Plot- and landscape-level changes in climate and vegetation following defoliation of exotic saltcedar (Tamarix sp.) from the biocontrol agent Diorhabda carinulata along a stream in the Mojave Desert (USA)

Journal of Arid Environments 89 (2013) 16e20

Contents lists available at SciVerse ScienceDirect

Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv

Short communication

Plot- and landscape-level changes in climate and vegetation following defoliation of exotic saltcedar (Tamarix sp.) from the biocontrol agent Diorhabda carinulata along a stream in the Mojave Desert (USA) H.L. Bateman a, *, P.L. Nagler b, E.P. Glenn c a b c

Arizona State University at the Polytechnic Campus, Department of Applied Sciences and Mathematics, 6073 S. Backus Mall, Mesa, AZ 85212, USA U.S. Geological Survey, Southwest Biological Science Center, Sonoran Desert Research Station, 1110 E. South Campus Drive, Tucson, AZ 85721, USA University of Arizona, Environmental Research Laboratory, 2601 E. Airport Drive, Tucson, AZ 85706, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 10 April 2012 Received in revised form 7 September 2012 Accepted 17 September 2012 Available online 3 November 2012

The biocontrol agent, northern tamarisk beetle (Diorhabda carinulata), has been used to defoliate nonnative saltcedar (Tamarix spp.) in USA western riparian systems since 2001. Biocontrol has the potential to impact biotic communities and climatic conditions in affected riparian areas. To determine the relationships between biocontrol establishment and effects on vegetation and climate at the plot and landscape scales, we measured temperature, relative humidity, foliage canopy, solar radiation, and used satellite imagery to assess saltcedar defoliation and evapotranspiration (ET) along the Virgin River in the Mojave Desert. Following defoliation solar radiation increased, daily humidity decreased, and maximum daily temperatures tended to increase. MODIS and Landsat satellite imagery showed defoliation was widespread, resulting in reductions in ET and vegetation indices. Because biocontrol beetles are spreading into new saltcedar habitats on arid western rivers, and the eventual equilibrium between beetles and saltcedar is unknown, it is necessary to monitor trends for ecosystem functions and higher trophic-level responses in habitats impacted by biocontrol. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: Microclimate NDVI Remote-sensing Riparian vegetation Virgin River Weed biocontrol

1. Introduction Non-native saltcedar (also known as tamarisk; Caryophyllales: Tamaricaceae, Tamarix spp.) is the third most dominant woody genus in riparian areas of the arid western USA, after native willow (Salix spp.) and cottonwood (Populus spp.; Friedman et al., 2005). Saltcedar can form dense, monotypic thickets supporting little native vegetation (DiTomaso, 1998) and negatively affects some wildlife species (Bateman and Ostoja, 2012). Natural resource managers spend considerable time and resources controlling saltcedar using a variety of techniques, including chemical (Duncan and McDaniel, 1998), mechanical, and burning methods (Shafroth et al., 2005). A technique that has drawn much attention is the use of the northern tamarisk beetle (Coleoptera: Chrysomelidae, Diorhabda spp.; Tracy and Robbins, 2009), a specialist herbivore, as a biological control agent (Lewis et al., 2003). Despite the widespread application of Diorhabda, and the success of saltcedar * Corresponding author. Tel.: þ1 480 727 1131; fax: þ1 480 727 1236. E-mail addresses: [email protected], [email protected] (H.L. Bateman), [email protected] (P.L. Nagler), [email protected] (E.P. Glenn). 0140-1963/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jaridenv.2012.09.011

defoliation, however, only limited research has quantified the consequences on biotic communities, abiotic components, and ecosystem services. Hultine et al. (2010) pointed to considerable promise for controlling saltcedar over large areas of invaded habitat; however, there may also be possible negative effects of Diorhabda releases on riparian ecology. Because adverse non-target effects of biocontrol agents have been observed, identifying potential hazards to native species and ecosystems is important for resource managers to balance the benefits and risks of biocontrol (DeClercq et al., 2011). The aim of our study was to determine the relationships between Diorhabda establishment and defoliation and the effects on vegetation and climate at the plot and landscape scales. Our research objectives included: (1) determining the abundance of Diorhabda and the timing and duration of saltcedar defoliation, (2) determine how defoliation affects microclimate (temperature and humidity) and microhabitat (solar radiation and percent canopy cover) at the plot scale, (3) determine the effects of defoliation on saltcedar evapotranspiration (ET) rates, and (4) determine how defoliation affects both the normalized difference vegetation index (NDVI) and the enhanced vegetation index (EVI) to evaluate seasonal and annual changes temporally. By collecting vegetation

