Species richness, phylogenetic distinctness and

Biodiversity

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Species richness, phylogenetic distinctness and conservation priorities of the avifauna of the ‘Río San Pedro-Meoqui’ Ramsar site, Chihuahua, Mexico Fernando Mondaca-Fernández, Israel Moreno-Contreras, Manuel JuradoRuiz & Adolfo G. Navarro-Sigüenza To cite this article: Fernando Mondaca-Fernández, Israel Moreno-Contreras, Manuel JuradoRuiz & Adolfo G. Navarro-Sigüenza (2017): Species richness, phylogenetic distinctness and conservation priorities of the avifauna of the ‘Río San Pedro-Meoqui’ Ramsar site, Chihuahua, Mexico, Biodiversity, DOI: 10.1080/14888386.2017.1408032 To link to this article: https://doi.org/10.1080/14888386.2017.1408032

Published online: 12 Dec 2017.

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Date: 12 December 2017, At: 17:04

Biodiversity, 2017 https://doi.org/10.1080/14888386.2017.1408032

Species richness, phylogenetic distinctness and conservation priorities of the avifauna of the ‘Río San Pedro-Meoqui’ Ramsar site, Chihuahua, Mexico Fernando Mondaca-Fernándeza, Israel Moreno-Contrerasb,c , Manuel Jurado-Ruizd and Adolfo G. Navarro-Sigüenzac a

Facultad de Zootecnia y Ecologia, Universidad Autónoma de Chihuahua, Chihuahua, México; bPosgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Ciudad de México, México; cMuseo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, México; dObservatorio de aves: Trogón Chihuahua, Chihuahua, México

Downloaded by [189.217.67.232] at 17:04 12 December 2017

ABSTRACT

We analysed the avifauna of the Ramsar site ‘Río San Pedro-Meoqui’ (RSPM) according to avifaunal richness, taxonomic distinctness and conservation. We recorded a total of 199 species constituting 41.11% of the species recorded from Chihuahua and 17.30% of the Mexican avifauna. Avifauna belongs to 137 genera and 49 families, where the most species-rich families were Anatidae (23 species) and Emberizidae (14 species). Taxonomic distinctness of the RSPM was compared with five other Ramsar sites and was above the funnel plot with a high average taxonomic distinctness (Δ⁺ = 90.13). The pair of Ramsar sites with highest dissimilarity were Laguna San Juan de los Ahorcados (68 species) and Manantiales Geotermales de Julimes (81 species) with 48.52% dissimilarity. The data presented herein indicates that a reassessment of the ornithological value of northern Mexican wetlands is needed given that some areas are ‘hotspots’ for the region’s bird species pool (the Chihuahuan Desert), under a taxonomic and phylogenetic perspective.

Introduction The designation of a wetland as a Ramsar site is done under the mission of the convention for the ‘conservation and wise use of all wetlands through local and national actions and international cooperation, as a contribution toward achieving sustainable development throughout the world’ (RAMSAR 2017). This designation is especially important in countries such as Mexico, where information on the state of conservation of their wetlands is deficient (Pérez-Arteaga, Gaston, and Kershaw 2002). In order to be considered as a Ramsar site, the proposed place must cover at least one of the nine criteria that the convention handles in two groups. Group A: sites that include representative, rare or unique types of wetlands and Group B: sites of international importance to conserve of biological diversity (RAMSAR 2017). Wetlands provide essential services and supply all our fresh water, however they continue to be degraded and converted into other land uses (RAMSAR 2017). Mexican wetlands are biologically diverse, ranging from coastal lagoons and mangrove swamps to riverine and floodplain systems, and permanent and ephemeral inland lakes and

CONTACT Fernando Mondaca-Fernández © 2017 Biodiversity Conservancy International

[email protected]

