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Introduction
Natural Protected Areas (NPA) are one of the most important Mexican administrative tools within the strategy for the conservation of in situ biodiversity (CONABIO; 2016). These areas are established with the objective of conserving or preserving representative extensions of the most important and well conserved natural ecosystems of the country (Maass et al., 2010). The General Law of Ecological Balance and Environmental Protection indicates that each NPA must have a Management Program (MP), that guides and regulates activities realized in its interior and nearby areas, and have the record of species inhabiting it (DOF, 2018). However, many NPA do not have systematic monitoring, causing a lack of information on its diversity (Pinkus et al., 2014). The Protected Area of Flora and Fauna from Santa Elena Canyon (PAFFSEC) houses or is shelter to between 85 % and 93 % of flora and fauna species, representative of the Chihuahua Desert; since this NPA was decreed (November 7th, 1994), conserving its biodiversity by applying alternatives that allow sustainable exploitation of resources has been a priority (CONANP, 2013). Riparian zones, due to their ecology, facilitate the establishment of biological groups, promote diversity and function as biological corridors (Meave et al., 1991; Granados-Sánchez et al., 2006; Free et al., 2015; Hamilton et al., 2015; Meli et al., 2015). Inside the PAFFSEC, riparian zones are established in San Antonio and San Carlos streams and in Rio Grande (river) (CONANP, 2013). The objective of this work was to record species of birds (B), land mammals (LM), fish (F) and riparian vegetation (RV), and generate information on riparian zones specific to the PAFFSEC in order to elaborate and apply strategies for the conservation and management of its natural resources.
Material and Methods
Area of study
The PAFFSEC is located in the municipalities of Manuel Benavides and Ojinaga in the state of Chihuahua, between the extreme geographical coordinates northwest 29° 25’ 53.08” N, 104° 14’ 24.56” W and southeast 28° 46’ 53.69” N 103° 31’ 56.20” W; with altitudes ranging from 575 to 2401 masl and has an extension of 277 thousand hectares. Climate is arid desert, characterized for annual average temperatures ranging between 18 and 22 ºC and precipitations from June to September (CONANP, 2013). Three riparian locations within the PAFFSEC were chosen: San Carlos Canyon (SCC) located over San Carlos and Nuevo Lajitas (NL) streams and San Antonio Canyon (SAC) located over San Antonio stream (Figure 1). These locations were chosen among 10 that were established in 2014, as strategic spots for monitoring water quality in the NPA (C.C.A., 2014), in addition to the lack of information on biological groups and the importance of ecosystemic health of these locations with respect to the area in general. The RV in the PAFFSEC is characterized by the presence of a shrubby stratum mainly composed of native reed Phragmites australis ((Steudel) Trinius, 1840), mule fat Baccharis salicifolia (Nutt, 1840), honey mesquite Prosopis glandulosa (Torrey, 1827), netleaf hackberry Celtis reticulata (Torr, 1824) and an arboreal stratum constituted by poplars Populus (Linnaeus, 1753) and willows Salix (Linnaeus, 1753); this association does not constitute a type of defined vegetation, since it usually mixes with elements from surrounding types of vegetation (Ruiz, 2010 and CONANP, 2013). In preliminary records of fauna in the PAFFSEC, 53 species of amphibians and reptiles, 209 of birds and 69 of mammals are cited (CONANP, 2013).
For Birds monitoring
The no fixed-radius count point´s method was used, where species and number of individuals observed during a period of 10 minutes were recorded (Hutto et al., 1986; Ralph et al., 1996). Counts were realized from 06:00 to 09:00 and from 15:00 to 18:00 with binoculars Bushenell © (12X42); species were photographed (Canon PowerShot SX420 IS) and taxonomically identified in the laboratory according to Kaufman (2005).
