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1284 MacGregor-Fors et al.- Invasion of saltcedars and native birds
Revista Mexicana de Biodiversidad 84: 1284-1291, 2013
DOI: 10.7550/rmb.33904
Tama-risk? Avian responses to the invasion of saltcedars (Tamarix
ramosissima) in Sonora, Mexico
Respuestas de las aves ante la invasión del pino salado (Tamarix ramosissima) en Sonora,
México
Ian MacGregor-Fors1, Rubén Ortega-Álvarez2, Alfredo Barrera-Guzmán3, Lucero Sevillano4
and Ek del-Val4
1Red de Ambiente y Sustentabilidad, Instituto de Ecología, A.C. Carretera antigua a Coatepec 351, El Haya, 91070 Xalapa,Veracruz, México.
2Iniciativa para la Conservación de las Aves de América del Norte-México, Comisión Nacional para el Conocimiento y Uso de la Biodiversidad,
Liga Periférico-Insurgentes Sur, Núm. 4903, Col. Parques del Pedregal, 14010 México, D. F., México.
3Museo de Zoología Alfonso Herrera, Facultad de Ciencias, Universidad Nacional Autónoma de México, Circuito exterior s/n, 04510 México, D.
F., México.
4Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Campus Morelia. Antigua Carretera a Pátzcuaro 8701, Ex
Hacienda de San José de la Huerta, 58190 Morelia, Michoacán, México.
ekdelval@cieco.unam.mx
Abstract. Although exotic plant invasions are one of the most important components of global change, previous studies
have found some of the alien species to provide resources and/or conditions to native biota. One example of this is
the saltcedar (Tamarix ramosissima). This exotic invasive tree has been related to several dramatic environmental
changes in North America. However, previous studies suggest that they offer resources and conditions for native
biota, such as the threatened southwestern willow flycatcher (Empidonax traillii). In this study, we surveyed avian
communities and bird nests at sites severely invaded by saltcedars, moderately invaded sites, and non-invaded sites
in northwestern Mexico. Our results show that although bird species richness and abundances do not differ among
the studied conditions, species composition did. Also, bird nest density differed among the studied conditions, with
non-invaded sites having the highest functional diversity of nesting birds. We suggest that future studies should gather
natural history and ecological information that allows managing this invasive species correctly both in the USA and
Mexico.
Key words: alien species, bird communities, biodiversity, exotic invaders, northwestern Mexico, species turnover.
Resumen. Las especies invasoras han sido reconocidas como uno de los principales componentes del cambio global;
sin embargo, algunos estudios han encontrado que también pueden proveer servicios o condiciones benéficas para
la biota nativa. Un ejemplo de esta situación lo representa el árbol exótico conocido como pino salado (Tamarix
ramosissima). Este árbol exótico ha estado involucrado con algunos de los cambios dramáticos en las condiciones
ambientales de los ecosistemas ribereños de Norteamérica. Sin embargo, algunos estudios han sugerido que también
ofrece recursos para la biota nativa, en particular para el mosquero saucero (Empidonax traillii). En este trabajo
estudiamos a las comunidades de aves y la abundancia de nidos en sitios con diferentes niveles de invasión del pino
salado (Tamarix ramosissima) en el norte de Sonora, México. Nuestros resultados muestran que a pesar de que la
riqueza y la abundancia de aves no estuvo significativamente influenciada por el nivel de invasión del pino salado,
la composición de especies si lo estuvo. Por otro lado, la densidad de nidos de aves fue diferente dependiendo de
la condición de invasión del sitio, siendo los sitios sin T. ramosissima los que mostraron una mayor diversidad
funcional de nidos. Sugerimos que estudios posteriores recaben información ecológica y de historia natural que permita
establecer planes de manejo para controlar esta especie invasora tanto en México como en los EUA.
Palabras clave: especies exóticas, comunidad de aves, biodiversidad, invasoras exóticas, noroeste de México, recambio
de especies.
Recibido: 09 octubre 2012; aceptado: 21 junio 2013
Revista Mexicana de Biodiversidad 84: 1284-1291, 2013
DOI: 10.7550/rmb.33904 1285
Introduction
The invasion of exotic species is one of the most
important components of global change, posing severe
threats to biodiversity, ecosystem functioning, resource
availability, economy, and even human health (Czech
et al., 2000; IUCN, 2000; Ricciardi et al., 2000). The
establishment of exotic species grows annually along with
their negative effects throughout the globe (Vitousek et
al., 1997). Specifically, the invasion of exotic plants has
been widely studied. Results from previous investigations
show both detrimental effects and positive ones, such as
providing some ecosystems services (Pejchar and Mooney,
2009); however, such positive effects are specific and often
overridden by their costs (Vitousek et al. 1997).
