A Tale of Three Species

Invasive species control and endangered species management in the Southwestern US.

Saltcedar, leaf and the Southwestern willow flycatcher

Erik Grijalva

March 11, 2015

Word cloud generated from abstracts from papers used in research for this paper

Abstract

Non-native Tamarix species were introduced into North America in the early 1800’s and by the mid-1900’s had expanded to cover over 0.6 million ha. Tamarix became a leading factor in the transformation of riparian corridors where it readily outcompetes natives, especially in the American Southwest. Species that relied on these corridors were either displaced or extirpated, leading to significant conservation efforts to restore or maintain native diversity. Chief among these species is the Southwestern willow flycatcher, a bird species which was heavily impacted by the changes to riparian habitats throughout its range. In the 1990’s, conservationists targeted the Tamarix infestation with an introduced biocontrol agent, the saltcedar leaf , which can defoliate large stands of Tamarix once established. Though originally released at sites distant from known locations of the flycatcher, the beetles have expanded their range to overlap with that of the endangered bird. Beetle release was curtailed in 2010 out of concern that defoliation of Tamarix stands presented an unacceptable risk to the population of flycatchers by exposing nests in Tamarix to increased predation and nestling heat stress. Despite this, the beetle population continues to expand its range. Conservationists are now integrating new understanding of the ecological role of Tamarix and the presence of the beetle into restoration strategies for the flycatcher and other native species.

Introduction The modern practices of conservation and habitat management is a no less complicated endeavor than the ecological systems that are the focus of the discipline. Conservationists are called upon to steward remnant threads of historic ecosystems while dealing with seemingly ubiquitous anthropogenic alterations to those same systems. These disturbances can be physical, as is the case with developments, grazing or water diversions, or they can be biological as is the case with invasive species, disrupted trophic structures, endangered species or severely modified habitats. Often land-managers are confronted with a toxic brew of many or all of these factors simultaneously. Such is the case in the Southwestern United States, where the introduction in the mid- 1800’s of several species of plants in the genus Tamarix (or saltcedar) coincided with radical changes to land-use, including increased grazing pressures on low-productivity rangelands and large-scale hydrologic changes from dam-building. More than 100 years later, saltcedar had established a vast and permanent presence over much of the southern portion of North America. Modifications to this arid environment had only increased in the intervening years, resulting in many native plant and species declines, including the Southwestern willow flycatcher (Empidonax traillii extimus, hereinafter SWWF). In the case of the SWWF, its native riparian habitat was hit hard by land modifications and it was also negatively impacted by saltcedar invasion in the same habitats. While some land managers sought to manage the rampant expansion and habitat degradation caused by the saltcedar, other conservationists sought to preserve the remaining SWWF populations. Although these goals seem to be in concert, the small amounts of intact riparian habitat that remained were too few to support the

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SWWF. Control efforts targeted at saltcedar, especially the introduction of the saltcedar leaf beetle, wound up degrading the only suitable habitat remaining to the imperiled SWWF. This paper examines the confluence of saltcedar, SWWF and the saltcedar leaf beetle in the context of conservation goals in the Southwest.

Tamarix Saltcedar (or Tamarisk) is the common name for a group of five shrubby tree species with grey-green leaves in the genus Tamarix, native to the Mediterranean and Eurasia. Several species were introduced into North America in 1823 by nurserymen, and it was through the horticultural trade and the US Department of Agriculture that saltcedar was propagated and distributed throughout the continent. Saltcedar was planted in undeveloped areas to provide windbreaks, shade or erosion control, and was used as an ornamental plant in urban developments. The particular life history and ecological characteristics of saltcedar have allowed the plants to spread to vast areas of largely arid habitats in the Southwestern US and elsewhere, especially in valuable riparian habitats. A summary of these characteristics is discussed in the following sections. Biology Saltcedar plants are phreatophytes, meaning that they use deep, penetrating root systems to access the water table. They typically rely on groundwater for survival, but can persist in areas without a reachable water table if periodically inundated or after establishment in previously wet conditions. Estimates of the lifespan of an individual saltcedar tree are on the order of 75 to 100 yr. Young plants can flower in the first year, producing numerous small white or pink flowers, and a mature plant can produce up to a million individual seeds in a single season. The small (~1 mm), light seeds are produced in a capsule, and are equipped with a pappus-like tuft of hair enabling wind and water dispersal. They require no dormancy period, though they do need moist soil for germination, and once sprouted can grow at rates of up to 4 m in a single growing season (Di Tomaso 1998). Interestingly, saltcedar seeds do not last long. Estimates of viability range from 3-40 weeks under typical conditions. However, they do have high initial viability, on the order of 95%, even germinating while still floating on water. Nevertheless, they are highly sensitive to competition at the seedling stage, and require open, sunny locations for survival. Once established the root system enables strong competition with other plants through extensive, branching networks of roots that can extend as deep as 50 m. Plants can re-sprout from roots, and above-ground stems can form adventitious roots to further vegetatively establish saltcedar stands. A mature plant can weather significant physical and environmental stresses, including burning, cutting, drought or flooding (Di Tomaso 1998). Ecology Saltcedar is capable of growing in a wide array of habitats, but is found at elevations no higher than 2,100 m. It prefers soils with significant organic matter with a high water table, and can tolerate high salinity (650 to 36,000 ppm). Dense stands shade or crowd out other species, forming dense, impenetrable monocultures. One of the more studied aspects of saltcedar ecology is the genus’ use of water and evapotranspiration rates. Saltcedar has been implicated