ARTICLE HISTORY

Received 3 September 2017 Accepted 19 November 2017 KEYWORDS

Avian richness; beta diversity; conservation management; hotspots; phylogenetic diversity; wetlands

marshes (Pérez-Arteaga, Gaston, and Kershaw 2002). In Mexico, wetland areas have seen considerable reduction and destruction which clearly has affected species negatively (Ramírez-Bastida, Navarro-Sigüenza, and Peterson 2006). The ‘Río San Pedro-Meoqui’ (RSPM) was designated as a Ramsar site on February 2nd 2012. To earn that designation the RSPM covers two of the nine possible criteria. Criterion 1: a wetland should be considered of international importance if it contains a representative, rare or unique example of a type of natural or near-natural wetland found within the appropriate biogeographic region, and Criterion 4: a wetland should be considered of international importance, if it supports plant and/or animal species in a critical stage in their biological cycle, or offers shelter when adverse conditions prevail. As a paradox, most Ramsar sites, at least in Mexico, lack reliable information about their flora and fauna when designated, specifically in the context of bird lists (PérezArteaga, Gaston, and Kershaw 2002; Ramírez-Bastida, Navarro-Sigüenza, and Peterson 2006). This was the case for the RSPM, which at the time of the designation, did


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not have information about its fauna to know with certainty, which birds it sustains during its critical biological stages (i.e. migration and reproduction) or if it only offers shelter in adverse conditions. This lack of information is evident in the technical datasheet showing non-native species not reported for that site (RAMSAR, and CONANP 2012). In this spirit, we primarily evaluated the species richness of birds (taxonomic diversity) in the RSPM employing observational surveys in five plots of the polygon officially decreed for this wetland, supplemented with published literature, Breeding Bird Survey data, museum records and online resources (eBird). Secondarily, we quantified the average taxonomic distinctness of each Ramsar site of the Chihuahuan Desert to determine its conservation importance under a phylogenetic perspective. Once we quantified these metrics (species richness and average taxonomic distinctness), we performed generalised linear models to evaluate the main spatial features influencing the capture of taxonomic and phylogenetic, as well as assessed the beta taxonomic diversity between wetlands diversities in the Mexican network of Chihuahuan Desert RAMSAR sites.

Methods Study area Data was collected at the Ramsar site RSPM; (28°15ʹ43.27ʺ N, 105°28ʹ51.02ʺ W; 1150 m above sea level), in the municipality of Meoqui, Chihuahua, Mexico (RAMSAR, and CONANP 2012). The study area was delimited following the official criteria: to west limits (Presa Francisco I. Madero; 28°09ʹ26ʺ N, 105°37ʹ12ʺ W), and in the east portion, in the confluence with the Conchos River (28°20ʹ42ʺ N, 105°24ʹ39.6ʺ W). The channel of the San Pedro River crosses the municipalities of Delicias, Rosales, and Meoqui (see Figure 1). The study area was decreed a RAMSAR site on 2 February 2012, with an area approximately of 373 ha. Regional climate presents mean annual temperature in the range 18–20°C and mean annual precipitation between 200 and 400 mm (RAMSAR, and CONANP 2012). The climate goes from very dry semi-warm (99.8%) to semidry (0.2%). This wetland is of natural origin and the current of the river in which it is found, is born at a point near Tarahumaran mountain range in the municipality of Guerrero, western Chihuahua. The vegetation of the site

Figure 1. Sites of bird sampling in the Ramsar site ‘Río San Pedro-Meoqui’, Chihuahua, Mexico. The buffer for each sampling point consists of a circular plot of 500-m radius.

