Revista Mexicana de Ciencias Forestales Vol. 12 (67)

Septiembre – Octubre (2021)

Fecha de recepción/Reception date: 5 de agosto de 2020

Fecha de aceptación/Acceptance date: 3 de junio de 2021

_______________________________

1Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias. Campo Experimental Saltillo. México

2Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias. Campo Experimental Zacatecas. México.

3Instituto de Investigaciones en Ecosistemas y Sustentabilidad. Universidad Nacional Autónoma de México, Campus Morelia. México.

*Autor para correspondencia; correo-e: jsaenz@cieco.unam.mx

Resumen

Atriplex canescens es una especie nativa ampliamente distribuida en las zonas semiáridas de Norteamérica, desde el norte de México hasta el oeste de Estados Unidos de América. La presente revisión de la información publicada sobre esta especie durante los últimos 25 años pretende mostrar su taxonomía, distribución geográfica, hábitat, usos actuales y potenciales, así como las amenazas para su hábitat. Los resultados evidenciaron que el uso más amplio de A. canescens es el forrajero, en la alimentación de ganado bovino, caprino y ovino. También, destacó su empleo en la rehabilitación de suelos degradados, la captura de carbono, la prevención de la erosión y la fitorremediación de suelos contaminados por desechos industriales. Además, tiene un amplio potencial en el campo biotecnológico, como control biológico, biocombustible y fuente de genes tolerantes a la sequía y salinidad; asimismo, el consumo de flores, frutos, hojas y raíces de A. canescens ha sido muy importante para las comunidades indígenas. Sin embargo, a pesar de su amplia distribución enfrenta algunas amenazas, como el cambio de uso de suelo, la competencia con especies invasoras y la reducción de la conectividad entre poblaciones naturales. En síntesis, A. canescens es un taxón con una gran diversidad de usos, por lo que es necesario generar conocimiento para su manejo sustentable y conservación.

Palabras clave: Atriplex canescens (Pursh) Nutt., forraje, manejo forestal, biotecnología, restauración ecológica, zonas semiáridas.

Abstract

Atriplex canescens is a native species widely distributed in semi-arid areas of North America, from northern Mexico to the western United States. This review aims to present the information published for the last 25 years on its taxonomy, geographic distribution, habitat, current and potential uses, and threats to its habitat. This review shows that the main use of A. canescens is the production of forage for the feeding of bovine, goat and ovine livestock. Equally prominent is the use of this species in the rehabilitation of degraded soils, carbon sequestration and the prevention of soil erosion, as well as in phytoremediation of soils contaminated by industrial wastes. In addition, A. canescens has a wide potential in the biotechnological field, as biological control, biofuel and source of drought- and salinity-tolerant genes. The consumption of flowers, fruits, leaves and roots of this species has also been important for the indigenous communities. However, despite its wide distribution, this species faces threats, such as land-use change, competition with invasive species and reduction of connectivity among populations. In summary, A. canescens is a multifunctional species, that demands further knowledge for its sustainable management and preservation.

Keywords: Atriplex canescens (Pursh) Nutt., forage, forest management, biotechnology, ecological restoration, semi-arid zones.

Introduction

The semi-arid zones of North America are ecosystems that harbor high biodiversity and provide a wide range of environmental services to human communities (Bradley and Colodner, 2020). They are characterized by limited water resources, extreme temperatures and the recurrence of prolonged droughts (Chambers et al., 2008). The shrub component is the main existing form of plant life, with a predominance of genera such as Larrea, Prosopis, Flourensia, and Atriplex (Granados et al., 2011).

Prominent among the shrub species is Atriplex canescens (Pursh) Nutt., considered a multifunctional taxon due to its wide distribution and importance (Sanderson and McArthur, 2004). A. canescens is perennial, evergreen, ashy or grayish in color, with deep roots and a large number of adventitious roots adapted to absorb water at great depths (Romero and Ramírez, 2003).

Furthermore, A. canescens is an excellent green biomass producer (up to 1.24 kg plant-1) under low rainfall conditions (Echavarría et al., 2009). Therefore, its main use is the production of fodder for livestock feed for grazing in semi-arid areas of the world (Mellado et al., 2006; Allison and Ashcroft, 2011).

However, it has a wide range of current and potential uses, some of which are little known among the scientific community and the managers of its populations. Therefore, the objective of this study was to compile and synthesize the information published during the last 25 years on the taxonomy, distribution, ecology, current and potential uses, as well as threats to the habitat of A. canescens. The following bibliographic databases were consulted: Scopus, Google Scholar, and other sources of information, such as theses and technical brochures.

The information will be very useful for determining the current state of knowledge about this taxon, as well as for disseminating and contextualizing its importance as a multifunctional species.