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in lowering water tables and completely drying up ponds, streams and other water sources across the arid Southwest. Indeed, evapotranspiration rates of saltcedar are among the highest found for phreatophytes in the Southwest, and that includes native riparian trees. However, the effect of evapotranspiration in saltcedar-implicated water drawdowns is case-specific, with dense stands having greater effect. When compared one-to-one with individual phreatophyte plants like willow, cottonwood and mesquite, saltcedar shows similar transpiration rates. Saltcedar outperforms these native plants by virtue of the total leaf area of equally-sized stands, with its numerous, small leaves creating a larger surface area for vapor exchange. It is also suggested that the ability of saltcedar to excrete salts contributes to a greater evapotranspiration potential that enables more water movement from the soil. Another key aspect of saltcedar ecology is its tolerance of high salinity soils and transport of salts from the soil. Since saltcedar is able to tolerate salinities that other riparian species cannot, it is able to outcompete native species where salinities approach the upper end of native tolerances. Further, saltcedar collects salts from the soil and transports them to be exuded through salt glands on the leaves. These salts are excreted and can form white residues on the outside of the plant. When the leaves senesce, they fall to the soil surface, often forming a saline crust. This process elevates the salinity of the upper layer of the soil beyond the tolerances of other species, further establishing saltcedar’s competitive advantage in these environments (Sogge et al. 2008, Mortenson et al. 2012, Bangert et al. 2013). Invasion The earliest reports of Saltcedar escaping cultivation come from the 1870’s, and by the 1920’s an estimated 4,000 ha was infested with escaped saltcedar. By 1970, the infestation was estimated at over 540,000 ha in an area encompassing much of the arid west from Oklahoma to California and from Colorado to Mexico. By 1987 the southwestern US alone supported an estimated 600,000 ha spreading at a rate of 3-4% a year (Di Tomaso 1998). This invasion has severe implications for riparian systems throughout the American Southwest. Given the biological and ecological characteristics outlined above, saltcedar has displaced large areas of native riparian vegetation and attendant wildlife, changed the salinity of large areas of land, increased salinity, changing hydrology along stream and river banks, increasing fire hazard, decreased forage. Zavaleta (2000) estimated that water loss due to saltcedar infestations was on the order of $127 million/year. However, recent work has indicated that since restoration of riparian or wetland sites currently dominated by saltcedar typically includes high water use native plants that support native fauna, there is likely to be no net change in water use in these areas if saltcedar is removed. In more upland settings, the water use argument is more cogent if saltcedar is replaced with lower water use plants (Nagler and Glenn 2013).

Biocontrol Effort General Tamarix control Given the environmental and economic impacts attributed to saltcedar invasion and rapid expansion, control and management efforts have been undertaken throughout its new range. Conventional control methods include herbicide applications and mechanical removal.