Saltcedars (Tamarix spp.) are Eurasian trees that were
introduced in the 1800’s to semiarid riparian systems in
southern USA and northern Mexico with 2 main purposes:
as wind barriers among crop plots, and as shade providers
for cattle (Brock, 1994). Saltcedar populations increased
dramatically in the 1960’s (Robinson, 1965). Their
establishment has been related to many environmental
alterations, such as river morphology modifications,
increasing soil salinity, displacing native vegetation, and
modifying fire regimes (Dudley et al., 2000; Zavaleta,
2000; Lewis et al., 2003). Since saltcedars covered
extensive areas in the USA, an intensive biological control
program was developed several years ago (USDA, 2005).
As many as 80 000 ha in Colorado, Utah, and Nevada are
now completely cleared from this exotic species thanks to
the use of the saltcedar leaf beetle as a biological control
agent (Diorhabda elongata; De Loach et al. 2009). The
saltcedar leaf beetle was not as successful in Texas due
to climatic mismatches; however, another closely related
species (D. sublinneata) was used. Since 2009, this
leaf beetle has expanded its populations and decimated
saltcedars southward down to Mexico (Zamorano, 2012).
Apart from saltcedar invasion, the environmental
status of rivers in northern Mexico is worrisome. Among
the main alterations, changes in water flow, damming, and
underground water pumping head the list (Zavaleta, 2000).
Altogether, the environmental status of rivers per se and the
presence of aggressive exotic plant species (e.g., saltcedars,
giant reeds-Arundo donax) have generated a complicated
scenario for the wildlife associated to riparian systems,
representing a severe threat for them. Some authors claim
that among other wildlife groups (e.g., insects, reptiles,
amphibians; King, 2005), birds use saltcedars as surrogate
habitat, even for nesting (Hunter et al., 1985; Suckling
et al., 1992; Guertin, 2003; King, 2005; Sogge et al.,
2008). One example of this is the threatened southwestern
willow flycatcher (Empidonax traillii). In fact, Paradzick
(2005) found that southwestern willow flycatchers tend
to select similar habitat traits in cottonwood-willow and
saltcedar habitat patches. However, other studies have
found negative effects of saltcedars on birds, diminishing
species richness and abundance in severely invaded areas
(Anderson et al., 1983; Anderson and Ohmart, 1984; King,
2005), with species-dependent effects (van Riper III et al.,
2008).
Even though saltcedars have invaded many areas
of northern Mexico, few studies have documented their
effects on the native biodiversity of this country (Scott
et al., 2009), and little is known about the threats that
saltcedars pose to Mexican bird communities. Previous
studies carried out in the USA show that saltcedar invaded
areas can support up to 49 bird species; however, its quality
as habitat varies across sites (Sogge et al., 2008). In this
study, we assessed shifts in bird communities associated
to the recent local invasion of saltcedars in northwestern
Mexico (as suggested by Hunter et al., 1985, 1988). For
this, we surveyed bird communities at severely invaded
sites, moderately invaded sites, and non-invaded sites,
contrasting diversity and composition metrics (i.e., species
richness, relative abundance, species turnover). We also
assessed the role that saltcedars play as nesting sites for
birds.
Materials and methods
Study area. This study was carried out in the surroundings
of the Ajos-Bavispe National Forest Reserve in Sonora
(30º40’32.4” N, 109º21’10.9” W), located in northwestern
Mexico, along the banks of the Bavispe river (Fig. 1).
The vegetation in the area is mainly comprised by a
riparian forest, including original tree species, such as Acer
grandidentatum, Alnus oblongifolia, Populus fremontii,
Platanus wrightii, Juglans major, and Fraxinus velutina;
as well as shrubs and lianas, such as Rhus trilobata,
Rosa woodsi, Ceanothus fenleri, Vitis arizonica and Rhus
radicans (Molina-Freaner and Van de Vender, 2010). The
conservation status of riparian vegetation in the Sonoran
Desert is of special concern since there have been many
hydrological exploitation projects that diverted water
flows from most of the region’s major rivers (including
the Bavispe river) by constructing dams and associated
irrigation canals. Inundating vegetation in reservoirs
behind dams and changes in river flows are among the
most severe pressures to threatened plants and nesting
birds in the Mexico-USA borderlands (Zamorano, 2012).