Traditional and binomial nomenclature

A. canescens is known in Mexico by several names: cenizo, in the states of Chihuahua and Sonora; costilla de vaca, in the states of Zacatecas and Coahuila, and chamizo, in the states of Baja California, Chihuahua and San Luis Potosí (Urrutia et al., 2014). In the United States of America, it is called four-wing saltbush, grey sage brush, and saltbush (Sanderson and McArthur, 2004). According to its etymology, Atriplex corresponds to its ancient Latin name, while canescens is the Latin epithet meaning "hoary, gray" (Dictionary of Botanical Epithets, 2019).

The species was described by F. T. Pursh in 1814 as Calligonum canescens; later, in 1818, T. Nutall repositioned it in the Atriplex Nutt. genus, which is currently accepted. Its synonyms are: Atriplex linearis S. Watson, A. nuttallii S. Watson, Obione canescens (Pursh) Moq., and Pterochiton canescens (Pursh) Nutt. It formerly belonged to the Chenopodiaceae family, but in recent years it was relocated to the Amaranthaceae family (The Plant List, 2020; Tropicos, 2020). Since the original description of the species in 1814, it has undergone modifications at both the genus and the family level; today, the valid scientific name is Atriplex canescens (Pursh) Nutt. Table 1 shows its complete taxonomic classification.

Table 1. Taxonomic classification of Atriplex canescens (Pursh) Nutt.

Source: Tropicos (2020).

Accepted infraspecific taxa include: Atriplex canescens var. canescens, Atriplex canescens var. linearis (S. Watson) Munz, Atriplex canescens var. aptera (A. Nelson) C. H. Hitchc., Atriplex canescens var. garrettii (Rydb.) L.D. Benson, and Atriplex canescens var. gigantea S.L. Welsh & Stutz (Tropicos, 2020).

Distribution of Atriplex canescens

Atriplex canescens is the most widely distributed species of the genus in North America (Sanderson and McArthur, 2004) (Figure 1). In Mexico, it grows in the states of Chihuahua, Coahuila, Nuevo León, San Luis Potosí, Zacatecas, Durango, Tamaulipas, Guanajuato, Querétaro, and Aguascalientes, in the so-called Chihuahuan Desert (Gutiérrez et al., 2012), as well as in Sonora and Baja California, within the Sonoran Desert (Romero and Ramírez, 2003).

Source: Prepared by the authors.

Figure 1. Distribution area of Atriplex canescens (Pursh) Nutt. in Mexico and the United States of America.

In the United States of America, it is located on the Pacific coast in California, Oregon and Washington; in the Mojave Desert in Nevada; in the Sonoran Desert in Arizona; in the Chihuahuan Desert in Colorado, New Mexico and Texas; in the Great Basin of Utah, Wyoming, Idaho, Nebraska, Oklahoma, Kansas, and in certain parts of South Dakota and Montana (Sanderson and McArthur, 2004).

Habitat

A. canescens predominates on soils with a high content of calcium carbonate, phosphorus, potassium, gypsum and salts, and a low content of organic matter and nitrogen (Glenn and Brown, 1998; Granados et al., 2011). It usually grows on Calcisol, Solonchak, and Solonets soils with a silty-sandy, sandy-clay, sandy-gravelly, and sandy-loam texture; on slopes between 1 and 3 % (Saucedo, 1998; Segura et al., 2014), and at altitudes of 0-2 600 m; an average annual rainfall of 100-500 mm, with hot, dry summers and cold winters, and an average annual temperature of 3 – 25 °C (Enríquez et al., 2011; Ogle et al., 2020).

This species forms monodominant stands, or stands associated with shrubs and grasslands, within the desert microphyllous and rosetophyllous scrub, low subspiny scrub, halophytic and open grasslands, and dunes in coastal areas (Enríquez et al., 2011; Granados et al., 2011). These characteristics allow this taxon to adapt to extreme environmental conditions, low nutrient contents, and high salt concentrations; therefore, it is very suitable for establishment in various environments.

Uses of A. canescens

Forage

A. canescens is the most important native forage species in the semi-arid zones of North America drom its characteristics, including: a high crude protein content in the leaves (16–20 %) (Enríquez et al., 2011); high concentrations of calcium (Ca), fiber, fat, and digestible nutrients (Romero and Ramírez, 2003); high forage availability all year round, as it is able to recover its aerial biomass in 100 days if the removal does not exceed 60 % of the foliage (Saucedo, 1998), and its high palatability. Therefore, it represents an important source of food for domestic livestock and wildlife in the semi-arid zones of northern Mexico, the United States of America, North Africa and Southeast Asia (Le Houérou, 2000; Mellado et al., 2006; Allison y Ashcroft, 2011).

The species can be used both in natural populations and in high density plantations (Gutiérrez et al., 2012; Ríos et al., 2012). Its consumption as fodder is considered an alternative to improve the nutritional status of grazing cattle, particularly during the dry season and winter, as well as in critical periods to avoid animal mortality due to lack of feed (Kronberg, 2015).

In northern Mexico, 60 % of the goats are fed with A. canescens (Romero and Ramírez, 2003) and have a productivity of up to 53 kg yr-1 of milk and 7 kg yr-1 of meat (Mellado et al., 2006). In addition, A. canescens results in a higher mass gain than other forage species (e.g. oats), since kids fed with this species have gains of 100 g day-1 versus 80 g day-1 when consuming forage oats (Echavarría et al., 2014).

