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Disappearance of a dominant bosque species: screwbean mesquite (Prosopis pubescens).

Riparian forests or "bosques" have been heavily affected by human development in the United States and are rapidly being cleared for agriculture, fuel use, recreational facilities, and urban growth (Ohmart et al., 1988; Szaro 1989). Bosque habitat is also being altered by excessive grazing (Kauffman and Kreuger, 1984), altered flood dynamics from damming and channelization (Snyder and Miller, 1992; Everitt, 1998), pollution (Ohmart et al., 1988), and competition with the exotic invasive saltcedar (Tamarix chinensis) (Howe and Knopf, 1991; Busch and Smith, 1995; Smith etal., 1998). Recently, human impacts on bosques have received much attention because of documented declines in willow (Salix) and cottonwood (Populus) (i.e., Sher et al., 2002; Pataki et al., 2005). This has led to a discussion of possible ways of restoring riparian vegetation in the Southwest (Anderson, 1998; Barrows, 1998; Nagler et al., 2008).

While investigating the insect communities associated with North American mesquite plants, I discovered that screwbean mesquite (Prosopis pubescens) is absent in many localities where it was previously recorded, including half of the extent of its range along the Rio Grande and along almost all of the Gila and Salt rivers. Historic accounts characterized this species as dominant within southwestern bosques (Ainsworth and Brown, 1933; Campbell and Dick-Peddie, 1964; Younker and Andersen, 1986; Ohmart et al., 1988). Previous studies predicted a decline in this species (Ohmart et al., 1988) and documented unhealthy-looking trees along the Colorado River (Smith et al., 1998; Anderson, 2007). Here, I survey P. pubescens throughout its former range and compare its current presence with previously published surveys and herbarium records to document the extent of its decline. I then speculate on the causes of its extirpation by examining the spatial pattern of its disappearance and comparing this pattern with predictions based on its biology.

Materials and Methods--To examine the extent of population decline in P. pubescens, I compiled historical presence-absence data and surveyed some of the historical locations for comparison. I created a list of historical presence data using herbarium specimens (Arizona State University Vascular Plant Herbarium, University of Arizona Herbarium, University of Texas Herbarium), online databases (Global Diversity Information Facility, http://gbif.org; Tropicos, http://tropicos.org; and Southwest Environmental Information Network, http:// swbiodiversity.org), and published localities (Campbell and Dick-Peddie, 1964; Younker and Andersen, 1986; Ohmart et al., 1988; Felger et al., 1997; Stromberg, 1997; Fleishman et al., 2003). Georeferenced points of historical absence were obtained using the vegetation surveys of Campbell and Dick-Peddie (1964) and Younker and Andersen (1986). I chose 112 localities to survey for P pubescens during the spring and summer (2009-2011). These sites were chosen because they could easily be accessed by car within the United States. I also happened to resurvey a few sites in Mexico while this study was still being conceived. Plants were easily identified by the unmistakable pod clusters that usually remain on the plant year round. Even when defoliated with no visible fruits in the branches or on the ground, the gnarled and peeling bark is very distinctive. Historical records were compared with recent field surveys using maps generated in ArcView 10.1 (ESRI, 2011). Additionally, sites resurveyed were classified as "urban," "farmland," "Tamarix dominated," or "native vegetation" to provide insight into possible causes of P. pubescens extirpation.

I supplemented the presence-absence data with data on changes in woody plant density by comparing historic surveys along the middle Rio Grande and lower Colorado River (Campbell and Dick-Peddie, 1964; Mizoue, 1984; Ohmart et al., 1988) with surveys conducted in 2011. Eight sites were surveyed along the Rio Grande from Bernardo, New Mexico to the New Mexico-Texas border, and six sites were surveyed along the Colorado River from Parker, Arizona to the Palo Verde Diversion Dam, Arizona (see Fig. 1b for survey locations). Estimates of density were based on average measurements of canopy cover between ten 15- x 12-m belt transects, as in Campbell and Dick-Peddie (1964). Woody plant species surveyed included P pubescens; species that may be potential competitors of P. pubescens: P glandulosa, Salix (S. gooddingii and S. exigua were not distinguished from one another), Populus fremontii along the Colorado River, P deltoides along the Rio Grande, and nonnatives T. chinensis and Elaeagnus angustifolia; and two understory shrubs indicative of wetter soils: Pluchea sericea and Baccharis salicifolia. Populus and Salix were lumped together in the Colorado River surveys as in Ohmart et al. (1988). Differences between surveys were analyzed using a paired t-test in R 3.0.0 (The R Project for Statistical Computing, http://www.R-project.org).