Groundwater pumping for agricultural and domestic
purposes is also severe in the region and has affected
nearly all river valleys leading to ground subsidence,
salinization, and threatening riparian forests in the Sonoran
1286 MacGregor-Fors et al.- Invasion of saltcedars and native birds
desert (Nabham and Holdsworth, 1998).
Bird and nest surveys. We surveyed diurnal breeding birds
from 07:00-11:00 in June 2011 using 5 min point counts
(25 m radius) located at least 250 m apart from each
other to assure survey independence (Ralph et al., 1996).
We used limited-radius point counts for assuring that all
birds recorded were actively using the surveyed area and
not nearby conditions with different habitat attributes, and
to maintain an identical sampled area per point count.
All birds seen or heard using the sampled area (e.g.,
perching, foraging, nesting) were recorded and included
in our analyses.
We established survey sites in 3 habitat conditions
related to saltcedar invasion: 1) severely invaded sites (>
90% saltcedar cover), 2) moderately invaded sites (presence
of saltcedars embedded in native plant communities), and
3) non-invaded sites (absence of saltcedars). Due to the
nature and distribution of these conditions we could not
proceed with a balanced design. Thus, we performed 8
point-counts in severely invaded sites, 3 in moderately
invaded sites, and 11 in non-invaded sites.
For nest surveys, we located a total of 32 sampling
plots near to the point counts. Of them, 12 were located in
severely invaded sites, 5 in moderately invaded sites, and
15 in non-invaded sites. We defined 25 m radius survey
areas at each nest sampling plot where we searched for
nests in all vegetation strata with equal sampling efforts
(20 min, 2 observers). Within each plot, we recorded
all nests found and identified the species that built them
whenever possible.
Habitat characterization. To characterize vegetation traits
in our survey sites, we recorded 13 variables within the
25 m radius where birds were surveyed: 1) tree cover,
2) tree species richness, 3) tree maximum height, 4) tree
minimum height, 5) dominant tree species, 6) shrub cover,
7) shrub species richness, 8) shrub maximum height, 9)
shrub minimum height, 10) herb cover, 11) herb species
richness, 12) herb maximum height, and 13) herb minimum
height.
Analyses. To contrast bird species richness values, we
compared the species richness statistical expectation for
each condition using EstimateS (Colwell, 2008). This
expectation is generated by the repeated re-sampling of
all pooled samples, allowing the statistical comparison of
different habitats/treatments (Gotelli and Colwell, 2001).
To determine if species richness values were statistically
different among the studied conditions, we compared their
84% confidence interval (CI). If their CIs did not overlap,
we considered the data to be statistically different with an
alpha= 0.05 (following Payton et al., 2003; MacGregor-
Fors and Payton, 2013). To assess if bird abundances
differed among habitats, we used a Kruskal-Wallis test. To
assess bird community composition shifts, we used a Bray-
Curtis multivariate cluster analysis (single linkage), based
on the abundance-based version of Bray and Curtis’s (1957)
species turnover index using BioDiversity Pro (McAleece,
1997). This analysis outputs a dendrogram with the single
linkage similarity among the compared conditions. To
assess if habitat traits were related to bird community
richness and abundance, we performed regression trees
using R (R Development Core Team, 2010). Regression
trees allow the interpretation of datasets where complex
nonlinear relationships occur between the set of response
and predictor variables (Deíath and Fabricius, 2000). This
analysis uses binary recursive partitioning to identify
threshold values of a set of predictor variables, which can
be a mix of continuous and categorical variables that are
related to the response variable. Thus, regression trees
identify successive critical values of predictor variables
splitting the response variable in a dichotomous and
hierarchical manner (Palomino and Carrascal, 2007). These
types of trees are analogous to multiple regression models,
specifically those using forward selection of predictor
variables (Crawley, 2007). Finally, we report the number
of nests found in severely, moderately, and non-invaded
Figure 1. Map of study and sampling area in northwestern
Mexico
Revista Mexicana de Biodiversidad 84: 1284-1291, 2013
DOI: 10.7550/rmb.33904 1287
sites, using a Fisher’s exact test to assess differences in the
frequency of nests we could identify. We used this test as
it is most suitable for small sample sizes.