Yields are also high, ranging between 4.2 and 9.5 t ha-1 of green matter, equivalent to 1.3 - 3.1 t ha-1 of dry matter, in agricultural soils under irrigation (Gutiérrez et al., 2012); while, in sites with a low annual rainfall (166 mm), yields can reach up to 1.8 t ha-1 of dry matter (Echavarría et al., 2014).

For the Zacatecas area, Echavarría et al. (2009) recorded that biomass production averages 1.24 kg of dry matter per plant in a six-year old plantation established on agricultural soil without irrigation and with an average annual rainfall of 407 mm. Enríquez et al. (2011) report that with a plant density of 1 800 individuals ha-1, forage production fluctuates from 3 582 kg ha-1 to 4 955 kg ha-1.

In combination with other forage sources, it improves digestive and productive qualities; for example, mixed with nopal cactus [Opuntia ficus-indica (‎L.‎) ‎Mill.], it reduces water consumption during drought events and doubles the milk production in goats (Urrutia et al., 2014), and the incorporation of oak acorns (Quercus havardii Rydb.) reduces the concentration of tannins and saponins in the rumen, thereby improving the digestive process of cattle (Deeds et al., 2010).

A. canescens is a rustic plant, since it does not require fertilizers or irrigation for its establishment (Petersen and Ueckert, 2005). This makes it a forage resource with high potential for planting ―especially on saline agricultural soils (Enríquez et al., 2011); in regions where the market for goats is important (Gutiérrez et al., 2012), and in pastures degraded by overgrazing (Pinales, 2008)―, alone or in association with grasses and mesquite (Ríos et al., 2012).

Among the North American wildlife that consume the foliage of A. canescens are the white-tailed deer (Odocoeilus virginianus Zimmermann), reindeer (Cervus canadensis Erxleben), pronghorn (Antilocapra americana Ord), bighorn sheep (Ovis canadensis Shaw), and hares (Lepus californicus Gray) (Ogle et al., 2020). In addition, its biomass provides shade and shelter for endangered species, such as the desert tortoise (Gopherus agassizii Cooper) and the mountain plover (Charadrius montanus Townsend) (Grover and De Falco, 1995; Smith and Keinath, 2004).

Given its importance as a forage species that is available green all year round and adaptable to extreme environmental conditions, it should be promoted for livestock feeding in pastures and abandoned agricultural areas; this would represent important savings for livestock producers, especially in places with recurrent droughts.

Restoration of degraded soils

A. canescens has a wide potential for the restoration of degraded soils; therefore, from its great capacity for propagation by seeds and to its growth characteristics, it has been successful in the reconversion of agricultural soils (McLendon et al., 2012) and overgrazed lands (Newman and Redente, 2001), and in the reforestation of abandoned mines (Booth et al., 2002), roadsides, and areas affected by fires (Ogle et al., 2020).

The roots of A. canescens reach up 6 m deep and they help prevent and reduce the process of soil erosion; for this reason, it is considered an important species for restoring vegetation cover (Sanderson and McArthur, 2004; Ogle et al., 2020), as well as for stabilizing steep slopes and mitigating the risk of landslides (Hu et al., 2013).

The ability of A. canescens to grow in sodic saline soils and other ecosystems has made it possible to restore the vegetation cover and facilitate the establishment of native flora, conserving local biodiversity (Newman and Redente, 2001). It also has a high potential for carbon sequestration, capturing up to 5 t year-1 of carbon dioxide in sites with low rainfall and infertile soils (Lailhacar et al., 1995).

The establishment of A. canescens plantations has demonstrated a great capacity to desalinate soils irrigated with brackish groundwater (Flores et al., 2017). In New Mexico, where 75 % of the groundwater is saline, this species has been able to retain such salts as Ca and Mg, thus improving the quality of water for agricultural use (Sarpong et al., 2019).

The characteristics described above make A. canescens an excellent option for use in programs for restoring degraded soils and overgrazed pastures, a situation that is increasingly recurrent in the semi-arid zones of North America.

Remediation and phytoremediation of contaminated soils

A. canescens is used in soil remediation at sites contaminated by mining, with oil and by-products of industrial production in the southwestern United States of America. Its growth on tailings dam substrate stabilizes the chemical residues from mining and prevents their spread through wind and rain (Rosario et al., 2007). Its tolerance to high selenium (Se) and uranium (U) contents allows it to grow on soils irrigated with water from the energy industry, which helps their rehabilitation or decontamination (Baumgartner et al., 2000).

It is also used to reduce the mobility of such contaminants as nitrate (NO3-2), ammonium (NH4+1), and sulfate (SO4-2) generated in uranium mines, thereby eliminating their propagation into the surrounding aquifers (Brestoff et al., 2013).