Results--Prosopsis pubescens was historically recorded 271 times at georeferenced locations, of which 182 were considered likely to be from separate stands because of the distance apart and site descriptions. These records range from 1901 to 1999. The map generated from these records shows P. pubescens to be historically abundant along the salt River from Phoenix, Arizona to Theodore Roosevelt Lake, Arizona; along the Gila River from Yuma, Arizona to the Coolidge Dam, Arizona; along the Colorado River from St. George, Utah to Yuma, Arizona; along the Rio Grande from Bernardo, New Mexico to the eastern edge of Big Bend National Park, Texas; and scattered along smaller rivers and at isolated cienegas in the southwestern United States and northern Mexico (Fig. 1a).

A total of 112 separate sites was surveyed, 81 of which were sites where P. pubescens was historically recorded (Fig. 1b). Only 38 sites were found to have stands of P. pubescens. Of the 81 sites surveyed where P. pubescens was historically present, I classified 24 as urban, 6 as farmland, 9 as Tamarix dominated, and 42 as native vegetation (Table 1). Prosopis pubescens was found at 3 of the 24 urban sites, 1 of the 6 farm sites, none of the Tamarix dominated sites, and 34 of the 42 sites with native vegetation. The Colorado River had the highest percentage of sites with native vegetation (68%) and the Salt and Gila rivers had the lowest (0%).

Plant cover surveys along the middle Rio Grande show that P. pubescens is decreasing on average across sites (P = 0.022) and has not increased significantly in density at any site (Fig. 2). Other drought-tolerant species, Tamarix and P. glandulosa (Cleverly et al., 1997), have increased overall, though not consistently (P = 0.092). Flood-tolerant genera, Salix, Populus, Pluchea, and Baccharis (Vandersande et al., 2001; Sher et al., 2002), did not shift in abundance consistently (P = 0.847). Prosopis pubescens has been replaced by Tamarix at two sites (Anthony and Rincon) and by Salix at three other sites (Los Cruces, Bernardo, and to a lesser extent Radium Springs).

Historically, along the Colorado River, P. pubescens appears to have cycled from low densities to high densities and back down again (Fig. 3). Prosopis glandulosa has had the opposite trend, Populus and Salix declined until 1960 and have been consistently low since, and Tamarix has significantly increased in density over time (P = 0.005).

Discussion--Screwbean mesquite has disappeared from 53% of the localities in which it was found a century ago. The decline of this species along portions of the Rio Grande and Colorado River has been as recent as the last 20 years. This once-dominant species that characterized southwestern riparian communities (Ainsworth and Brown, 1933; Campbell and Dick-Peddie, 1964; Younker and Andersen, 1986; Ohmart et al., 1988) is now only found in isolated patches. Its decline was previously predicted (Ohmart et al., 1988) and recognized (Smith et al., 1998; Anderson, 2007), but now the full extent of the loss can be quantified.

Factors that can be hypothesized as affecting the demise of P pubescens include concurrent population shifts of interacting species, such as T. chinensis or a pathogen, climate change, habitat destruction by people, desiccation, and inundation. Each of these stressors makes for different predictions of the expected spatial pattern of P. pubescens loss over time. The data collected in this study can therefore be used as a baseline to understand why this species is disappearing.

Tamarix chinensis is often considered an efficient invasive species because of its potential to outcompete natives (Howe and Knopf, 1991; Busch and Smith, 1995; Smith et al., 1998). It produces comparatively high numbers of seeds (Warren and Turner, 1975), is grazed less often by herbivores (Stromberg, 1997), may alter the local environment by increasing fire frequency and intensity (Busch, 1995) or increasing soil salinity (Busch and Smith, 1995; Vandersande et al., 2001), and may be able to tolerate fire regimes, long-term inundation, water scarcity, and high soil salinity that native woody plants cannot (Busch and Smith, 1995; Shafroth et al., 2002; Pataki et al., 2005). However, the spatial pattern of P. pubescens is inconsistent with competition with T. chinensis. Sites surveyed for temporal changes in vegetative cover did not always transition from sites with P. pubescens to sites dominated by T. chinensis or any one tree species. Furthermore, although soil salinity was not measured at any of the sites surveyed, P. pubescens being killed by soil salinization is unlikely because experimental tests show that it tolerates salinities higher than the levels found along the Rio Grande and Colorado River (Jackson et al., 1990; S. I. Miyamoto et al., in litt.).