Results
Due to the nature of our sampling design, with
incomparable numbers, we could not contrast bird species
richness expectations using one single comparable
accumulated abundance cut-off, as suggested by Moreno
(2001) and Magurran (2004). Thus, we used 2 abundance
cut-off values, given by the least total abundance in the
less abundant conditions. Bird species richness values
did not show significant differences among the studied
conditions using both cut-off values: 1) 11 individuals
(total abundance recorded at moderately invaded sites):
severely invaded= 8.4 ± 1.4, moderately invaded= 8.0 ±
3.3, non-invaded= 8.4 ± 1.6 computed species, and 2) 31
individuals (total abundance recorded at severely invaded
sites): severely invaded= 16 ± 3.3, non-invaded= 17.3 ± 3.0.
Similarly, relative abundances did not differ significantly
among the studied conditions (individuals / point count:
H3,23= 5.7, p= 0.12). The Bray-Curtis multivariate cluster
analysis revealed that the studied bird communities were
highly different among conditions, regardless of their
closeness, showing low average similarity among them
(~33% similarity). Specifically, the most similar paired
comparison was ‘severely invaded-non-invaded’ (38.1%),
while the most dissimilar was ‘moderately invaded-non-
invaded’ (25.4% similarity). Only 3 of the 13 measured
explanatory variables were considered by the regression
tree analyses for both bird species richness and abundance:
1) tree cover, 2) shrub cover, and 3) tree maximum height.
In both cases (i.e., bird richness, abundance), tree cover
was the variable that explained most of the variation and
was positively related.
We found a total of 43 bird nests in the sampled plots,
of which 49% corresponded to 3 generalist bird species: 1)
Sinaloa wren (Thryothorus sinaloa), 2) common ground-
dove (Columbina passerina), and 3) gila woodpecker
(Melanerpes uropygialis). When we calculated the relative
number of recorded nests per condition (total number of
nests / plot), moderately invaded areas ranked highest (2
nests / plot), followed by severely invades sites (1.4 nests
/ plot), and non-invaded sites (1.06 nests / plot). Although
we could not determine the exact species related to all
recorded nests because they were not active and were
presumably from a prior breeding season (32% unidentified
nests), results from the set of nests that could be identified
indicate a higher number of species nesting in non-invaded
sites (6 species, including unidentified hummingbirds,
verdins-Auriparus flaviceps, vermilion flycatchers-
Pyrocephalus rubinus, and house finches-Haemorhous
mexicanus). On the other hand, severely invaded sites had
nests of 5 identified species, and moderately invaded sites
only had nests of 3 bird species (Table 1). The Fishe’s
exact test revealed significant differences in the number
of species nesting among the 3 studied saltcedar invasion
conditions (p= 0.004).
Discussion
Ecosystem alterations, including the impacts of invasive
exotic species, jeopardize the demographic status of native
species worldwide. In fact, the negative impacts of invasive
exotic species can go beyond the loss of certain species,
impacting several ecological aspects including negative
effects on native species’ populations, communities, biotic
interactions, and even ecosystem processes (Vila et al.,
2011). Moreover, the presence and effects of invasive
species often imply substantial economic losses, severe
sanitary problems, and therefore represent a direct threat to
human health (Simberloff, 1996; Pimentel et al., 2001). In
Mexico, there is a dearth of knowledge about the biology
and ecology of most invasive exotic species. For most
invasive species, we ignore the consequences of their
presence on biodiversity, ecosystem processes, and their
effect on the human communities that directly interact
with them. We do know that there are at least 800 exotic
invasive species in the country and most of them, are
plants (83%; Aguirre-Muñoz et al., 2009). In this sense,
the study of the ecology and impacts of invasive species,
and particularly of the aggressive Tamarix ramosissima
in northern Mexico, are crucial to understand them and
therefore create a solid background that justifies the
implementation of control strategies.
Previous studies show that the response of bird
communities to the invasion of saltcedars can vary.