A. canescens has the ability to retain, recover and extract industrial pollutants from soils with high plutonium (Pu) content and NO3-2 (McKeon et al., 2006; Caldwell et al., 2011). Its biomass is capable of absorbing and removing particles of heavy metals from soils contaminated with cadmium (Cd), chromium (Cr), zinc (Zn), lead (Pb), and copper (Cu) in polluted water (Sawalha et al., 2009).

Its roots can extract NO3-2 from contaminated aquifers (McKeon et al., 2006; Jordan et al., 2008), as well as recover sodium (Na) and phosphorus (P) from wastewater (Howe and Wagner, 1999). This represents a low-cost method for the remediation of soil and water contamination with industrial by-products (Rosario et al., 2007).

Based on the above characteristics, A. canescens has a wide potential for the remediation and phytoremediation of contaminated soils, much more than annual herbaceous plants such as Thlaspi caerulescens J. Presl & C. Presl, Sedum alfredii Hance, and Alyssum murale Waldst. & Kit, or than very complex and costly physicochemical and thermal methods (Delgadillo et al., 2011).

Household consumption

The household use of A. canescens has been very important for the indigenous people of northern Mexico and the southwestern United States of America. The seeds are used in the preparation of flour to make bread; the macerated leaves are used to season food, and the burnt branches, to color tortillas (Beck, 2016). Medicinal use: the roots and flowers are used to relieve insect bites, treat coughs, nasal congestion, headaches and stomach aches (Kuznar, 2001). Other relevant uses are ornamental, as an abrasive, as a cleaner, and as a dye for basketry and textiles (Sinenski, 2013).

Although information is still very scarce, it is mandatory to assess the medicinal and food properties and traditional uses of A. canescens in a systematic way, since this species could prove very useful and beneficial for society if used on an industrial scale.

Biotechnology

A. canescens has a significant role in the biotechnological field; for example, leaf extracts possess secondary metabolites with potential for inhibition of bacteria like Staphylococcus aureus Rosenbach, which causes skin, bone, cardiac and respiratory infections (Castro et al., 2001). Extracts from the seeds are used for the control of the larvae of the common mosquito (Culex quinquefasciatus Say) (Ouda et al., 1998). In addition, its biomass has a large potential as biofuel (Castellanos et al., 2012). Recently, the incorporation of A. canescens genes on soybean that induce tolerance to drought and salinity has been evaluated (Qin et al., 2017; Guo et al., 2019).

It is necessary to continue exploring the potential applications of A. canescens in biotechnology, as this may lead to important advances in bioenergy, agriculture, as well as in pest and disease control.

Threats to the conservation of Atriplex canescens

Natural populations of A. canescens face threats to their utilization and conservation. Overgrazing generates adult shrub mortality, limits natural regeneration of seedlings (Gibbens et al., 2005) and induces the propagation of species such as Larrea tridentata (DC.) Cav. and Prosopis glandulosa Torr., potential competitors of A. canescens (Mata-González et al., 2007).

Cattle have a preference for consuming female flowering plants, which alters flowering patterns and long-term reproductive success (Cibils et al., 2003). A. canescens is vulnerable to invasive exotic species; thus, in southern Texas, it has been displaced by African grass, Eragrostis lehmianna Nees (Leavitt et al., 2010). In addition, lagomorphs consume up to 99 % of the seedlings in A. canescens plantations (Clements and Harmon, 2017).

Urban sprawl is a major disturbance factor in the semi-arid areas of the southwestern United States of America in cities such as Phoenix, Arizona and Los Angeles, California (Bohn et al., 2018). In Mexico, this has been less of a problem in cities with agroindustrial activity, such as Torreón, Coahuila (Ballesteros-Barrera et al., 2007). Expansion of the agricultural frontier and overgrazing of native grasslands constitute the greatest threats in the north of the country (Pool et al., 2014).

Road construction contributes to the fragmentation of the habitat of A. canescens by altering the genetic and ecological connectivity between populations (Ballesteros-Barrera et al., 2007). Expansion of open pit mining concessions in northern Mexico (Téllez and Sánchez, 2018), combined with the long history of this type of mining in the southwestern United States of America (Ingram et al., 2020), can also drastically reduce its habitat.

Climate change will reduce seasonal precipitation in the southwestern United States and northern Mexico, potentially altering the phenological cycle of this species (Cázares et al., 2010). In addition, the expansion of highly flammable exotic grasslands is likely to induce very severe fires and thus generate a high mortality rate of A. canescens (Underwood et al., 2019). Thus, despite the great capacity of this taxon to develop under extreme environmental conditions, it is also very susceptible to changes in habitat, and, therefore, efforts must be made to preserve it.

Conclusions

A. canescens represents an important non-timber forest resource in the semi-arid zones of North America, with a wide variety of current and potential uses, including forage, rehabilitation of degraded and contaminated soils, and with various biotechnological and domestic applications. Although this species is widely distributed, it is threatened by a variety of human activities. Therefore, its wild populations must be preserved, given its multiple uses in the areas where it is naturally distributed, as well as its potential utilization in other parts of the world.