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Figure 2. Vegetation communities of the Río San Pedro-Meoqui, Chihuahua, Mexico.

is composed by xerophytic, herbaceous, and shrub plants of different sizes mixed with some agave species (Agave sp.), mesquite (Prosopis sp.), cottonwood (Populus sp.), willow (Salix babilonica), ash (Fraxinus excelsior) and a large extension of walnut orchards (Juglans regia) bordering the river. The sub-basin is characterised by a flat topographic configuration where agricultural fields and farmland are located (Figure 2). So, its main hydraulic feature is a dense and extensive network of primary and secondary agricultural channels and drains (RAMSAR, and CONANP 2012). Data collection Data collection was performed from June 2013 to 2017 employing the ‘area-search method’ (Ralph et al. 1993) in five plots (Figure 1). In this method the observer moves around in a somewhat restricted area (circular plot of 500-m radii) by searching the sky and all layers of vegetation within; birds were identified by sight and/ or sound. Most surveys were conducted during the peak of bird activity from 06:00 to between 09:00 and 11:00, with occasional nocturnal observations from 17:00 to 19:30. Fieldwork was supplemented with censuses of the Breeding Bird Surveys (from 2009 to 2017) carried out by FMF and MJR following the protocol previously standardised and in two localities (Presa Francisco I. Madero and El Torreón). Binoculars and photographic cameras (30× zoom) were used to record birds and specialised field guides were used for species identification. We generated a list of species following the taxonomy of the International Ornithological Committee (Gill and Donsker 2017), but with Icteria virens merged within Icteriidae (Barker et al. 2013). We categorised species’ seasonality according to data obtained during our field work and by published data for Mexican birds (Howell and

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Webb 1995) in the following classes: permanent resident (observed year round), summer resident (species breeding or spending the summer), winter visitor, and transient (species present during migration only and not spending the winter in the area). The categories of conservation status defined under Mexican law (SEMARNAT 2010) are ‘special protection’ and ‘threatened’. Complementary distributional information was gathered of primary occurrence localities from several sources; by searching the database of the ‘Atlas of Mexican bird distributions’ (Navarro-Sigüenza, Peterson, and Gordillo-Martínez 2003; Peterson, Navarro-Sigüenza, and Gordillo-Martínez 2016) and one principal observational data online source in May 2017 (eBird 2017), as well as by reviewing relevant literature (e.g. Moreno-Contreras et al. 2016). We only selected those records properly supported by strong evidence such as specimens in scientific collections, photographs showing diagnostic characteristics, or detailed field observations of species that could, according to published data, occur in our study area. After carefully reviewing the data, we performed a series of ecological analyses employing checklists of other Mexican Ramsar sites located in the Chihuahuan Desert ecoregion to compare beta diversity. To do this, we delineated the Chihuahuan Desert ecoregion by using the shapefile proposed by INEGI, CONABIO, and INE (2008), and subsequently we obtained the checklist of each RAMSAR site (CONANP 2016) using personal observations, eBird data and published literature (Contreras-Balderas 1984; García-Salas, Contreras-Balderas, and González-Rojas 1995; Contreras-Balderas, García-Salas, and GonzálezRojas 1997; Contreras-Balderas et al. 2004; RuvalcabaOrtega, González-Rojas, and Canales-del Castillo 2008; Suárez-García et al. 2017). Statistical analyses All ecological analyses were performed in the R-environment (R Development Core Team 2016). We calculated one univariate measure to compare bird taxonomic composition: the average taxonomic distinctness (AvTD, Δ⁺; Clarke and Warwick 1998) for presence- absence data. Taxonomic distinctness (Δ⁺) is defined as the average path or branch length between species occurring in a sample, through a taxonomic hierarchy or phylogenetic tree. We used the taxa2dist and taxondive functions of the ‘vegan’ library (Oksanen et al. 2017) and we adopted a variable step weighting strategy for the four taxonomic levels (species, genus, family, and order), in order to determine taxonomic distinctness (Δ⁺) for each Ramsar site (n = 6). Under the null hypothesis of equal average taxonomic distinctness in each sample versus the master list, we evaluated the differences in average taxonomic