Although the dominance of saltcedars often reduce bird
species richness and abundance (Anderson et al., 1983;
Anderson and Ohmart, 1984), the presence of this exotic
invasive plant has also resulted in the increase of both bird
species richness and abundance under certain conditions
(Brock, 1994; King, 2005; van Riper III et al., 2008). In
this study, bird species richness and abundance did not
show significant differences in the studied conditions, not
matching any of the previous studies we know of. This
result could be due to several non-exclusive factors, such
as: 1) the time-scale of our study, 2) the recent invasion
of saltcedars in our study area (1970s-1980s) resulting in
a time-lag between the invasion process and the response
of bird communities, 3) the importance of tree cover
as an explanatory variable of bird species richness and
abundance, regardless of the species it is comprised by,
1288 MacGregor-Fors et al.- Invasion of saltcedars and native birds
and 4) a possible landscape configuration that results in
sink-and-source dynamics, with invaded areas having low
habitat quality, and thus, high avian mortality, and non-
invaded areas generating enough individuals to support
similar numbers in all conditions (Hunter et al., 1988).
Recording a similar number of individuals of a similar
number of species in the 3 studied conditions suggests
that saltcedar stands offer suitable conditions for a set of
bird species (as suggested by van Riper III et al., 2008).
However, our bird composition analysis revealed high
dissimilarity among the recorded bird communities (~67%
dissimilarity), showing that the studied conditions offer
resources for different birds, with saltcedars incorporating
novel resources into the landscape (van Riper III et al.,
2008).
Our surveys show that birds are using saltcedars
for nesting when areas are severely invaded, but not in
moderately invaded areas, where birds preferred to nest
on native plant species (e.g., mesquites, cottonwoods,
acacias). This result indicates that plant composition
including native species is crucial for nesting birds,
as birds prefer them over exotic species. We recorded
several common ground-dove nests in severely invaded
sites and none in the other studied conditions. Common
gound-doves are a common generalist species capable
of breeding in diverse habitats throughout the region,
preferring disturbed conditions (Hensley, 1959; Short,
1974; Howell and Webb, 1995). We also recorded 2
Zenaida dove nests and 2 Sinaloa wren nests in severely
invaded sites. As common gound-doves, Zenaida doves
are also a generalists species associated with open and
disturbed areas; while Sinaloa wrens where the most
abundant nester in the study area, with the least number
of nests recorded in severely invaded sites. Interestingly,
only 47% of the recorded nests in severely invaded sites
were constructed on saltcedars. We found a low number
of nests (n= 10) at moderately invaded sites; however,
at this condition none of the nests were constructed on
saltcedars. Not surprisingly, we recorded a higher number
of nesting species pertaining to different functional groups
(i.e., omnivore, insectivore, granivore, nectarivore) at non-
invaded sites. Additionally, we recorded an important
number of Sinaloa wren nests (n= 7) at non-invaded sites.
Among the other species recorded nesting at non-invaded
sites, the vermilion flycatcher was also recorded nesting in
severely invaded sites. This is completely expectable, as
it is a common insectivore species associated to disturbed
areas and known to nest near water sources (Howell and
Webb, 1995). Aside of this species, we recorded 1 gila
woodpecker nest, 1 verdin nest, and 1 house finch nest at
non-invaded sites. Although all these species are common
and nest widely in the study area, we did not record them
nesting in severely invaded sites.
In summary, our results show, for the first time in
saltcedar invaded areas in Mexico, that although bird
diversity values (i.e., species richness, abundance) did
Table 1. Recorded birds nests in the study area
Condition Recorded nests Species (number of nests)
Severely invaded sites 17 Columbina passerina (4)
Zenaida sp. (2)
Hummingbird (1)
Pyrocephalus rubinus (1)
Thryothorus sinaloa (2)
Undetermined (7)
Moderately invaded sites 10 Melanerpes uropygialis (4)
Thryothorus sinaloa (3)
Undetermined (3)
Non-invaded sites 16 Melanerpes uropygialis (1)
Hummingbird (1)
Pyrocephalus rubinus (1)
Thryothorus sinaloa (7)
Auriparus flaviceps (1)
Haemorhous mexicanus (1)
Undetermined (4)
Revista Mexicana de Biodiversidad 84: 1284-1291, 2013
DOI: 10.7550/rmb.33904 1289
not differ among severely invaded, moderately invaded,
and non-invaded sites, species composition varied greatly
with the invasion and degree of dominance of this exotic
invasive plant species, suggesting that invaded and non-
invaded sites offer a different array of resources for
birds. Most interestingly, we found that bird only nest
in saltcedars when the exotic invasive tree is dominant,
while non-invaded sites had a higher amount of nests
pertaining to a wider array of birds, both taxonomically
and functionally. It is noteworthy to underline that we did
not record any threatened bird species in areas invaded by
saltcedars, including the southwestern willow flycatcher,
which is of conservation concern in the USA.