Acknowledgments

The authors are grateful to the Graduate Program in Biological Sciences of the Universidad Nacional Autónoma de México for the facilities to carry out this work.

Conflict of interests

The authors declare no conflict of interest.

Contribution by author

David Castillo Quiroz, Ramón Gutiérrez Luna, Diana Yemilet Ávila Flores and Francisco Castillo Reyes: information search, drafting and review of the manuscript; Jesús Eduardo Sáenz Ceja: information search and drafting of the manuscript.

References

Allison, C. D. and N. Ashcroft. 2011. New Mexico Range Plants. New Mexico State University. Las Cruces, NM, USA. 48 p. https://aces.nmsu.edu/pubs/_circulars/CR374/ (24 de junio de 2020).

Ballesteros-Barrera, C., E. Martínez-Meyer and H. Gadsden. 2007. Effects of land-cover transformation and climate change on the distribution of two microendemic lizards, genus Uma, of northern Mexico. Journal of Herpetology 41 (4): 733-740. Doi: 10.1670/06-276.1.

Baumgartner, D. J., E. P. Glenn, G. Moss, T. L. Thompson, J. F. Artiola and R. O. Kuehl. 2000. Effect of irrigation water contaminated with uranium mill tailings on Sudan grass, sorghum vulgare var. sudanense, and fourwing saltbush, Atriplex canescens. Arid Soil Research and Rehabilitation 14 (1): 43-57. Doi: 10.1080/089030600263166.

Beck, M. 2016. Archaeological signatures of corn preparation in the U. S. Southwest. Journal of Southwestern Anthropology and History 67 (2): 187-218. Doi: 10.1080/00231940.2001.11758454.

Bohn, T. J., E. R. Vivoni, G. Mascaro and D. D. White. 2018. Land and water use changes in the US-Mexico border region, 1992-2011. Environmental Research Letters 12: 114005. Doi: 10.1088/1748-9326/aae53e.

Booth, D. T., J. K. Gores, G. E. Schuman and R. A. Olson. 2002. Shrub densities on pre-1985 reclaimed mine lands in Wyoming. Restoration Ecology 7 (1): 24-32. Doi: 10.1046/j.1526-100X.1999.07103.x.

Bradley, C. M. AND D. Colodner. 2020. The Sonoran Desert. In: Goldstein, M. I. and D. A. DellaSalla (eds.). Encyclopedia of the World´s Biomes. Elsevier. New York, USA. pp. 110-125. Doi: 10.1016/B978-0-12-409548-9.11939-6.

Brestoff, C. J., U. Nguyen, E. P. Glenn, J. Waugh and P. L. Nagler. 2013. Effects of grazing on leaf area index, fractional cover and evapotranspiration by a desert phreatophyte community at a former uranium mill site on the Colorado Plateau. Journal of Environmental Management 114: 92-104. Doi: 10.1016/j.jenvman.2012.09.026.

Caldwell, E., M. Duff, C. Ferguson and D. Coughlin. 2011. Plutonium uptake and behavior in vegetation of the desert southwest: A preliminary assessment. Journal of Environmental Monitoring 13: 2575. Doi: 10.1039/c1em10208g.

Castellanos V., A. E., J. Llano S., M. Esqueda V. y O. Téllez. 2012. Uso de la biodiversidad de las zonas áridas de México como insumos para biodiesel y biocombustibles. In: Castellanos V., A., M. Esqueda V. (eds.). Uso de la biodiversidad para bioenergía y biocombustibles en zonas áridas de México. Universidad de Sonora. Hermosillo, Son., México. pp. 43-64.

Castro F., R., C. A. Meza H., M. R. Contreras Q. y J. Santos G. 2001. Uso de fitoextractos en el control del crecimiento in vitro de bacterias enteropatógenas. Revista Chapingo Serie Zonas Áridas 2 (1): 96-99. https://revistas.chapingo.mx/zonas_aridas/contenido.php?id_articulo=896&doi=0000 (10 de junio de 2020).

Cázares M., J., C. Montaña and M. Franco. 2010. The role of pollen limitation on the coexistence of two dioeciuous, wind-pollinated, closely related shrubs in a fluctuating environment. Oecologia 164: 679-687. Doi: 10.1007/s00442-010-1696-z.

Chambers, J. C., N. Devoe and A. Evenden. 2008. Collaborative management and research in the Great Basin: Examining the issues and developing a framework for action. General Technical Report RMRS-GTR-204. USDA Forest Service. Fort Collins, CO, USA. 66 p. Doi: 10.2737/RMRS-GTR-204.

Cibils, A. F., D. M. Swift and R. H. Hart. 2003. Female-biased herbivory in fourwing saltbush browsed by cattle. Journal of Range Management 56 (1): 47-51. Doi: 10.2458/azu_jrm_v56i1_cibils2.

Clements, C. D. and D. N. Harmon. 2017. Four-wing saltbush (Atriplex canescens) seed and seedling consumption by granivorous rodents. Rangelands 39 (6): 182-186. Doi: 10.1016/j.rala.2017.10.002.