H.L. Bateman et al. / Journal of Arid Environments 89 (2013) 16e20

and climate data prior to and following biocontrol establishment, our results provide baseline information on habitat altered by biocontrol defoliation which could affect ecosystem processes in saltcedar stands. 2. Methods In the Mojave Desert of the USA, the Virgin River (a tributary to the Colorado River) contains both extensive saltcedar stands (Tamarix parviflora, Tamarix ramosissima, and Tamarix chinensis) and native trees such as cottonwood, willow, and mesquite (Prosopis spp.). In 2006, weed managers moved a biological control agent (Diorhabda carinulata) to control saltcedar infestations along the Virgin River. We monitored the effects of biocontrol defoliation between Mesquite (three sites) and Gold Butte (two sites) in Clark County, Nevada USA during 2010 and 2011 (Appendix 1 online version only). Because northern tamarisk beetle larvae drop to the litter to pupate and adults emerge from the litter (Herrera et al., 2005), we monitored beetles in nine liter pitfall traps installed at ground level. Pitfall traps were associated with a larger research effort monitoring herpetofauna and ground arthropods (Bateman and Ostoja, 2012). Northern tamarisk beetle adults and larvae were counted daily at the five sites in June and July during 35 days and 31 days in 2010 and 2011, respectively. Maximum daily temperature and relative humidity were collected at 10 min intervals with data loggers (HOBO Pro v2, Onset Computer Corporation, Pocasset, MA, USA) from 47 to 50 days from day of the year (DOY) 152 (1 June 2011) to DOY 203 (22 July 2011) at each of the five sites. Loggers were installed at approximately 1.5 m from ground level and were under canopy cover of saltcedar. Daytime was considered to be from 0540 to 1950 based on sunrise and sunset. Reference data, or maximum daily temperatures not affected by saltcedar biocontrol, were collected from a NOAA weather station (i.e., Mesquite 2NE) installed at an unknown height located in Mesquite, Nevada. Ocular estimates of defoliation (categories: 0, 1e5%, 5e25%, 25e50%, 50e75%, 75e95%, and >95%) of the immediate area (within 1 m of data logger) were recorded twice prior to and twice following defoliation. Because defoliation from biocontrol can occur rapidly, we defined plots as defoliated when trees reached 75% defoliation. We measured percent canopy cover using a concave densiometer at each of the five sites. Densiometer measures were taken at four locations within 1 m of data loggers twice prior to and twice after defoliation. We measured photosynthetically active radiation (PAR) twice prior to and twice following defoliation at four locations (N, E, S, and W) within 1 m of data loggers using a radiation sensor (LI-190 Quantum Sensor, LI-COR Biosciences, Lincoln, NE, USA). A control PAR measurement was taken in full sun with no sky obstructed by vegetation. PAR measurements were recorded by a technician at the data logger location, and then the technician walked to an area of open terrain, with no vegetation canopy to record the control measurement. Our measurements of radiation were the average percent difference between the four understory readings and the control reading. The densiometer measures canopy closure, including stems and branches; whereas, the LI-COR provides a direct measure of light transmission through the canopy. It is possible to have high canopy closure but light penetration into the canopy due to reflection and scattering of light. We compared percent canopy cover and radiation before and after defoliation using a paired t-test. Two 2011 Landsat 5 images (Path 38 Row 35), with 30 m resolution, encompassing the Mesquite sites were acquired, one before biocontrol defoliation (DOY 156, 5 June 2011) and one during the defoliation period (DOY 203, 22 July 2011). Two additional Landsat

17

5 images (Path 39, Row 35) encompassing the Gold Butte sites were acquired on DOY 173 (22 June 2011) before biocontrol defoliation and on DOY 201 (20 July 2011) after evidence of biocontrol defoliation. Images were acquired from the USGS Earth Explorer website and were processed to Level 1T by the U. S. Geological Survey. Digital number (DN) pixel values for each reflectance band were converted to surface reflectance values using the COST-TM 5 model as developed by Chavez (1996). The sun zenith angle and the earthesun distance at the time of image acquisition is included to correct for haze in the atmosphere. After converting pixels to surface reflectance values, the NDVI was calculated as:

NDVI ¼ ðrNIR  rRedÞ=ðrNIR þ rRedÞ

(1) 1

NDVI values were converted to ET estimates (mm d ) using a modification of the method outlined in Baugh and Groeneveld (2006), Groeneveld and Baugh (2007) and Groeneveld et al. (2007). Groeneveld et al. (2007) reported an r2 of 0.95 between ET measured at eddy covariance flux towers and ET estimated from single summer Landsat images for phreatophyte communities in the western USA. In this method, NDVI values are first scaled (NDVI*) between bare soil (NDVI* ¼ 0) and fully transpiring vegetation (NDVI* ¼ 1.0) by the formula:

NDVI* ¼ 1  ðNDVIMax  NDVIÞ=ðNDVIMax  NDVISoil Þ

(2)

where NDVIMax is the maximum NDVI observed on the image and NDVISoil is determined from an image area of apparent bare soil or rock outcropping on the image. ET is then estimated by multiplying NDVI* by the rate of potential ET (ETo) determined from meteorological data:

ET ¼ NDVI*ðETo Þ

(3)

ETo was determined by the BlaneyeCriddle formula, based on mean monthly temperature and hours of sunlight:

  ETo mm d1 ¼ pð0:46 TMean þ 8Þ

(4)

where p is the mean daily percentage of annual daytime hours (determined from a table based on latitude) and TMean is mean monthly temperature in  C (Brouwer, 1986). Nagler et al. (2009) showed that the BlaneyeCriddle ETo gives values about 10% lower than the more complete PenmaneMonteith equation, and is useful in riparian studies where only temperature data are available to estimate ETo. NDVI and ET were determined for an 11.6 ha polygon encompassing Mesquite field sites and a 4.8 ha polygon at Gold Butte sites along the Virgin River. Pixel resolution was approximately 30 m in the Landsat images. We used MODIS as a complimentary method to the Landsat estimates. In a similar approach, Nagler et al. (2009) correlated ground measurements of ET by riparian species and alfalfa on the Lower Colorado River with ETo and the EVI from MODIS (250 m resolution). Although MODIS has lower spatial resolution than Landsat, it has nearly-daily coverage of the earth, and is especially useful in revealing temporal patterns of biophysical variables such as leaf area index (LAI) and ET (Glenn et al., 2008). Hence, the combination of Landsat and MODIS imagery provides both high spatial and high temporal resolution. EVI values were obtained from Oak Ridge National Laboratory DAAC website which displays approximate pixel footprints on a high-resolution Google Earth image. We selected three individual pixels per study area (Mesquite and Gold Butte) for analyses. One pixel encompassed the two field sampling sites and the other two were in wide areas of apparent saltcedar cover approximately 1 km upstream and downstream of the study site. Pixels were contained

18

H.L. Bateman et al. / Journal of Arid Environments 89 (2013) 16e20

wholly within the riparian corridor and did not encompass open water or bare soil. MOD13Q1 16-day composite EVI values were converted to scaled EVI values (EVI*) similar to Equation (2):

EVI* ¼ 1  ðEVIMax  EVIÞ=ðEVIMax  EVISoil Þ

(5)

where EVIMax ¼ 0.542 and EVISoil ¼ 0.091 based on a large database from previous studies (Nagler et al., 2005). ET was then calculated as:

ET ¼ 1:22ETo ðEVI*Þ

(6)

The coefficient 1.22 was determined by the linear equation of best fit between measured ET and EVI* and ETo (r2 ¼ 0.80; Nagler et al., 2009). 3. Results

measurements. Percent foliar canopy cover slightly decreased in plots following defoliation (t(4) ¼ 2.791, p ¼ 0.049). Prior to defoliation, plots averaged 97.6% (SD ¼ 1.8) canopy cover and averaged 94.6% (SD ¼ 3.9) canopy cover following defoliation. Relative humidity and temperature were recorded 25e30 days prior to defoliation and 10e11 days following defoliation. Both average daily relative humidity and maximum daily relative humidity (Fig. 1B) showed declines concurrent with defoliation. Average daily relative humidity in plots decreased following defoliation (t(4) ¼ 10.305, p < 0.001); prior to defoliation plots averaged 33.1% (SD ¼ 3.6) and following defoliation plots averaged 18.9% (SD ¼ 1.8). Average maximum daily temperatures tended to be greater following defoliation (Wilcoxon Signed Rank Test, W ¼ 15.0, p ¼ 0.063; Fig. 1C) with an average of 40.4  C (SD ¼ 1.5) before defoliation and 43.6  C (SD ¼ 0.6) after defoliation. Maximum daily temperature collected during the same time period from a NOAA