Although our results are quite robust and suggest
a concrete response of birds to saltcedar invasion in
northwestern Mexico, we suggest that future studies gather
multi-taxonomic data in order to generate information that
could aid to develop management plans, precise policy
making, and further actions to diminish, or void, the
ecosystem effects that saltcedar have on recently invaded
systems. We strongly suggest to take into consideration
the role that saltcedars are playing in Mexican ecosystems,
particularly in agroecosystems across Chihuahua and
Sonora in order to avoid social discontent since people
have actively planted them in some areas to increase shade
for cattle and as wind-barriers among agricultural plots.
Acknowledgements
We are most grateful with the personnel of the Ajos-
Bavispe National Preserve, specially the director Juan
Mario Cirett, and our field collaborators Roberto Martínez,
Guadalupe González y Manuel Munguía. The project was
funded by the Conabio-JE004.
Literature cited
Anderson, B. W., R. D. Ohmart and J. Rice. 1983. Avian
and vegetation community structure and their seasonal
relationships in the Lower Colorado River Valley. Condor
85:392-405.
Anderson, B. W. and R. D. Ohmart. 1984. Vegetation
management study for the enhancement of wildlife along
the lower Colorado river. Comprehensive final report to USA
Bureau of reclamation. Boulder City. 97 p.
Aguirre-Muñoz, A. R. and R. Mendoza Alfaro. 2009. Especies
exóticas invasoras: impactos sobre las poblaciones de
flora y fauna, los procesos ecológicos y la economía. In
Capital natural de México, Vol. II: estado de conservación y
tendencias de cambio, R. Dirzo, R. González and I. J. March
(eds.). Conabio, México, D. F. p. 277-318.
Best, L. B. and D. F. Stauffer. 1980. Factors affecting nesting
success in riparian bird communities. Condor 82:149-158
Brock, J. H. 1994. Tamarix spp. (Salt Cedar), an invasive exotic
woody plant in arid and semiarid riparian habitats of western
USA. In Ecology and management of invasive riverside
plants, L. C. Waal, L. E. Child, P. M. Wade and J. H. Brock
(eds.). John Wiley & Sons, Cambdridge. p. 27-44.
Colwell, R. K. 2008. EstimateS: Statistical estimation of species
richness and shared species from samples, version 8.2 http://
purl.oclc.org/estimates; last access: 7.X.2012.
Crawley, M. J. 2007. The R Book. Wiley and Sons, Chichester,
England. 1076 p.
Czech, B., P. R. Krausman and P. K. Devers. 2000. Economic
associations among causes of species endangerment in the
United States. Bioscience 50:593-601.
De’ath, G. and K. E. Fabricius. 2000. Classification and regression
trees: a powerful yet simple technique for ecological data
analysis. Ecology 81:3178-3192.
De Loach, C. J., P. A. Lewis, J. C. Herr, R. I. Carruthers, J.
L. Tracy and J. Johnston. 2003. Host specificity of the
leaf beetle, Diorhabda elongate deserticola (Coleoptera:
Chrysomelidae) from Asia, a biological control agent for
saltcedars (Tamarix: Tamaricaceae) in the Western United
States. Biological Control 27:117-147.
De Loach, C. J., A. E. Knuston, P. J. Moran, J. H. Everitt, G. J.
Michels, M. A. Muegge, C. W. Randal, T. G. Fain, M. P.
Donet and C. M. Ritzi. 2009. Progress on biological control
of saltcedar in the Western U.S.: Emphasis-Texas 2004-
2009. USDA-ARS, Texas. 67 p.
Dudley, T. L., C. J. De Loach, J. Lovich and R. I. Carruthers.
2000. Saltcedar invasion of western riparian areas: impacts
and new prospects for control. Transactions 65th North
American Wildlife and Natural Resources Conference. 24-
28 March 2000, Chicago. p. 345-381.
Ellis, L. M. 1995. Bird use of saltcedar and cottonwood vegetation
in the middle Rio Grande Valley, New Mexico. Journal of
Arid Environments 30:339-349.
Gotelli, N. J. and R. K. Colwell. 2001. Quantifying biodiversity:
procedures and pitfalls in the measurement and comparison
of species richness. Ecology Letters 4:379-391.