For land mammals sampling
Direct and indirect methods were used: 20 Sherman traps (Sherman Traps©) were placed in December 2017 and 40 in April, July and December 2018. From these, halve of each were placed on each side of the streams, in transects of variable length with a regular distance of 10 m between them. These traps were baited with oat flakes, activated at 18:00 and checked at 06:00, during two consecutive nights. The captured samples were photographed (Canon EOS 1100D/EOS Rebel T3 12.6X) (Ceballos-González and List, 2011). In each study area, one (December 2017), two (April 2018) and three (July and December 2018) trail-cams (Muddy Outdoors © and Cuddeback) were placed, where evidences were observed (footprints, excreta and trails) and in places suggested by the PAFFSCE’s technicians. Traps were placed 50 cm above ground, fixed onto a vertical surface and baited with a combination of sardine and rotten egg (Arroyo et al., 2013; Cruz-Jácome et al., 2015). Cameras remained active for seven days during field work. Specimens that were photographed and captured were taxonomically identified based on the classifications of Anderson (1972), Burt and Grossenheider (1980), Bowers et al. (2004) and Reid (2006). Lastly, two onekilometer transects were established (one on each side of the stream, following its natural flow) searching for footprints and scats which were photographed and collected for their later identification according to Aranda (2012).
Fish sampling
Was manual in shallow parts of the streams and with fishing spoon net with a beam of light of 0.3 cm in the deep parts; this fishing net was used by “sweeping” the depth of the stream from the center to the shore or over the aquatic vegetation with quick movements (Espinosa and Salinas, 2014). The collected samples were photographed (Canon PowerShot SX420 IS) and posteriorly released; they were taxonomically identified in the laboratory based on De la Maza-Benignos and Frías-García (2015).
For riparian Vegetation Sampling
Two 100 m interception lines were realized (one on each side) of the first terrace of the stream channel edge (Guerra, 2002); species were recorded, photographed (Canon PowerShot SX420 IS) and identified in the laboratory based on Rzedowski (2006).
Data analysis
A database was created, in which the total number of species in riparian zones was determined; the nomenclature authority for fauna was obtained from Langer (1979), Ramírez-Pulido et al. (2014), ITIS (2019), and of flora in Tropicos (2019); the category of risk was determined according to NOM-059-SEMARNAT-2010 standard (T: threatened; E: Probably extinct in the wild; D: endangered; Pr: subject to special protection) (SEMARNAT, 2010); the status of vulnerability was assigned according to the Red List of Threatened Species of the International Union for Conservation of Nature (IUCN) (CR: critically endangered; EN: endangered; DD or NA: deficient data; LC: least concern; NT: near threatened; VU: vulnerable) (IUCN, 2019); the trophic guild of land mammals and birds was according to González-Salazar et al. (2014). The type of dispersion of plants was defined based on Baskin and Baskin (1973), Armesto and Rozzi (1989), Milton (1998), Rojas-Aréchiga and Vázquez-Yanes (2000), Jurado et al. (2001), Pessarakli (2002), DiTomaso and Healy (2003), Dauer (2007), Austin (2010), Flores et al. (2011), Les (2017), CABI (2019), CONABIO (2019), FEIS (2019), Flora of North America (2019), Red de Herbarios del Noroeste de México (2019), SEINet (2019), Southwest Desert Flora (2019) and Tropicos (2019). The register of invasive species in riparian zones was specified based on the portal of Enciclovida (CONABIO, 2016).
Results and Discussion
The records of flora and fauna species was distributed into 34 orders, 76 families and 138 genera (Table 1). In accordance with NOM-059-SEMARNAT-2010 standard (SEMARNAT, 2010), seven species were found to be threatened, three endangered, two probably extinct in the wild and 11 subject to special protection. In the case of IUCN Red List of Threatened Species (IUCN, 2019), one near threatened species was recorded, 114 in least concern and one classified as vulnerable. Six invasive species were identified (CONABIO, 2016).
In SCC, 83 species were recorded (B: 29, LM: 12, F: 1, RV: 41), in NL 92 species (B: 43, LM: 18, F: 2, RV: 29) and in the SAC, 92 species as well (B: 48, LM: 16, F: 1 and RV: 27).
Table 1 Biological records of riparian areas of the Protected Area of Flora and Fauna from Santa Elena Canyon.
| Biological groups | Birds | Land mammals | Fish | Vegetation | Total | |
|---|---|---|---|---|---|---|
| Orders | 12 | 4 | 1 | 17 | 34 | |
| Families | 33 | 13 | 2 | 27 | 76 | |
| Genera | 57 | 24 | 2 | 55 | 138 | |
| Species | 73 | 24 | 2 | 67 | 166 | |
| Risk status* | 17 | 5 | 1 | - | 23 | |
| Invasive species** | 1 | 2 | 1 | 2 | 6 | |
| Vulnerable status*** | 72 | 24 | 2 | 18 | 116 |
According to *NOM-059-SEMARNAT-2010 (SEMARNAT, 2010); **Enciclovida (CONABIO, 2016); *** IUCN Red List of Threatened Species (IUCN, 2019).