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distinctness (ATD, Δ+) from expected Δ+ derived from the total species list of the bird richness reported for all samples (‘master list’). Values of ATD located within the 95% probability funnel based on the total number of species sampled indicated that species composition in the corresponding Ramsar site fell within the expected range. This taxonomic-related index has been employed in other studies to evaluate the phylogenetic importance of protected areas (Moreno-Contreras et al. 2017). To evaluate the possible dependence of the taxonomic distinctness on the richness, we plotted a linear regression. To determine if spatial features influence the species richness and average taxonomic distinctness, we measured three spatial design features (size, shape and fragmentation level) for each Ramsar site. The size of each wetland was measured in ArcGIS 10.3 (ESRI, 2010; www.esri.com) using the default function ‘calculate geometry’ from the attribute table. We measured shape (CIPQ) following the formulae proposed by Osserman (1978). A shape with a high value of CIPQ is considered to be more compact than a shape with a lower CIPQ. A circle is the most compact shape and by definition above it will have a compactness value of 1. To estimate fragmentation levels, we focussed on land-cover type heterogeneity using variation in plant productivity. We downloaded global habitat heterogeneity layers from www.earthenv.org (Tuanmu and Jetz 2015). For the analysis, we used the coefficient of variation (CV = σ/μ; σ, standard deviation; μ, average) of the enhanced vegetation index (EVI) imagery acquired by the moderate resolution imaging spectroradiometer (MODIS). The mean value for each Ramsar site was selected as variable explanatory. All maps were projected to North America Equidistant Conic for calculations, thus balancing the distortion between area and shape. We used generalised linear models (GLMs) to assess the effect of spatial features on the Ramsar sites to capture species richness and average taxonomic distinctness. Species richness and average taxonomic distinctness were used as the dependent variables in all models, with size, shape index and fragmentation level (coefficient of variation) being incorporated as ﬁxed factors. Species richness was fitted with a Poisson error distribution and log link, whereas average taxonomic distinctness was fitted with a Gaussian error distribution with an identity link. We standardised all independent variables using the ‘arm’ package (Gelman and Su 2016) to make coefficients comparable on a common scale. In order to estimate the explanatory power of GLMs, we calculated pseudo-R2 values according to the McFadden’s formula using the ‘pR2’ function in R package pscl (Jackman 2015). To compare taxonomic beta diversity between Ramsar sites, we used the Simpson pairwise dissimilarity index (βsim) (Lennon et al. 2001). The analysis was performed

by using the betadivers function in vegan (Oksanen et al. 2017). We calculated the above mentioned as follows: βsim = min(b, c)/min(b, c) + a, where a is the number of species common to both sites, b is the number of species that occur in the first site but not in the second and c is the number of species that occur in the second site but not in the first. This index describe spatial turnover without the influence of richness gradients (Baselga 2010) and its performance presents symmetry, homogeneity, and nested quadrats (Koleff, Gaston, and Lennon 2003). Simpson pairwise dissimilarity index ranges from 0%, when sites are completely different from one another, to 100%, when sites are completely identical. We visualised the resulting species level matrix by using the ggdendrogram function implemented in ‘ggdendro’ library (deVries and Ripley 2016) with a group-average (UPGMA) clustering.

Results Species richness We recorded a total of 199 species for the Ramsar site, belonging to 137 genera and 49 families (see Appendix 1). The most species-rich families were Anatidae (n = 23 species) and Emberizidae (n = 14 species). Relating to seasonality, 80 were permanent residents, 22 summer residents, 70 winter visitors and 27 transients. With 13 species listed by Mexican law under the ‘special protection’ category, one species listed as ‘threatened’ and one endangered species. As part of the surveys, we recorded nine species that constituted new seasonal or geographic records for Chihuahua: Dendrocygna bicolor, Cyrtonyx montezumae, Plegadis chihi, Nycticorax nycticorax, Ardea herodias, Pandion haliaetus, Ictinia mississippiensis, Rallus tenuirostris and Setophaga ruticilla. Photographic documentation of particularly noteworthy records is displayed in Figure 3. Ecological diversity in Ramsar sites Our master list for ecological analyses included 274 species. The estimated Δ⁺ values resulting from the species list of the Ramsar sites analyzed, plotted against the number of species in each PA, are shown in Figure 4, superimposed on the 95% funnel for the simulated distribution of Δ⁺ for subsets of fixed number of species drawn randomly from the 274 bird species of the Ramsar sites in the study. According to these Δ⁺ values, most of the Ramsar sites were as diverse as expected, because they were located inside the funnel. However, there were at least three sites were found outside of the funnel plot: below of the funnel plot was Río Sabinas, whereas that above of the funnel plot were RSPM and Cañón de Fernández. The conservation