Hausner, V. H., N. G. Yoccoz, K. Strann and R. A. Ims. 2002.
Changes in bird communities by planting non-native spruce
in coastal birch forests of northern Norway. Ecoscience
9:470-481.
Hensley, M. 1959. Notes on the nesting of selected species of
birds of the Sonoran desert. Wilson Bulletin 71:86-92.
Hinojosa-Huerta, O. M., H. Iturribarría-Rojas, Y. Carrillo-
Guerrero, M. de la Garza-Treviño and E. Zamora-Hernández.
2004. Bird conservation plan for the Colorado river delta.
Pronatura Noroeste, Sonora. 70 p.
Howell, S. N. G. and S. Webb. 1995. A guide to the birds of
Mexico and northern Central America. Oxford University
Press, Oxford. 1010 p.
Hunter, W. C., R. Ohmart and B. Anderson. 1988. Use of exotic
saltcedar (Tamarix chinensis) by birds in arid riparian
systems. Condor 90:113-123.
Hunter, W.C., B. W. Anderson and R. D. Ohmart. 1985. Summer
avian community composition of Tamarix habitats in three
1290 MacGregor-Fors et al.- Invasion of saltcedars and native birds
southwestern desert riparian systems. In Riparian ecosystems
and their management: reconciling conflicting uses, R. R.
Johnson, C. D. Ziebell, D. R. Patron, P. F. Folliort and R. H.
Hamre (eds.). Gen. Tech. Rep. RM-120, U.S. Department of
Agriculture, Fort Collins. p. 128-143.
IUCN (International Union for Conservation of Nature). 2000.
Guidelines for the prevention of biodiversity loss caused by
alien invasive species. Fifth Meeting of the Conference of
the Parties to the Convention on Biological Diversity, 15-26
May 2000. Nairobi, Kenya.
King, M. A. 2005. New habitats for old: Tamarisk-dominated
riparian communities and marshes in the Grand Canyon. UC
Davis, CA. https://www.geology.ucdavis.edu/~shlemonc/
html/trips/Grand%20Canyon%20web/html/reports/PDFs/
King.pdf; last access: 7.X.2012.
Lewis, P. A., C. J. De Loach, A. E. Knutson, J. L. Tracy and T.
Robbins. 2003. Biology of Diorhabda elongata deserticola
(Coleoptera: Chrysomelidae), an Asian leaf beetle for
biological control of saltcedars (Tamarix sp.) in the United
States. Biological Control 27:101-116.
MacGregor-Fors, I. and M. E. Payton. 2013. Contrasting
diversity values: Statistical inferences based on overlapping
confidence intervals. PLoS One 8:e56794.
Magurran, A. E. 2004. Measuring biological diversity. Blackwell
Publishing, Oxford. 254 p.
McAleece, N. 1997. BioDiversity Professional. http://
www.sams.ac.uk/peter-lamont/biodiversity-pro/
?searchterm=biodiversity%20pro; last access: 7.X.2012.
Molina-Freaner, F. E. and T. R. Van de Vender. 2010. Diversidad
biológica de Sonora. UNAM-Conabio, México, D. F.
496 p.
Moreno, C. E. 2001. Métodos para medir la biodiversidad. M&T-
Manuales y Tesis SEA, Zaragoza, España. 84 p.
Nabhan, G. P. and A. R. Holdsworth. 1998. State of the Sonoran
Desert Biome: uniqueness, biodiversity, threats and the
adequacy of protection in the Sonoran Bioregion. Wildlands
project. Tucson. 81 p.
Palomino, D. and L. M. Carrascal. 2007. Threshold distances to
nearby cities and roads influence the bird community of a
mosaic landscape. Biological Conservation 140:100-109.
Paradzick, C. E. 2005. Southwestern willow flycatcher habitat
selection along the Gila and Lower San Pedro rivers, Arizona:
vegetation and hydrogeomorphic considerations. Msc thesis,
Arizona State University. Tempe, Arizona, 172 p.
Payton, M. E., M. H. Greenstone and N. Schenker. 2003.
Overlapping confidence intervals or standard error intervals:
What do they mean in terms of statistical significance?
Journal of Insect Science 3:34
Pejchar, L. and H. A. Mooney. 2009. Invasive species, ecosystem
services and human well-being. Trends in Ecology and
Evolution 24:497-504.