Birds
This biological group was the most representative with 73 species, distributed in 12 orders, 33 families and 57 genera. The most represented families were Tyrannidae (eight species), Cardinalidae (seven species) and Passerellidae (six species). According to the NOM059-SEMARNAT-2010 standard (SEMARNAT, 2010), 17 species were found in a risk category: two threatened, three in risk of extinction, two probably extinct in the wild and 10 subject to special protection. In accordance with the IUCN Red List of Threatened Species (IUCN, 2019), 71 species were in least concern and one near threatened: Loggerhead Shrike Lanius ludovicianus (Linnaeus, 1766). A total of 48 % (n=35) of the species were insectivore. From bird species identified in this study, 11 were not included in the MP of the area, among them, the house sparrow Passer domesticus (Linnaeus, 1758) which is also considered as an invasive species (CONABIO, 2016). In SAC, 48 bird species were recorded, 43 in NL and 29 in SCC (Appendix 1). The records of these species concur with studies at riparian areas in southern United States of America located in the Chihuahua Desert: Szaro and Jakle (1985) registered 41 species in a riparian zone in the Arizona desert, U.S.A., of which 24 were shared with this study; Ellis (1995), reported 45 species of birds associated to Rio Grande river in New Mexico, U.S.A., of which 19 concurred with this work; Texas Parks and Wildlife (2002) registered 25 species in Rio Grande corridor which coincided with this study. Garza de León et al. (2007), in the list of avifauna of the state of Coahuila, mentioned 30 critical species, including three (Harris’s hawk Parabuteo unicinctus (Temminck, 1824), mallard Anas platyrhynchos (Linnaeus, 1758) and orchard oriole Icterus spurius (Linnaeus, 1766)) riparian birds. The National Commission of Protected Natural Areas (CONANP) reported 69 species when monitoring grassland birds in the Protected Area de of Flora and Fauna from Maderas del Carmen (PAFFMC), a contiguous area to the PAFFSEC (CONANP, 2013b); of these species, 11 were considered as indicators of habitat quality, of which seven coincided with this study: northern mockingbird Mimus polyglottos (Linnaeus, 1758), scaled quail Callipepla squamata (Vigors, 1830), white-crowned sparrow Zonotrichia leucophrys (Forster, 1772) mourning dove Zenaida macroura (Linnaeus, 1758), blue grosbeak Passerina caerulea (Linnaeus, 1758), summer tanager Piranga rubra (Linnaeus, 1758) and the black-throated sparrow Amphispiza bilineata (Cassin, 1850), being P. rubra a new sighting for the PAFFSEC.
CONANP registered in the PAFFMC five (zonetailed hawk Buteo albonotatus (Kaup, 1847) Eurasian siskin Spinus pinus (Wilson, 1810), eastern phoebe Sayornis phoebe (Latham, 1790), American robin Turdus migratorius (Linnaeus, 1766), American bushtit Psaltriparus (Bonaparte, 1850)) of the 12 missing taxa in the PAFFSEC (CONANP, 2013a); and one (Cassin’s kingbird Tyrannus vociferans (Swainson, 1826)) in the Protected Area of Flora and Fauna from Ocampo (PAFFO) (CONANP, 2015). The presence of Lucy’s warbler Leiothlypis luciae (Cooper, 1861) coincides with Powell and Steidi (2015), who performed a study in mountain riparian areas at the south of Arizona and with Texas Parks and Wildlife (2002) in Rio Grande corridor, who also registered gray hawk Buteo plagiatus (Schlegel, 1862) and golden-fronted woodpecker Melanerpes aurifrons (Wagler, 1829). The record of willow flycatcher Empidonax traillii (Audubon, 1828) coincided with Szaro y Jakle (1985) and warbling vireo Vireo gilvus (Audubon, 1844) with Ellis (1995).
The record of the larger proportion of insectivore birds was related to Guevara et al. (2008), who mentioned that riparian zones constituted a fundamental element for some insectivore and migratory birds.
The presence of P. domesticus invasive species coincided with Wauer (1996) and National Park Service (2018), whom reported it in Big Bend National Park, a contiguous area to the north of PAFFSEC. Loope et al. (1988) documented this species as invasive since 1984 in five natural reserves of arid zones in U.S.A. Rosenber et al. (1987) did not associate this species with riparian areas. While Peterson (1990) and Chávez-Zichinelli et al. (2010) associated it with urban zones, which in our study may be related to human settlements near study areas.