Other possible causes of declines in P. pubescens, including climate change, species interactions, and disease, are inconsistent with the observed spatial pattern of decline. Extirpation was not concentrated at lower elevations or lower latitudes, as would be expected if climate change was killing trees by exposing them to conditions outside their range of tolerance. Nor was the extirpation of P. pubescens clustered, as would be expected if there was concurrent spread of a disease or other pest species, or the concurrent decline of a mutualist. Pollinators of P. pubescens are abundant and seed predators are unlikely to be decimating enough seeds to cause the population declines seen in this study. An undiscovered disease, suggested by Anderson (2007), or an unknown interacting species cannot be ruled out, but there is currently no support for either playing a role in the decline of P. pubescens.

The distribution of remaining P. pubescens populations is consistent with human development playing a large role in its disappearance. Trees are still present in the most undisturbed lands but have disappeared most frequently from areas that have been developed for housing. All but 2 of the 18 sites surveyed within federal, state, or local parks still had P. pubescens. The two parks where they were absent were Socorro Nature Area, for which a 1994 trail guide notes P. pubescens along the trail, and Big Bend Ranch State Park, within which I found eight records from 1941 to 1976. The riparian areas surveyed can be ranked in terms of human development as follows: the Salt and Gila rivers are the most disturbed, followed by the lower Colorado River, and last the middle Rio Grande (Lacey et al., 1975; Snyder and Miller, 1992). Prosopis pubescens had disappeared from much of the Salt and Gila rivers by the 1970s (Lacey et al., 1975; Minckley and Clark, 1984) and has only been recorded in the past decade in Phoenix, Arizona. Contrary to prediction; P. pubescens has disappeared from more sites along the Rio Grande than the Colorado River. I hypothesize that this is due to different site properties of these two rivers. Prosopis pubescens is most often found along the banks or "first bottom" of the Colorado River and in the historic, disconnected floodplain or "second bottom" along the Rio Grande (Ohmart et al., 1988). The lack of P. pubescens along the Rio Grande is therefore consistent with human disturbance as a cause, since development is generally higher within the second bottom (Ohmart et al., 1988). Other sites on smaller rivers and at cienagas vary in disturbance on the basis of their isolation and since only 8 of 44 cienegas that historically held P. pubescens were resurveyed; discussing how P. pubescens has fared within them would be premature. However, the only cienegas surveyed that still had P. pubescens were on federally protected lands: within Ash Meadows National Wildlife Refuge, which possibly supports the largest population of P. pubescens, and at Quitobaquito Spring in Organ Pipe National Monument.

Several lines of evidence suggest that river damming and channelization play a secondary role in the extirpation of P. pubescens. First, historical events along the small section of the Colorado River resurveyed correlate well with expected vegetative changes. Altering the flow of rivers affects the soil, water, and other physical characteristics that ultimately change plant communities (Ohmart et al., 1988; Snyder and Miller, 1992; Molles et al., 1998; Shafroth et al., 2002). Communities directly behind the dam will be inundated by water for much of the year, whereas communities in front of the dam will become more xeric. The construction of Parker Dam may have led to the sharp decrease in Populus and Salix downstream, seen in surveys from 1938 and 1960. My surveys show that they are still declining. The Palo Verde Diversion Dam was completed in 1958 and would have raised the river level upstream, which would be expected to cause P. glandulosa numbers to decline. Indeed, this is what resurveys show, but it is not clear why P glandulosa numbers have rebounded recently or why P pubescens numbers have dropped from 1983 to present. The section resurveyed may not be representative of trends along the entire Colorado River. Anecdotally, several groves of P pubescens along the Colorado River were found with their trunks submerged in water and although they appeared healthy, they may not live long under these conditions according to Ohmart et al. (1988). Second, gaps in the range of P. pubescens exist around large reservoirs like Elephant Butte, Lake Mead, and Lake Havasu--areas that may have had populations decimated by rapid flooding. Finally, sites resurveyed within the second bottom of the Rio Grande where P. pubescens is declining or gone have almost all become more xeric, as would be expected if these trees are dying from a lack of water. Because the Rio Grande sites are farther from the riverbank, trees there are expected to be getting less groundwater than those along the Colorado River. Though Prosopis is generally considered a genus capable of high drought tolerance (see Cleverly et al., 1997), there is some evidence that P pubescens cannot survive extreme drought conditions that now exist along dammed rivers (Collier et al., 1997; Smith et al., 1998). The summary of this evidence suggests that P. pubescens may be dying from both long-term inundation above reservoirs, occurring mostly along the Colorado River, and desiccation, occurring mostly along the Rio Grande.