Deeds, B. E., C. B. Scott and R. Brantley. 2010. Feeding shinoak to meat goats improves four-wing saltbush and total intake. The Texas Journal of Agriculture and Natural Resources 23 (1): 1-11. https://txjanr.agintexas.org/index.php/txjanr/article/view/57 (3 de mayo de 2020).

Delgadillo L., A. E., C. A. González R., F. Prieto G., J. R. Villagómez I. y O. Acevedo S. 2011. Fitorremediación: una alternativa para eliminar la contaminación. Tropical and subtropical agroecosystems 14(2):597-612. http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S187004622011000200002&lng=es&tlng=es.

Dictionary of Botanical Epithets. 2019. Acicularifolius-acoroides http://botanicalepithets.net/dictionary/dictionary.5.html (6 de mayo de 2020).

Echavarría C., F. G., A. Serna P., F.A. Rubio A., A. F. Rumayor R., H. Salinas y G. Homero. 2009. Productividad del chamizo Atriplex canescens con fines de reconversión: dos casos de estudio. Técnica Pecuaria en México 47(1)93-106. https://cienciaspecuarias.inifap.gob.mx/index.php/Pecuarias/article/view/1485    (29 de julio de 2021).

Echavarría C., F. G., A. Serna P., M. J. Flores N, G. Medina G., R. Gutiérrez L. y H. Salinas G. 2014. Sistema de producción de forrajes de temporal y pastoreo de cabras, opción para la reconversión productiva. Revista Chapingo Serie Zonas Áridas 14 (1): 29-40. Doi:10.5154/r.rchsza.2015.04.004.

Enríquez C., E., M. A. Parra G. y F. Ramírez M. 2011. Producción y valor nutritivo de forraje de Atriplex en un suelo salino. Biotecnia 13 (2): 29-34. Doi: 10.18633/bt.v13i2.86.

Flores, A. M., M. K. Shukla, B. J. Schutte, G. Picchioni and D. Daniel. 2017. Physiologic response of six plant species grown in two contrasting soils and irrigated with brackish groundwater and RO concentrate. Arid Land Research and Management 31 (2): 182-203. Doi: 10.1080/15324982.2016.1275068.

Gibbens, R. P., R. P. McNeely, K. M. Havstad, R. F. Beck and B. Nolen. 2005. Vegetation changes in the Jornada Basin from 1858 to 1998. Journal of Arid Environments 61: 651-668. Doi: 10.1016/j.jaridenv.2004.10.001.

Glenn, E. P. and J. J. Brown. 1998. Effects of soil salt levels on the growth and water use efficiency of Atriplex canescens (Chenopodiaceae) varieties in drying soil. American Journal of Botany 85 (1): 10-16. Doi: 10.2307/2446548.

Granados S., D., A. Sánchez G., R. L. Granados V. y A. Borja de la Rosa. 2011. Ecología de la vegetación del Desierto Chihuahuense. Revista Chapingo Serie Ciencias Forestales y del Ambiente 17: 111-130. Doi: 10.5154/r.rchscfa.2010.10.102.

Grover, M. C. and L. A. De Falco. 1995. Desert tortoise (Gopherus agassizii): Status-of-knowledge outline with references. General Technical Report INT-GTR-316. USDA Forest Service. Ogden, UT, USA. 134 p. Doi: 10.2737/INT-GTR-316.

Guo, H., L. Zhang, Y. Cui, S. Wang and A. Bao. 2019. Identification of candidate genes related to salt tolerance of the secretohalophyte Atriplex canescens by transcriptomic analysis. BMC Plant Biology 19: 213. Doi: 10.1186/s12870-019-1827-6.

Gutiérrez L., R., D. Rodríguez T., G. Martínez T., C. Aguirre C. y R. A. Sánchez G. 2012. Bancos de proteína para rumiantes en el semiárido mexicano. Folleto técnico Núm. 47. INIFAP. Campo Experimental Zacatecas, Calera de Víctor Rosales, Zac., México. 30 p. http://www.zacatecas.inifap.gob.mx/publicaciones/bancpro.pdf        (8 de mayo de 2020).

Howe, J. and M. R. Wagner. 1999. Effects of pulpmill effluent irrigation on the distribution of elements in the profile of an arid region soil. Environmental pollution 105 (1): 129-135. Doi: 10.1016/S0269-7491(98)00168-7.

Hu, X., G. Brierley., H. Zhu, G. Li, J. Fu, X. Mao, Q. Yu and N. Qlao. 2013. An exploratory analysis of vegetation strategies to reduce shallow landslide activity on loess hillslopes, Northeast Qinghai-Tibet Plateau, China. Journal of Mountain Science 10 (4): 668-686. Doi: 10.1007/s11629-013-2584-x.

Ingram, J. C., L. Jones, J. Credo and T. Rock. 2020. Uranium and arsenic unregulated water issues on Navajo lands. Journal of Vacuum Science and Technology A 38: 031004. Doi: 10.1116/1.5142283.