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While there have been successes with these methods, the ability of the plant to re-sprout from damaged tissue and the high logistic and financial cost of these methods has precluded their widespread use. Further, both of these methods incur a high non-target or collateral cost on associated plant and animal species present in or around stands of saltcedar. Remote or inaccessible habitats that are invaded by saltcedar do not readily lend themselves to conventional control methods, and many sites are re-infested because of the intense labor required both for initial control and any necessary follow-up treatments. The limitations of chemical and mechanical control methods make widespread control impossible to achieve, let alone a reversal of saltcedar’s expansion across the Southwest (Powell 2005, Shafroth et al. 2005, Dickie et al. 2014). Biocontrol Classical biocontrol of invasive species relies on trophic interactions present in the invader’s native range. Based in part on the idea of competitive or predatory release, where the invader is free from consumer pressures or competitors found in the native ecosystem, biocontrol seeks to replicate consumer pressure on the invader by introducing species capable of controlling the invasive species. In the case of plants, specialist herbivores are identified from the invader’s native environment that exhibit host specificity and high levels of control efficacy (Berro 2013). While the latter is important as a matter of course, the former is especially important to avoid spread of the biocontrol agent to non-target native plants. Choice experiments are typically run on potential agents to assure that prospective species will starve rather than switching to native analogs (Paxton et al. 2011). In the case of saltcedar, efforts to investigate the use of biocontrol agents were begun by the U.S. Department of Agriculture-Agricultural Research Service Program (USDA-ARS) in the 1960s (Dudley and Deloach 2004a). Work was done both overseas and in domestic quarantine settings, eventually leading in 1994 to the identification of two potential species of biocontrol agents for release by the Animal and Plant Health Inspection Service (APHIS). The first was a mealy bug (Trabutina mannipara) and the second was the saltcedar leaf beetle (Diorhabda elongata) (Dudley and Bean 2012). The saltcedar leaf beetle seemed like a good choice, as its native distribution included climates similar to those of the main areas of infestation of saltcedar in North America. It is easy to handle, has rapid population growth and has a major effect on target plants once established. While the mealy bug was also considered, and in fact had the potential to be better adapted to the hotter climates of the Southwest, other considerations (discussed below) removed the mealy bug from release plans (Bright et al. 2013). Cage releases of the saltcedar leaf beetle were done in the late 1990’s, followed by open release of the beetle on seven infested sites in 2001. Observations over the next decade showed moderate to high rates of spread from introduction sites, but no complete mortality of target plants except in cage experiments where the beetle was maintained at artificially high densities. Defoliation by the beetle resulted in significant re-sprouting that extended the plant’s overall growing season by as much as 4 weeks (Dudley and Deloach 2004a). As of 2013, the success of the saltcedar leaf beetle as a biocontrol agent was equivocal. In terms of suppressing the growth of stands of saltcedar, the beetle can exhibit extensive defoliation, but this is typically temporary or cyclical, with plants re-sprouting from damaged tissue. Beetles were

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found to avoid previously defoliated plants in the subsequent season, allowing significant regrowth before another round of defoliation. Complete mortality of saltcedar stands or individuals with the leaf beetle alone is rare, and the compositional outcome of beetle occupancy in saltcedar stands is a heterogeneous mixture of saltcedar in various stages of defoliation. However, the seasonal rapidity of defoliation events, though only temporarily damaging to the saltcedar, can have dramatic effects on structural habitat components of riparian species that use saltcedar (Nagler and Glenn 2013). (Tracy et al. 2013).

Southwestern Willow Flycatcher One of the primary species affected by both the invasion of saltcedar into riparian corridors and by the introduction of the saltcedar leaf beetle is the Southwestern willow flycatcher. The SWWF is a small (~15 cm) bird that requires riparian habitat that is dense with its eponymous willow species as well as cottonwoods and other species. It also requires proximity to standing water or streams which supply its diet of flying . The native habitat of the SWWF has been heavily impacted by grazing pressures, water diversion, development, pollution and invasive species. This degradation of the SWWF habitat was abetted by the expansion of saltcedar which replaced remnant native habitat throughout the SWWF range. As a consequence, the SWWF is a federally endangered species (Brown and Trosset 1989, Paradzick and Woodward 2003). Contemporaneous with biocontrol trials for the mealy bug and leaf beetle, it was recognized that the SWWF was using saltcedar for nesting and migration corridors, especially in the Southwest and Arizona, likely because native alternatives had been extirpated. As a result, the US Fish and Wildlife Service (FWS) determined that release of biocontrol agents proximate to populations of saltcedar supporting SWWF could constitute a loss of habitat, and therefore a ‘take’ under the Endangered Species Act. Despite the fact that saltcedar was one of the factors putting the SWWF at risk of extinction, APHIS entered into Section 7 consultation with FWS regarding the biocontrol effort. Based on this consultation and resultant Biological Opinion, the mealy bug was removed from consideration because of its ability to tolerate the climate of the Southwest, while the beetle was released 320 km away from any known use of saltcedar by SWWF. The concern centered around two potential impacts (Dudley and DeLoach 2004b). The first was concern that the leaf beetle would defoliate stands of saltcedar wholesale, at a rate that would expose SWWF to predation and other pressures before native analogs could re- establish. The second concern was that leaf beetles would concentrate saltcedar toxins from consuming the leaves which could poison the SWWF or other insectivorous wildlife if it predated on the beetles.