Pimentel, D., S. McNair, J. Janecka, J. Wightman, C. Sommonds,
C. O’Connell, E. Wong, L. Russel, J. Zern, T. Aquino and
T. Tsomondo. 2001. Economic and environmental threats
of alien plant, animal and microbe invasions. Agriculture,
Ecosystems and Environment 84:1-20.
R Development Core Team. 2010. R: A language and environment
for statistical computing. R Foundation for Statistical
Computing, Vienna. http://www.R-project.org; last access:
7.X.2012.
Ralph, C. J., G. R. Geupel, P. Pyle, T. E. Martin, D. F. DeSante
and B. Milá. 1996. Manual de métodos de campo para el
monitoreo de aves terrestres. U.S. Department of Agriculture,
Albany, California. 44 p.
Ricciardi, A., W. W. M. Steiner, R. M. Mack and D. Simberloff.
2000. Toward a global information system for invasive
species. BioScience 50:239-44.
Robinson, T. W. 1965. Introduction, spread and areal extent of
saltcedar (Tamarix) in the western states. USA Geological
Survey Professional Paper 491-A. U.S. Government Printing
Office, Washington, D.C.
Scott, M. L., P. L. Nagler, E. P. Glenn, C. Valdes-Casillas, J.
A. Erker, E. W. Reynolds, P. B. Shafroth, E. Gómez-Limón
and C. L. Jones. 2009. Assessing the extent and diversity
of riparian ecosystems in Sonora, Mexico. Biodiversity and
Conservation 18:247-269.
Short, L. L. 1974. Nesting of Southern Sonoran birds during the
summer rainy season. Condor 76:21-32.
Simberloff, D. 1996. Impacts of introduced species in the United
States. Consequences 2:13-22.
Sogge, M. K., S. J. Sferra and E. H. Paxton. 2008. Tamarix
as habitat for birds: implications for riparian restoration
in the Southwestern United States. Restoration Ecology
16:146-154.
Stromber, J. C., M. K. Chew, P. L. Nagler and E. P. Glenn.
2009. Changing perceptions of change: the role of scientists
in Tamarix river management. Restoration Ecology
17:177-186.
Strong, T. R. and C. E. Bock. 1990. Bird species distribution
patterns in riparian habitats in Southeastern Arizona. Condor
92:866-885.
Suckling, K., D. Hoganand and R. D. Silver. 1992. Petition
to list the southwest willow flycatcher Empidonax traillii
extimus as a federally endangered species. Letter to the
Secretary of the Interior. January 25, 1992. Luna, New
Mexico.
USDA (United States Department of Agriculture). 2005.
Program for biological control of saltcedar (Tamarix spp.)
in thirteen states. http://www.aphis.usda.gov/plant_health/
ea/downloads/salteafonsi.pdf; last access: 7.X.2012.
Van Horne, B. 1983. Density as a misleading indicator of habitat
quality. Journal of Wildlife Management 47:893- 901.
Van Riper III, C., K. L. Paxton, C. O’Brien, P. B. Shafroth and
L. J. McGrath. 2008. Rethinking Avian response to Tamarix
on the Lower Colorado River: a threshold hypothesis.
Restoration Ecology 16:155-167.
Vila, M., J. L. Espinar, M. Hejda, P. E. Hulme, V. Jarosik, J. L.
Maron, J. Perlg, U. Schaffner, Y. Sun and P. Pysek. 2011.
Ecological impacts of invasive alien plants: a meta-analysis
of their effects on species, communities and ecosystems.
Ecology Letters 14:702-708.
Vitousek, P. M., C. M. D’Antonio, L. L. Loope, M. Rejmánek,
Revista Mexicana de Biodiversidad 84: 1284-1291, 2013
DOI: 10.7550/rmb.33904 1291
R. Westbrooks. 1997. Introduced species: a significant
component of human-caused global change. New Zealand
Journal of Ecology 21:1-16.
Zamorano, P. 2012. Monitoring of the distribution of the beetle
(Diorhabda sublineata) released as biological control of
saltcedar (Tamarix spp.) on the banks of the Rio Grande
and Rio Conchos. Weeds Across borders Meeting 2012.
Cancún, México. http://www.weedcenter.org/wab/2012/
sp/docs/Session%207/6%20Zamorano-25abr12.pdf; last
access: 7.X.2012.
Zavaleta, E. 2000. The economic value of controlling and
invasive shrub. Ambio 29:462-467.