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A B

C D

E F Figure 3. Noteworthy bird records obtained from our fieldwork: (a) Dendrocygna bicolor (Fulvous Whistling Duck), (b) Ardea herodias (Great Blue Heron), (c) Pandion haliaetus (Western Osprey), (d) Ictinia mississippiensis (Mississippi Kite), (e) Rallus tenuirostris (Aztec Rail), (f) Setophaga ruticilla (American Redstart).

sites with highest average taxonomic distinctness was Laguna San Juan de los Ahorcados (Δ⁺ = 91.67), whereas Río Sabinas was the site with lowest average taxonomic distinctness (Δ⁺ = 86.08). RSPM had high average taxonomic distinctness (Δ⁺ = 90.13).The expected average taxonomic distinctness was 88.46. As expected, there is a weak but non-significant increase in average taxonomic distinctness values with increasing numbers of species in sample (R2 = 0.18, p = 0.39, intercept = −10.26). The model for bird species richness being influenced by the spatial features had moderate explanatory power (pseudo-R2 = 0.64; Table 1). On the other hand, the model explicating average taxonomic distinctness

(ATD) as response variable has a poor explanatory power (pseudo-R2 = 0.20; Table 1). The pair of Ramsar sites with highest dissimilarity were Laguna San Juan de los Ahorcados (68 species) and Manantiales Geotermales de Julimes (81 species) with 48.52% dissimilarity, whereas RSPM (199 species) and Laguna San Juan de los Ahorcados were the least dissimilarity, with 1.47% (Figure 5).

Discussion The present study presents a comprehensive survey data on bird presence in RSPM located in the Mexican portion


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Figure 4. Simulated distribution of average taxonomic distinctness (theoretical mean: horizontal line) for random subsets of species from the full species list of 274 species from bird communities of all Ramsar sites of the Chihuahuan Desert ecoregion. The 95% confidence limits (funnel) indicate the expected range of taxonomic distinctness of the entire bird data-set. The red line indicates the trend between bird richness and average taxonomic distinctness. RS: Río Sabinas; MGJ: Manantiales Geotermales de Julimes; CC: Cuatro Ciénegas; CF: Cañón de Fernández; LSJA: Laguna San Juan de los Ahorcados; RSPM: Río San Pedro-Meoqui. Table 1. Results obtained from generalised linear models for the richness and average taxonomic distinctness (ATD). Model Bird richness Intercept Area Compactness CV ATD Intercept Area Compactness CV

Estimate

Std. Error

z value

P value

4.84 −0.10 −1.04 −0.92

0.03 0.11 0.11 0.17

129.18 −0.91 −8.80 −5.25

< 2e-16*** 0.36 < 2e-16*** 1.51e-07***

89.03 −4.18 0.17 −1.46

0.94 2.97 2.90 3.78

94.51 −1.40 0.06 −0.38

0.000112 *** 0.29 0.95 0.73

Asterisks indicate significance levels for the following: * for a ¼ 0.05; **for a ¼ 0.01; ***for a ¼ 0.001.