Endangered Species Management Criticism of single-species management of ecosystems is fairly widespread in conservation literature. The Endangered Species Act, however, gives precedent to preserving

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individual rare species with general exclusion of considerations of overall ecosystem function or impacts to co- occurring flora or fauna. While this may work in theory for those species whose presence enables support of whole- Figure 1: Hypothetical flow chart of biocontrol impacts from Paxton et al. 2011. ecosystem function (ex. keystone, umbrella, foundation, or flagship species), in cases where preservation of the rare species is reliant on maintenance of habitat-degrading invasives, single-species ecosystem management is a fraught exercise. If the SWWF is an inappropriate indicator of overall ecosystem health or quality, then using this species as the fulcrum for conservation efforts may expose associated species to continued habitat degradation and decline. Dudley (2004) argues that “It is not rational to attempt to maintain stasis of a damaged system until all questions about the SWWF are answered”. This is especially the case in a disturbed system that may have localized successional trajectories arising from specific disturbance events, or have established novel systems. In the intervening years from the initial introduction of the leaf beetle the ranges for the SWWF and the leaf beetle have overlapped (Hinojosa-Huerta 2006, York et al. 2011, Nagler and Glenn 2013). The beetle spread well beyond the initial introduction sites and concern that the beetle would impact SWWF compelled APHIS to discontinue saltcedar leaf beetle release in 2010. Evidence suggests that defoliation effects on SWWF are mixed. Leaf beetles become food source for the SWWF, while the timing of nesting could serve as an ecological trap for the species. SWWF nests in the spring when the saltcedar is still green, but their nesting period extends into the summer when saltcedar defoliation occurs. This can expose the nest to predation or heat stress [see Figure 1 from Paxton (2011)]. SWWF is capable of utilizing other nest vegetation where present, and in mixed stands of saltcedar and natives can adapt to the seasonality of saltcedar defoliation. Levels of saltcedar infestation also govern nesting success of SWWF. Estimates of acceptable cover of native tree species range from 10-40% for optimal habitat. It is not until saltcedar achieves 90% cover that habitat value decreases significantly (Cohn 2005, van Riper et al. 2008, Nagler and Glenn 2013). This suggests that the effects of leaf beetle defoliation and SWWF response are likely to be highly site-specific. In less saline areas of its range, native tree species are able to compete in light gaps or exposed niches vacated by saltcedar subject to defoliation. These areas are also ripe for concentrated restoration activities to enhance overall species diversity and habitat heterogeneity. However, in more saline sites like those of the lower Colorado River, repeated

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defoliation events will diminish SWWF saltcedar habitat with little ability for less salt tolerant natives to establish.

Conclusions It can be argued that the sides in this conundrum are each viewing the ecosystem from the perspective of a single species. On the one side are the conservation and restoration communities concerned with the spread and impacts of saltcedar, and thereby the overall health of the ecosystems of the Southwest. In this view, a significant portion of the damage done to these systems over the last two centuries can be mitigated by controlling saltcedar and restoring some semblance of native function or composition to otherwise transformed landscapes. On the other side are the regulatory agencies constrained by the Endangered Species Act to protect rare species no matter the overall impact to the ecosystem, and ecologists who argue that removal of saltcedar alone, without considering the site-specific impacts of removal, can have significant negative consequences that are likely unacceptable for all involved. Meanwhile, the saltcedar leaf beetle is unaware that it is unwelcome in areas where it was not intentionally released. Despite the efforts of APHIS to only release the beetles at sites distant from SWWF, the beetle population continues to expand into new areas, increasing interactions with SWWF. It seems that now there is opportunity to learn from the interactions between saltcedar, the beetle, and SWWF as well as the related interactions of the communities in which these individuals are found. There is really little alternative. For the foreseeable future, both saltcedar and the saltcedar leaf beetle are permanent residents of the Southwest. The interplay between these two species and the other species (native and non- native) in this large and heterogeneous region is likely far from any sort of equilibrium. Which species ultimately benefit or suffer from the beetle release may take decades to resolve. What the introduction of the beetle seems to have accomplished is a greater research focus on community assembly (and disassembly) in habitats of the Southwest. This is especially true regarding the SWWF, which, for good or ill, wields outsized regulatory heft. Ancillary benefits of this focus radiate to other species and to land-management approaches throughout the region. One of the most concrete perspectives that has arisen from the experience of saltcedar biocontrol seems to be the (retrospectively obvious) conclusion that there will be no magical silver bullet capable of removing a century’s worth of saltcedar invasion. Work to preserve the unique communities of the Southwest, including endangered species like the SWWF and others will have to include the full suite of tools available along with significant re- planting and targeted restoration tailored to site-specific conditions. Saltcedar has become deeply interwoven into the ecology, culture and politics of the region creating a complicated, reticulate network of local and regional interests and perspectives. Complete eradication is unlikely, though local-scale management may approach this functional goal when coupled with integrative restoration work. Future work will need to further elevate whole-ecosystem management goals over single-species advocacy where possible — incorporating the latest understanding of the ecology of the marquee species of saltcedar and the flycatcher into regional planning — if anything approaching long-term stability of these severely altered systems is to be achieved.

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