3.1. Microhabitat changes following defoliation Sites were considered to be 75% defoliated by 11e12 July 2011. Leaf beetles were present in sites at least 25 days prior to 75% defoliation of saltcedar, reaching a peak from 5 to 10 days before defoliation and then decreasing (Fig. 1A). Solar radiation measures increased in plots following defoliation (t(4) ¼ 3.996, p ¼ 0.016). Prior to defoliation, plots averaged 11.2% (SD ¼ 12.3) of available solar radiation compared to control measurements. Following defoliation, plots averaged 34.7% (SD ¼ 24.4) of available solar radiation compared to control

Fig. 1. Conditions at five sites along the Virgin River in Nevada during 2011 affected by biocontrol of saltcedar (Tamarix sp.). (A) Daily northern tamarisk beetle (Diorhabda carinulata) counts in pitfall traps. Blank values represent no data collected when traps were closed. (B) Maximum daily relative humidity (mean and standard error). (C) Maximum daily temperature (mean and standard error) at study sites (black circles) and maximum temperature at Mesquite, NV NOAA weather station (gray circles). Zero days since defoliation was the day ocular estimate determine that defoliation was >75%.

Fig. 2. Images of sites (red polygons) of the normalized difference vegetation index (NDVI) along the Virgin River in Nevada affected by biocontrol of saltcedar (Tamarix sp.). (A) NDVI image of a section of the Virgin River near Mesquite, Nevada on 5 June 2011, before beetle defoliation of saltcedar. (B) NDVI image on 22 July 2011, during defoliation. Lighter colored pixels denote higher NDVI values. Images are zoomed in to show the resolution limits of the individual pixels (ca. 30 m). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

H.L. Bateman et al. / Journal of Arid Environments 89 (2013) 16e20

reference site averaged 40.6  C (SD ¼ 5.2) before defoliation and 39.8  C (SD ¼ 3.4) after defoliation (Fig. 1C). 3.2. NDVI and ET changes following defoliation Biocontrol had a marked negative effect on NDVI in 2011, which was 0.475 (SD ¼ 0.104) before defoliation and 0.254 (SD ¼ 0.060) following defoliation at the Mesquite sites (Fig. 2). Defoliation was not confined to the polygon encompassing the field survey sites but extended over the entire river reach (Fig. 2). Estimated ET values for the Mesquite sites were 2.29 mm d1 before and 0.49 mm d1 after beetle defoliation, representing 36% and 7% of ETo respectively. Biocontrol defoliation was less pronounced at the Gold Butte sites, with NDVI values of 0.457 (SD ¼ 0.059) and 0.300 (SD ¼ 0.030) and ET values of 2.36 mm d1 and 1.08 mm d1 (35% and 15% of ETo) before and after defoliation, respectively. Temporal patterns of EVI and ET revealed by MODIS imagery for the Virgin River showed a typical pattern of increase in spring and decrease in fall (Fig. 3). At the Mesquite sites, peak values of EVI and ET in 2010 were similar to 2009 (Fig. 3A and B), but a mid-season decrease in both variables was evident during this first year of biocontrol defoliation. In 2011, peak values for EVI and ET at the Mesquite sites were only half as great as in previous years, presumably due to biocontrol defoliation (Fig. 3A and B). In 2009, and 2010, peak ET values were about 4.5 mm d1 but were reduced to 2.5 mm d1 in 2011. As with the Landsat data, Gold Butte sites

19

were impacted less than Mesquite sites. A small late-season reduction in EVI and ET was noted in 2011 but no apparent effects of biocontrol were noted in 2010, and although peak EVI and ET values were similar across the three years, they were lower than the Mesquite sites (Fig. 3C and D). 4. Discussion The microclimate of saltcedar stands becomes dryer and hotter with increased solar radiation following the reduction in foliar cover after biocontrol defoliation from the northern tamarisk beetle. Although the month of July can be hotter than June in the Mojave Desert, the observed increase in temperature in our sites was not evident at a nearby NOAA weather station. Prior to defoliation, maximum temperatures from our sites were slightly lower than maximum temperatures recorded at the station. About eight days prior to 75% defoliation, our sites became hotter and remained hotter than the weather station presumably because the station was unaffected by biocontrol. Although the magnitude of change in solar radiation was greater than the change measured in foliar canopy cover, this is likely due to the difference in precision between the two instruments. As such, these measurements are related but not inverse to each other. This study and others have documented that the northern tamarisk beetle can cause a reduction in saltcedar NDVI and ET values, followed by saltcedar regrowth a few weeks following

