined between 2009 and 2019. This implies that tamarisk beetle impacts are continuing to accumulate even though land managers have noted the presence of the beetles in this reach of the river for 7 years since 2012.

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.

Invasive Saltcedar and Drought Impact Ant Communities and Isopods in South-Central Nebraska

The establishment and spread of non-native species often results in negative impacts on biodiversity and ecosystem function. Several species of saltcedar, Tamarix spp. L., have been recently naturalized in large portions of the United States where they have altered plant and animal communities. To test the prediction that saltcedar negatively affects invertebrates, we measured ant genera diversity and the activity density of the exotic isopod Armadillidium vulgare Latrielle (Isopoda: Oniscoidea) for 2 yr using pitfall traps located within 30 5-m2 plots with or without saltcedar at a south-central Nebraska reservoir. From 2005 to 2006, we collected 10,837 ants representing 17 genera and 4,953 A. vulgare. Per plot, the average number of ant genera was not different between saltcedar (x̅ = 3.9) and non-saltcedar areas ( x̅ = 3.9); however, saltcedar plots were compositionally different and more similar from plot to plot (i.e., they had lower beta diversity than control plots) in 2005, but not in 2006. Isopods were likewise temporally affected with higher activity density (+89%) in control plots in 2005, but higher activity density (+27%) in saltcedar plots in 2006. The observed temporal differences occurred as the drought that initially enabled the saltcedar invasion became less severe in 2006. Combined, our results suggest that invertebrate groups like ants, which are generally omnivorous, may be better equipped than more specialized taxa like detritivores to withstand habitat changes due to invasions by non-native species, especially during extreme weather events such as prolonged droughts.

Water Deficit Transcriptomic Responses Differ in the Invasive Tamarix chinensis and T. ramosissima Established in the Southern and Northern United States

Tamarix spp. (saltcedar) were introduced from Asia to the southern United States as windbreak and ornamental plants and have spread into natural areas. This study determined differential gene expression responses to water deficit (WD) in seedlings of T. chinensis and T. ramosissima from established invasive stands in New Mexico and Montana, respectively. A reference de novo transcriptome was developed using RNA sequences from WD and well-watered samples. Blast2GO analysis of the resulting 271,872 transcripts yielded 89,389 homologs. The reference Tamarix (Tamaricaceae, Carophyllales order) transcriptome showed homology with 14,247 predicted genes of the Beta vulgaris subsp. vulgaris (Amaranthaceae, Carophyllales order) genome assembly. T. ramosissima took longer to show water stress symptoms than T. chinensis. There were 2068 and 669 differentially expressed genes (DEG) in T. chinensis and T. ramosissima, respectively; 332 were DEG in common between the two species. Network analysis showed large biological process networks of similar gene content for each of the species under water deficit. Two distinct molecular function gene ontology networks (binding and transcription factor-related) encompassing multiple up-regulated transcription factors (MYB, NAC, and WRKY) and a cellular components network containing many down-regulated photosynthesis-related genes were identified in T. chinensis, in contrast to one small molecular function network in T. ramosissima.