Figure 5. Dendrogram showing the ecological affinities and complementarity of Ramsar sites of the Chihuahuan Desert ecoregion. RS: Río Sabinas; MGJ: Manantiales Geotermales de Julimes; CC: Cuatrociénegas; CF: Cañón de Fernández; LSJA: Laguna San Juan de los Ahorcados; RSPM: Río San Pedro-Meoqui.

of the Chihuahuan Desert ecoregion, and to determine its conservation value under a comparative and integrative perspective. The 199 species recorded in our study constitute 41.11% of the species recorded from Chihuahua (I. Moreno in litt.) and 17.30% of the Mexican avifauna (Navarro-Sigüenza et al. 2014). We found the seasonality of several additional species different from that indicated by Howell and Webb (1995). Several warblers listed as transients are now established as winter visitors, whereas other species previously mentioned as permanent residents are only migrants or winter visitors in the RSPM and adjacent localities. For the case of the herons, some species have resident populations in our study area, one pattern observed similarly in northern Chihuahua (Moreno-Contreras et al. 2016). It is possible that the high availability of food resources and suitable nesting sites caused by human activities allows the establishment of year-round residents. Two important records are the observation of Dendrocygna bicolor, extending its breeding range in northern Mexico (Howell and Webb 1995) and Rallus tenuirostris, because its presence not just extends the breeding range for this endemic species but because of its label as ‘in danger of extinction’ (SEMARNAT 2010). This gives the RSPM, together with the other 14 species listed under the ‘special protection’ or ‘threatened’, enough data to cover a new criteria to reinforce its designation as a Ramsar site. Species richness was generally higher in the Ramsar sites of the eastern portion of the Chihuahuan Desert; the exception was RSPM with 199 species (Figure 6). Conversely, average taxonomic distinctness was relatively higher in western sites (Figure 7). Regarding multiple


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Figure 6. Number of bird species near the Ramsar site in the Chihuahuan Desert ecoregion.

regressions, this study adds evidence on the importance of taking into account spatial features when establishing new conservation areas (e.g. Ramsar sites). Clearly, the bird species richness in wetland habitats is strongly influenced by the habitat’s heterogeneity, the compactness, and the area of the polygons; coinciding with results obtained for protected natural areas (Paz-Durán et al. 2015). The regression approach explained the little variance of the average taxonomic distinctness. The average taxonomic distinctness (considered as a proxy of phylogenetic diversity), is explicitly influenced by the spatial scaling of species diversity, the phylogenetic tree describing the evolutionary history of these species, and their position in the phylogeny (the ‘regional species pool’). In turn, these three components are driven by multiple evolutionary and ecological processes, including speciation and extinction, dispersal limitation, environmental filtering and intra- and inter-specific interactions (Morlon et al. 2011). Possibly variables explained climatic heterogeneity or anthropogenic pressure could better explain the variance captured of the phylogenetic distinctness in each Ramsar site, more research is needed to disentangle the evolutionary history of the Chihuahuan Desert.

The avifauna of the Chihuahuan Desert has been recognised for its low alpha diversity (Gómez de Silva and Medellín 2002), but with a remarkable uniqueness of evolutionary history (Hubbard 1974). We detected that Río Sabinas was the Ramsar site with lowest taxonomic distinctness. If the value is lower than expected, then a genuine loss of bird diversity has occurred in wetland habitats. This is likely to be due to environmental degradation, such as habitat disturbance or water pollution. In the case of RSPM, the average taxonomic distinctness is above of the funnel plot, indicating a good representation of the evolutionary history of the Chihuahuan Desert bird diversity. In the case of taxonomic beta diversity, we found a high dissimilarity between the most northern and southern Ramsar sites, corresponding to an altitudinal gradient. The trend of high beta diversity at coarse spatial scales is likely a result of a complex interplay of habitat heterogeneity (Cramer & Willig 2005), contrasting types of vegetation and biogeographic histories as area increases seem to be important to explain beta diversity at coarse-scales (Ochoa-Ochoa et al. 2014). Contrary to our expectations, Río Sabinas had a relatively low dissimilarity in comparison with the remaining Ramsar sites. This finding indicates