Conclusions--This study compared herbarium records and published vegetation surveys with field surveys to conclude that P. pubescens has had a substantial, recent reduction in range leading to disjunction between populations. Human development is probably the main cause of P. pubescens extirpation, but local flooding and groundwater depletion are also likely contributing factors. Prosopis pubescens is unlikely to go extinct because some very large stands remain in areas that are currently well protected. The most impressive of these is the 23,000 acres of P. pubescens at Ash Meadows National Wildlife Refuge. However, the loss of P. pubescens from bosques may be an indicator of ecosystem-wide problems. Salix and Populus are sensitive to high salinities and low water tables (Jackson et al., 1990) and are mainly found within the first bottom. Prosopis pubescens seedlings are less affected by flood control because seeds are dispersed by animals, are found farther away from the river's edge along the Rio Grande (Campbell and Dick-Peddie, 1964), and are tolerant of higher soil salinity (Jackson et al., 1990) and longer periods of drought (Cleverly et al., 1997). Therefore, Salix and Populus might be expected to be the first species to decline after disturbance, whereas P. pubescens is expected to decline only after serious habitat alterations. These alterations, brought about by human disturbance, may therefore be altering the bosque ecosystem more than has been previously considered (Ohmart et al., 1977; Howe and Knopf, 1991; Snyder and Miller, 1992; Busch and Smith, 1995; Stromberg, 1997; Shafroth et al., 2002; Sher et al., 2002; Pataki et al., 2005). The extirpation of dominant tree species like S. gooddingii, Populus deltoides, P. fremontii, and Prosopis pubescens by human activities is likely to have a cascading impact on riparian ecosystems, which is critical habitat for many species (Franzreb, 1987; Farley et al., 1994).

Connecting disjunct bosque communities will require restoration, the return of natural flood cycles, and reduction of urban growth along natural waterways. Past attempts at vegetation restoration have had mixed success (Anderson and Ohmart, 1982; Hughes, 1993; Anderson, 1998; Barrows, 1998; Taylor et al., 1999); therefore we still have much to learn about how to manage these ecosystems. Natural annual flooding of southwestern riparian areas is important for seed dispersal (Stromberg, 1997), providing nutrients for seed germination, helping seedlings by uprooting competing plants (Stromberg, 1993), and replenishing groundwater supplies for trees (Busch and Smith, 1995; Shafroth et al., 2002). Plans to regularly flood the Colorado River by releasing water from Hoover Dam (Collier et al., 1997) will hopefully prove to be an effective means of restoring and maintaining native plant and animal communities downstream. If so, perhaps similar plans will be drawn up for the Rio Grande and other disrupted waterways. This restoration is not only important for preserving bosque communities through reconnecting disjunct populations, but has also been shown to lead to high revenues from outdoor activities and tourism (Collier et al., 1997; Varady et al., 2001). The loss of screwbean mesquite is another indicator of the impact human disturbance is having on southwestern riparian communities and hopefully can also be an indicator of the return of native bosques in the future.

I thank M. Rosenzweig, J. Bronstein, and the Bronstein lab for comments and advice; G. Dello Russo and two anonymous reviewers for their helpful critique; and S. Trageser and M. Gonzales for help in the field.

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Submitted 2 May 2013.

Acceptance recommended by Associate Editor, Dr. James E. Moore, 26 September 2013.

Steven E. Foldi, Correspondent. sfoldi@email.arizona.edu

Ecology and Evolutionary Biology Department, University of Arizona, Tucson, AZ 85721

Table 1--Sites where Prosopis pubescens was historically recorded,
classified by current status. Sites are broken down by main
riparian systems and classified as "urban" (buildings visible
within 50 m and woody plant cover less than 5%), "farmland" (area
used for grazing or agriculture and woody plant cover less than
5%), "Tamarix dominated" (> 90% cover), or "native vegetation" (>
5% woody plant cover, < 90% Tamarix).

Location                                 Classification

                      Urban   Farmland    > 90%      Native     Total
                                         Tamarix   vegetation

Rio Grande              7        1          3           9        20
Colorado River          6        1          2          19        28
Salt River              1        1          1           0         3
Gila River              6        0          2           0         8
Small river/cienega     4        3          1          14        22
Total                  24        6          9          42        81
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Date:Sep 1, 2014
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