Jordan, F., W. J. Waugh, E. P. Glenn, L. Sam, T. Thompson and T. L. Thomspon. 2008. Natural bioremediation of a nitrate-contaminated soil-and-aquifer system in a desert environment. Journal of Arid Environment 72: 748-763. Doi:10.1016/j.jaridenv.2007.09.002.

Kronberg, S. L. 2015. Improving cattle nutrition on the Great Plains with shrubs and fecal seeding of fourwing saltbush. Rangeland Ecology and Management 68: 285-289. Doi: 10.1016/j.rama.2015.03.003.

Kuznar, L. A. 2001. Ecological mutualism in Navajo corrals: Implications for Navajo environmental perceptions and human/plant coevolution. Journal of Anthropological Research 57 (1): 17-39. Doi: 10.1086/jar.57.1.3630796.

Lailhacar, S., H. Rivera, H. Silva y J. Caldentey. 1995. Rendimiento de leña y recuperación al corte en diferentes especies y procedencias arbustivas del género Atriplex. Revista de Ciencias Forestales 10(1-2): 85-97.

http://www.revistacienciasforestales.uchile.cl/1995_vol10/n1-2a08.pdf                 (8 de mayo de 2020).

Le Houérou H. N. 2000. Utilization of fodder trees and shrubs in the arid and semiarid zones of West Africa and North Africa. Arid Soil Research and Rehabilitation 14: 101-135. Doi: 10.1080/089030600263058.

Leavitt, D. J., A. F. Leavitt and C. M. Ritzi. 2010. Post-grazing changes of vegetation in Big Bend National Park, Texas: a 50-year perspective. The Southwestern Naturalist 55 (4): 493-500. Doi: 10.1894/DW-123.1.

Mata-González, R., B. Figueroa-Sandoval, F. Clemente and M. Manzano. 2007. Vegetation changes after livestock grazing exclusion and shrub control in the southern Chihuahuan Desert. Western North American Naturalist 67 (1):63-70. Doi: 10.3398/1527-0904(2007)67[63:VCALGE]2.0.CO;2.

McKeon, C., E. P. Glenn, W. J. Waugh, C. Eastoe, F. Jordan and S. G. Nelson. 2006. Growth and water and nitrate uptake patterns of grazed and ungrazed dsesert shrubs growing over a nitrate contamination plume. Journal of Arid Environments 64: 1-21. Doi: 10.1016/j.jaridenv.2005.04.008.

McLendon, T., E. Naumburg and D. W. Martin. 2012. Secondary succession following cultivation in an arid ecosystem: The Owen Valley, California. Journal of Arid Environments 82: 136-146. Doi: 10.1016/j.jaridenv.2012.02.011.

Mellado, M., R. Estrada, L. Olivares, F. Pastor and J. Mellado. 2006. Diet selection among goats of different milk production potential on rangeland. Journal of Arid Environments 66: 127-134. Doi: 10.1016/j.jaridenv.2005.10.012.

Newman, G. J. and E. F. Redente. 2001. Long-term plant community development as influenced by revegetation techniques. Journal of Range Management 54 (6): 717-724. Doi: 10.2458/azu_jrm_v54i6_newman.

Ogle, D. G., L. St. John, D. Tilley and K. Leir. 2020. Plant guide for fourwing saltbush (Atriplex canescens). USDA Natural Resources Conservation Service. Aberdeen, ID, USA. 6 p. https://plants.usda.gov/plantguide/pdf/pg_atca2.pdf        (8 de mayo de 2020).

Ouda, N. A., B. M. Al-Chalabi, F. M. R. Al-Charchafchi and Z. H. Mohsen. 1998. Insecticidal and ovicidal effects of the seed extract of Atriplex canescens against Culex quinquefasciatus. Pharmaceutical Biology 36 (1): 69-71. Doi: 10.1076/phbi.36.1.69.4621.

Petersen, J. L. and D. N. Ueckert. 2005. Fourwing saltbush seed yield and quality: Irrigation, fertilization, and ecotype effects. Rangeland Ecology and Management 58 (3): 299-307. Doi: 10.2111/1551-5028(2005)58[299:FSSYAQ]2.0.CO;2.

Pinales Q., J. F. 2008. Tres arbustivas forrajeras en el norte-centro de Nuevo León. INIFAP. Campo Experimental General Terán. Desplegable Técnico Núm. 8.

General Terán, N. L., México. 6 p. http://www.inifapcirne.gob.mx/Biblioteca/Publicaciones/769.pdf (6 de abril de 2020).

Pool, D. B., A. O. Panjabi, A. Macías D. and D. M. Solhjem. 2014. Rapid expansion of croplands in Chihuahua, Mexico threatens declining North American grasslands bird species. Biological Conservation 170: 274-281. Doi: 10.1016/j.biocon.2013.12.019.