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Figure 7. Average taxonomic distinctness (ATD) by Ramsar site in the Chihuahuan Desert ecoregion.

that the intersection of the Chihuahuan Desert and Tamaulipan mezquital present a diffuse ecological barrier for the spatial turnover in bird communities in northern Mexico. It is also possible that a small area of some Ramsar sites (for example, Manantiales Geotermales de Julimes), ecological processes related to topography, environmental heterogeneity, and in general the local environmental conditions are influencing the beta diversity and capture of bird species richness (Ochoa-Ochoa et al. 2014). These results confirmed the importance of Mexican Ramsar sites of the Chihuahuan Desert for avian biodiversity in providing key wintering sites, staging areas and breeding habitats. Past surveys were sporadic, mentioning only relevant bird records and rarely covered the whole of RSPM (for instance Moreno-Contreras et al. 2016). In a previous study, Moreno-Contreras et al. (2017) found that those protected areas related to ‘desert scrub’ with an abundance of bodies of water have more phylogenetic distinctness than those protected areas associated to the Sierra Madre Occidental. It seems intuitive that bodies of water as stopover sites along of the Chihuahuan Desert, contribute with the presence of many migrant bird species (aquatic and land birds) from adjacent ecoregions in

conjunction with the presence of birds typical of the desert ecosystem. Clearly, these seasonal movements increase the phylogenetic distinctness in desert scrub localities. The data presented here and in other studies indicates that a reassessment of the ornithological value of northern Mexican wetlands is urgent by demonstrating that some areas are ‘hotspots’ for the regional bird species pool of the Chihuahuan Desert, under a phylogenetic perspective. Conservation recommendations Until today, the RSPM did include within it a management plan, even during the moment of their designation as a Ramsar site (RAMSAR, and CONANP 2012). Without that plan, the impact of the actions in the site by the municipal government (e.g. throwing of organic waste from the municipality and construction of roads in the river cutting their natural flow) local people (e.g. using off-road vehicles; leaving garbage in the site and fishing) the agricultural and construction business (e.g. extraction of construction’s material as rock and sand from the breeding zones and water extraction) and the ‘normal’ consequences from the population increase in the area:


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feral dogs and cats are hunting and cattle is grazing in the middle of breeding zones. All of that is done without planning or with the proper care for the conservation and possible contamination of the site. Some of the solutions for those actions are beyond our possible reach (e.g. the construction of a water’s treatment plant), however some actions can be implemented from the municipality without major complications in order to help in the immediate conservation of the site: (1) implementation of the ecological police to stop the use of off-road vehicles, people leaving garbage, fishing, and extraction of water and construction’s material; (2) regulate the entry of any vehicle to the zone allowing only entry by foot or ecological transportation (e.g. bicycle); and (3) work with the municipal ecological office to ensure feral animals are removed from the site. At the state level, the Chihuahuan Desert ecoregion is considered well protected by the protected areas network of Chihuahua (Moreno-Contreras et al. 2017), although it faces a variety of significant challenges for its avifauna, which is notoriously reflected in the RSPM, for example. Future investigations should evaluate the conservation importance of Ramsar sites under a functional approach, employing birds or other biological groups as a measuring stick, and to determine the representativeness of inland body waters at a state and ecoregional level.

Acknowledgements We thank dozens of bird watchers for sharing their observations at eBird. We are also grateful to Museo de Zoología, Facultad de Ciencias for providing specimen records for this study.

Disclosure statement No potential conflict of interest was reported by the authors.

Funding IMC received a Master scholarship grant provided by CONACyT and UNAM [grant number 451119].