0.5

8

B

A 0.4

ET (mm d-1)

6

EVI

0.3

0.2

4

2

0.1

0

0.0

2009

2010

2011

2012

2009

2010

2011

2012

2010

2011

2012

8

0.5

C

D

0.4

ET (mm d-1)

6

EVI

0.3

0.2

4

2

0.1

0.0

0

2009

2010

2011

2012

2009

Fig. 3. Enhanced vegetation index (EVI) and evapotranspiration (ET) along the Virgin River in Nevada affected by biocontrol of saltcedar (Tamarix sp.). (A) EVI values for three MODIS pixels and (B) ET values calculated from EVI (closed circles) and ETo (solid line) at the Mesquite sites along the Virgin River. (C) EVI values for three MODIS pixels and (D) ET values calculated from EVI (closed circles) and ETo (solid line) at the Gold Butte site along the Virgin River. Bars are plus standard errors of means.

20

H.L. Bateman et al. / Journal of Arid Environments 89 (2013) 16e20

defoliation. One study on the Colorado Plateau documented over 50 days of reduced NDVI in saltcedar stands following biocontrol (Dennison et al., 2009). In the early stages of biocontrol expansion, the reduction in NDVI from defoliation can create substantial declines in saltcedar water use (Pattison et al., 2011). Hudgeons et al. (2007) found that repeated defoliation can occur for several years leading to reduced survival and reproduction of saltcedar. However, Nagler et al. (2012) showed that NDVI values eventually return to pre-beetle-release levels, due to regeneration of saltcedar and infill with other species, both native and non-native. This study and others have demonstrated that using remotely sensed images to calculate vegetation indices can be a viable method to document the timing and extent of saltcedar defoliation from biocontrol. Although initial saltcedar biocontrol releases have been monitored, no comprehensive program is currently in place to monitor the rapid spread of Diorhabda spp. that has resulted from numerous subsequent releases. An exception is the Virgin River in the Mojave Desert, where efforts to monitor multiple plant and animal taxa have been ongoing since 2009 before arrival of the northern tamarisk beetle (Bateman et al., 2010). Biocontrol beetles are spreading into new saltcedar habitats on arid western rivers, and the eventual equilibrium state between beetles and saltcedar is unknown. Thus, long-term trends for ecosystem functions (e.g., vegetation growth and structure, and water resources) and higher trophic-level responses in habitats impacted by saltcedar biocontrol remains uncertain and necessitate further monitoring. Ultimately, riparian restoration efforts might be needed to restore and improve vegetation and habitat value for native plants and animals inhabiting beetle-infested river reaches. Acknowledgments We thank the Bureau of Land Management in Nevada for permitting access to study sites. We thank technician Aaron Switalski for collecting field data. Funding for H.L.B. has come from the Department of Applied Sciences and Mathematics at Arizona State University. We thank two anonymous reviewers for their valuable comments to the manuscript. Any use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. government. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.jaridenv.2012.09.011. References Bateman, H.L., Dudley, T.L., Bean, D.W., Ostoja, S.M., Hultine, K.R., Kuehn, M.J., 2010. A river system to watch: documenting the effects of saltcedar (Tamarix spp.) biocontrol in the Virgin River Valley. Ecological Restoration 28, 405e410. Bateman, H.L., Ostoja, S.M., 2012. Invasive woody plants affect the composition of native lizard and small mammal communities in riparian woodlands. Animal Conservation 15, 294e304.