Qin, D., C. Zhao, X. Liu and P. Wang. 2017. Transgenic soybeans expressing betaine aldehyde dehydrogenase from Atriplex canescens show increased drought tolerance. Plant Breeding 136 (5): 699-709. Doi: 10.1111/pbr.12518.

Ríos S., J. C., L. M. Valenzuela N., M. Rivera G., R. Trucios C. y G. Sosa P. 2012. Diseño de un sistema silvopastoril en zonas degradadas con mezquite en Chihuahua, México. Tecnociencia Chihuahua 6 (3): 174-180. http://tecnociencia.uach.mx/numeros/v6n3/Data/Diseno_de_un_sistema_silvopastoril_en_zonas_degradadas_con_mezquite_en_Chihuahua_Mexico.pdf (6 de abril de 2020).

Romero P., J. I. y R. G. Ramírez L. 2003. Atriplex canescens (Purch, Nutt), como fuente de alimento para zonas áridas. Ciencia UANL 6 (1): 85-92. http://eprints.uanl.mx/id/eprint/1462 (6 de abril de 2020).

Rosario, K., S. L. Iverson, D. A. Henderson, S. Chartrand, C. McKeon, E. P. Glenn and R. M. Maier. 2007. Bacterial community changes during plant establishment at the San Pedro River mine tailings site. Journal of Environmental Quality 36: 1249-1259. Doi: 10.2134/jeq2006.0315.

Sanderson, S. C. and E. D. McArthur. 2004. Fourwing saltbush (Atriplex canescens) seed transfer zones. General Technical Report RMRS-GTR-125. USDA Forest Service. Fort Collins, CO, USA. Doi: 10.2737/RMRS-GTR-125.

Sarpong, K. A., A. Amiri, S. Ellis, O. J. Idowu and C. E. Brewer. 2019. Short-term leachability of salts from Atriplex-derived biochars. Science of the Total Environment 688: 701-707. Doi: 10.1016/j.scitotenv.2019.06.273.

Saucedo T., R. A. 1998. Producción de forraje y respuesta a la defoliación del chamizo (Atriplex canescens) durante la primavera. Técnica Pecuaria en México 36 (3): 233-242. https://cienciaspecuarias.inifap.gob.mx/index.php/Pecuarias/article/view/624       (10 de junio de 2020).

Sawalha, M. F., J. R. Peralta V., B. Sánchez S. and J. L. Gardea T. 2009. Sorption of hazardous metals from single and multi-element solutions by saltbush biomass in batch and continuous mode: Interference of calcium and magnesium in batch mode. Journal of Environmental Management 90: 1213-1218. Doi:10.1016/j.jenvman.2008.06.002.

Segura C., M. A., A. Huerta G., M. Fortis H., J. A. Montemayor T., L. Martínez C. y P. Yescas C. 2014. Cartografía de la probabilidad de ocurrencia de Atriplex canescens en una región árida de México. Agrociencia 48: 639-652. https://agrociencia-colpos.mx/index.php/agrociencia/article/view/1108 (8 de mayo de 2020).

Sinenski, R. J. 2013. Risk management strategies and dietary change at the early agricultural village of Las Capas. Tesis de maestría. Northern Arizona University. Flagstaff, AR, USA. 347 p. https://pqdtopen.proquest.com/doc/1493005076.html?FMT=AI (8 de junio de 2020).

Smith, H. and D. A. Keinath. 2004. Species assessment for mountain plover (Charadrius montanus) in Wyoming. USDI Bureau of Land Management. Cheyenne, Wyoming, USA. 53 p. https://www.uwyo.edu/wyndd/_files/docs/reports/speciesassessments/mountainplover-nov2004.pdf (6 de abril de 2020).

Téllez R., I. y M. T. Sánchez S. 2018. La expansión territorial de la minería mexicana durante el periodo 2000-2017: Una lectura desde el caso del estado de Morelos. Investigaciones Geográficas 96. Doi: 10.14350/rig.59607.

The Plant List. 2020. The Plant List, a working list of all plant species.

http://www.theplantlist.org/tpl1.1/record/kew-2665120 (5 de mayo de 2020).

Tropicos. 2020. Missouri Botanical Garden. https://www.tropicos.org/name/7200079 (31de junio de 2020).

Underwood, E. C., R. C. Klinger and M. L. Brooks. 2019. Effects of invasive plants on fire regimes and postfire vegetation diversity in an arid ecosystem. Ecology and Evolution 9 (22): 12421-12435. Doi: 10.1002/ece3.5650.

Urrutia M., J., H. G. Gámez V., S. Beltrán L. y M. O. Díaz G. 2014. Utilización de Atriplex canescens y Opuntia ficus indica en la alimentación de cabras lactantes durante la sequía. Agronomía Mesoamericana 25 (2): 287-296. Doi: 10.15517/AM.V25I2.15431.

All the texts published by Revista Mexicana de Ciencias Forestales –with no exception– are distributed under a Creative Commons License Attribution-NonCommercial 4.0 International (CC BY-NC 4.0), which allows third parties to use the publication as long as the work’s authorship and its first publication in this journal are mentioned.