Land mammals
Species found in categories of risk according to NOM-059-SEMARNAT-2010 standard were: Texas antelope squirrel Ammospermophilus interpres (Merriam, 1890), Ring-tailed cat Bassariscus astutus (Lichtenstein, 1830), Merriam’s kangaroo rat Dipodomys merriami (Mearns, 1890), American badger Taxidea taxus (Schreber, 1778) and the Kit fox Vulpes macrotis (Merriam, 1888) as threatened (SEMARNAT, 2010). In the IUCN Red List of Threatened Species (IUCN, 2019) were 23 species in least concern and one (Barbary sheep Ammotragus lervia (Pallas, 1777)) as vulnerable. The greater proportion (29 %: n=7) of LM were herbivorous. Species identified as invasive were A. lervia and the wild boar Sus scrofa (Linnaeus, 1758) (CONABIO, 2016). Based on the MP of the PAFFSEC (CONANP, 2013), the species A. interpres and Spilogale (Gray, 1865) were not included in this biological register, therefore this species was the first record of said taxa in the PAFFSEC.
In SCC, 12 species were registered, 18 in NL and 16 in SAC (Appendix 2). Anderson (1972) and López-González and García-Mendoza (2012) reported 22 of the 24 species identified in this study in riparian zones in the south of U.S.A., being invasive the remaining two. Frey (2014) enlisted 90 mammals (land and flying) in the riparian zones of the Gila river in New Mexico, U.S.A.: 21 LM coincided with those identified in this work, except A. inerpres and the two previously indicated invasive species. Small mammals present in this study coincided with Anderson et al. (2000), Falck et al. (2014) and Hamilton et al. (2015), who reported Dipodomys (Gray, 1841), Mustela (Linnaeus, 1758), Neotoma (Say and Ord, 1825), Peromyscus (Gloger, 1841) and Reithrodontomys (Giglioli, 1874) genera in riparian zones of the Chihuahua Desert. The presence of Chaetodipus (Merriami, 1889) and Sylvilagus (Gray, 1867) coincided with Anderson (1994), who reported them in riparian zones of Arizona, U.S.A. The new records of A. interpres and Spilogale genus for the PAFFSEC coincided with the list of species of contiguous NPA to this area (PAFFMC and PAFFO) (CONANP, 2013a; CONANP, 2015).
The proportion of herbivorous LM, related to the one of other trophic guilds, is of great importance, since the presence of herbivores in riparian zones plays an essential role on the structure and spatial distribution of vegetal communities (Rabeil, 2007).
Regarding the two invasive species registered (A. lervia and S. scrofa), the Commission for Environmental Cooperation (C.C.A., 2014a) and CONANP (2013) mentioned that they constitute a threat for native species. The Ministery of Environment and Natural Ressources and CONANP promoted supports for the “Fortalecimiento al Control de chivo berberisco (A. lervia)” in the PAFFSEC and for the “Programa de Atención y Manejo del cerdo asilvestrado (S. scrofa) in NPAs contiguous to this area (PAFFMC and PAFFO) (CONANP, 2019).
Fish
This biological group was the least represented with two species comprised in one order, two families and two genera. The roundnose minnow Dionda episcopa (Girard, 1856) is subject to special protection according to NOM-059-SEMARNAT-2010 standard (SEMARNAT, 2010) and was present in the three riparian zones of study. The plains killifish Fundulus zebrinus (Jordan and Gilbert, 1883) was found only in NL and was considered as invasive, according to Enciclovida (CONABIO, 2016) (Appendix 3). Both species were of least concern according to IUCN Red List of Threatened Species (IUCN, 2019) and were absent in the MP of the PAFFSEC. De la Maza-Benignos and FríasGarcía (2015) reported six species within the PAFFSEC; nevertheless, the presence of two species was recorded in this work. It could be due to the fact that this work was restricted to three riparian areas into the PAFFSEC. Lozano et al. (2009) mentioned F. zebrinus as an invasive species of the aquatic systems in northern Mexico and D. episcopa as an endemic species.