Baugh, W.M., Groeneveld, D.P., 2006. Broadband vegetation index performance evaluated for a low-cover environment. International Journal of Remote Sensing 27, 4715e4730. Brouwer, C., 1986. Irrigation Water Management: Irrigation Water Needs. FAO, Rome. http://www.fao.org/docrep/S2022E/s2022e00.htm#Contents (accessed 04.11.11.). Chavez Jr., P.S., 1996. Image-based atmospheric correctionseRevisited and improved. Photogrammetric Engineering & Remote Sensing 62, 1025e1036. DeClercq, P., Manson, P., Babendreier, D., 2011. Benefits and risks of exotic biological control agents. BioControl 56, 681e698. Dennison, P.E., Nagler, P.L., Hultine, K.R., Glenn, E.P., Ehleringer, J.R., 2009. Remote monitoring of tamarisk defoliation and evapotranspiration following saltcedar leaf beetle attack. Remote Sensing of Environment 113, 1462e1472. DiTomaso, J., 1998. Impact, biology, and ecology of saltcedar (Tamarix spp.) in the southwestern United States. Weed Technology 12, 326e336. Duncan, K.W., McDaniel, K.C., 1998. Saltcedar (Tamarix spp.) management with imazapyr. Weed Technology 12, 337e344. Friedman, J., Auble, G., Shafroth, P., Scott, M., Merigliano, M., Freehling, M., Griffen, E., 2005. Dominance of non-native riparian trees in western USA. Biological Invasions 7, 747e751. Glenn, E.P., Huete, A.R., Nagler, P.L., Nelson, S.G., 2008. Relationship between remotely sensed vegetation indices, canopy attributes and plant physiological processes: what vegetation indices can and cannot tell us about the landscape. Sensors 8, 2136e2160. Groeneveld, D.P., Baugh, W.M., 2007. Correcting satellite data to detect vegetation signal for eco-hydrologic analyses. Journal of Hydrology 344, 135e145. Groeneveld, D.P., Baugh, W.M., Sanderson, J.S., Cooper, D.J., 2007. Annual groundwater evapotranspiration mapped from single satellite scenes. Journal of Hydrology 344, 146e156. Herrera, A.M., Dahlsten, D.D., Tomic-Carruthers, N., Carruthers, R.I., 2005. Estimating temperature-dependent developmental rates of Diorhabda elongata (Coleoptera: Chrysomelidae), a biological control agent of saltcedar (Tamarix spp. Environmental Entomology 34, 775e784. Hudgeons, J.L., Knutson, A.E., Heinz, K.M., DeLoach, C.J., Dudley, T.L., Pattison, R.R., Kiniry, J.R., 2007. Defoliation by introduced Diorhabda elongata leaf beetles (Coleoptera: Chrysomelidae) reduces carbohydrate reserves and regrowth of Tamarix (Tamaricaceae). Biological Control 43, 213e221. Hultine, K.R., Belnap, J., van Riper III, C., Ehleringer, J.R., Dennison, P.E., Lee, M.E., Nagler, P.L., Snyder, K.A., Uselman, S.M., West, J.B., 2010. Tamarisk biocontrol in the western United States: ecological and societal implications. Frontiers in Ecology and the Environment 8, 467e474. Lewis, P.A., DeLoach, C.J., Knutson, A.E., Tracy, J.L., Robbins, T.O., 2003. Biology of Diorhabda elongata deserticola (Coleoptera: Chrysomelidae), an Asian leaf beetle for biological control of saltcedars (Tamarix spp.) in the United States. Biological Control 27, 101e116. Nagler, P.L., Brown, T., Hultine, K.R., van Riper III, C., Bean, D.W., Dennison, P., Murray, R.S., Glenn, E.P., 2012. Regional scale impacts of Tamarix leaf beetles (Diorhabda carinulata) on the water availability of western U.S. rivers as determined by multi-scale remote sensing methods. Remote Sensing of Environment 118, 227e240. Nagler, P.L., Morino, K., Murray, R.S., Osterberg, J., Glenn, E.P., 2009. An empirical algorithm for estimating agricultural and riparian evapotranspiration using MODIS Enhanced Vegetation Index and ground measurements of ET. I. Description of method. Remote Sensing 1, 1273e1297. Nagler, P.L., Scott, R., Westenberg, C., Cleverly, J.R., Glenn, E.P., Huete, A.R., 2005. Evapotranspiration on western U.S. rivers estimated using the Enhanced Vegetation Index from MODIS and data from eddy covariance and Bowen ratio flux towers. Remote Sensing of Environment 97, 337e351. Pattison, R.R., D’Antonio, C.M., Dudley, T.L., Allander, K.K., Rice, R., 2011. Early impacts of biological control on canopy cover and water use of the invasive saltcedar tree (Tamarix spp.) in western Nevada, USA. Oecologia 165, 605e616. Shafroth, P.B., Cleverly, J.R., Dudley, T.L., van Riper III, C., Stuart, J.N., 2005. Control of Tamarix in the western United States: implications for water salvage, wildlife use, and riparian restoration. Environmental Management 35, 231e246. Tracy, J.T., Robbins, T.O., 2009. Taxonomic revision and biogeography of the Tamarixfeeding Diorhabda elongata (Brullé, 1832) species group (Coleoptera: Chrysomelidae: Galerucinae: Galerucini) and analysis of their potential in biological control of Tamarisk. Zootaxa 2101, 1e152.