Riparian vegetation
This biological group was represented by 17 orders, 27 families and 67 species; of which none was in category of risk according to NOM-059-SERMARNAT-2010 standard (SEMARNAT, 2010); 18 species in low concern according to the IUCN Red List of Threatened Species (IUCN, 2019), among which were: Hamatocactus hamatacanthus (Knuth, 1936), cane cholla Cylindropuntia imbricata (Knuth, 1935), cardinal flower Lobelia cardinalis (Linnaeus, 1753) and spikesedge Eleocharis obtuse (Schult, 1824). Forty-eight percent of species (n=32) presented endozoochory. The horseweed Erigeron canadensis (Linnaeus, 1753) and the saltcedar Tamarix ramosissima (Ledebour, 1829) were identified as invasive species according to Enciclovida (CONABIO, 2016). In the MP of the PAFFSEC (CONANP, 2013) 18 taxa were not included, constituting the first record of these species in the area. The zone with a greater register of species was SCC with 41 species, followed by NL with 29 species and lastly SAC with 27 species (Appendix 4).
Regarding RV, the presence of characteristic genus like Populus (Linnaeus, 1753), Salix (Linnaeus, 1753) and Prosopis (1767) was similar to the one described by Fleishman et al. (2003) and Merritt and Bateman (2012) in riparian areas in desert ecosystems. Of the 18 taxa registered in this study and not included in the MP of the PAFFSEC, CONANP recorded four (broom snakeweed Guierrezia sarothrae ((Pursh) Britton and Rusby, 1887), saddlebush Mortonia sempervirens (Gray, 1852), agarita Berberis trifoliata (Moric, 1841) and Vitis genus (Linnaeus, 1753)) in the MP of the PAFFMC and one (Cyperus (Linnaeus, 1753)) in the MP of the PAFFO, and three more (Texas guaiacum Guaiacum angustifolium (Engelmann, 1848), Texas flase agave Hechtia texensis (Watson, 1885), Acacia gerggii Senegalia greggii (Britton and Rose, 1928)) in both MP (CONANP, 2013a; CONANP, 2015).
Most of the species presented endozoochory, which could be considered as evidence on the importance and presence of fauna assemblages in the areas (Granados-Sánchez et al., 2011).
In NL the presence of the invasive species T. ramosissima was registered, which has been widely studied in riparian zones in southwest U.S.A., and northerm of Mexico (Loope et al., 1988; Glenn and Nagler, 2005; Lozano et al., 2009; Granados-Sánchez et al., 2011, CONANP, 2013a; Fuentes, 2017), due to its high tolerance to hydric stress and since it can cause displacement of native species, when desiccating and salinizing the flooding planes where it was established (Smith et al., 1998). This caused a decline in richness and presence of bird unique species, since an environment dominated by T. ramosissima contributes little to diversity, with respect to the native RV (Brand et al., 2008). However, some bird species like E. traillii used this tree to seek shelter and nestle (Fleishman et al., 2003). Therefore, the issue about the eradication of T. ramosissima could be harmful for the biota that requires a ripe vegetative community, since there was no native RV capable of being restored in the short term (Fleishman et al., 2003; Shafroth et al., 2005).
Riparian areas provide habitat, nourishment, rest sites for fauna and are considered as corridors for the dispersion of plants and animals; they also play an important role in relation to climate change, since their environmental heterogeneity allowed these areas to function as shelter for a vast number of species when having its distribution modified (Camacho-Rico et al., 2006; Granados-Sánchez et al., 2006). Diverse authors have worked in riparian areas located in the desert of southern U.S.A. and northern Mexico, which have reported the presence of native species exclusive of these areas.
Conclusions
In the north of Mexico, riparian zones have been poorly studied despite their important role on the maintenance of regional biodiversity and on the generation of environmental services.
This work presents results of a systematic monitoring in the short term (December 2017 - December 2018), 166 species were identified, that either inhabit or benefit from the riparian areas in the Protected Area of Flora and Fauna from Santa Elena Canyon, considered as a representative area of the Chihuahua desert.
This research complements the biological records of the Management Program, reporting 34 new species in the area, of which, 23 were considered in a category of risk of NOM-059-SEMARNAT-2010 standard and 116 in category of vulnerability of the International Union for Conservation of Nature Red List of Threatened Species. The above information lays the foundation for future development of management and conservation strategies of natural resources of the Protected Area of Flora and Fauna from Santa Elena Canyon, therefore fulfilling the objectives established in the present study.