ORCID Israel Moreno-Contreras 7587

http://orcid.org/0000-0001-6000-

References Barker, F. K., K. J. Burns, J. Klicka, S. M. Lanyon, and I. J. Lovette. 2013. “Going to Extremes: Contrasting Rates of Diversification in a Recent Radiation of New World Passerine Birds.” Systematic Biology 62 (2): 298–320.

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BIODIVERSITY

Appendix 1.


Bird species recorded from Río San Pedro-Meoqui, Chihuahua, Mexico. NOM: En = endangered species, Th = threatened species, Sp = subject to special protection. Season: PR = permanent resident, SR = summer resident, WV = winter visitor, T = transient. * = endemic species Family/scientific name Dendrocygna autumnalis Dendrocygna bicolor Branta canadensis Anser rossii Anser caerulescens Anser albifrons Aix sponsa Spatula cyanoptera Spatula discors Spatula clypeata Mareca strepera Mareca americana Anas platyrhynchos Anas diazi Anas acuta Anas carolinensis Aythya valisineria Aythya americana Aythya collaris Aythya affinis Bucephala albeola Mergus merganser Oxyura jamaicensis Callipepla squamata Cyrtonyx montezumae Podilymbus podiceps Podiceps nigricollis Aechmophorus occidentalis Eudocimus albus Plegadis chihi Nycticorax nycticorax Nyctanassa violacea Butorides virescens Bubulcus ibis Ardea herodias Ardea alba Egretta tricolor Egretta thula Pelecanus erythrorhynchos Pelecanus occidentalis Phalacrocorax brasilianus Phalacrocorax auritus Cathartes aura Coragyps atratus Pandion haliaetus Elanus leucurus Accipiter striatus Accipiter cooperii Circus hudsonius Ictinia mississippiensis Buteogallus anthracinus Parabuteo unicinctus Buteo plagiatus Buteo swainsoni Buteo albonotatus Buteo jamaicensis Rallus tenuirostris* Porzana carolina Gallinula galeata Fulica americana Antigone canadensis Himantopus mexicanus Recurvirostra americana Charadrius vociferus Numenius americanus Calidris himantopus

English name Black-bellied Whistling Duck Fulvous Whistling Duck Canada Goose Ross’s Goose Snow Goose Greater White-fronted Goose Wood Duck Cinnamon Teal Blue-winged Teal Northern Shoveler Gadwall American Wigeon Mallard Mexican Duck Northern Pintail Green-winged Teal Canvasback Redhead Ring-necked Duck Lesser Scaup Bufflehead Common Merganser Ruddy Duck Scaled Quail Montezuma Quail Pied-billed Grebe Black-necked Grebe Western Grebe American White Ibis White-faced Ibis Black-crowned Night Heron Yellow-crowned Night Heron Green Heron Western Cattle Egret Great Blue Heron Great Egret Tricolored Heron Snowy Egret American White Pelican Brown Pelican Neotropic Cormorant Double-crested Cormorant Turkey Vulture Black Vulture Western Osprey White-tailed Kite Sharp-shinned Hawk Cooper’s Hawk Northern Harrier Mississippi Kite Common Black Hawk Harris’s Hawk Grey Hawk Swainson’s Hawk Zone-tailed Hawk Red-tailed Hawk Aztec Rail Sora Common Gallinule American Coot Sandhill Crane Black-necked Stilt American Avocet Killdeer Long-billed Curlew Stilt Sandpiper

NOM Season PR SR WV WV WV WV WV PR WV WV WV WV PR Th PR WV WV WV WV WV WV WV WV PR PR Sp PR PR WV WV T WV PR PR PR PR PR PR T PR WV WV PR PR PR PR PR PR Sp WV Sp WV WV Sp SR Sp T Sp PR PR Sp SR Sp T PR En PR WV PR PR Sp WV PR PR PR WV T

Family/scientific name Calidris minutilla Calidris mauri Limnodromus scolopaceus Gallinago delicata Phalaropus tricolor Actitis macularius Tringa solitaria Tringa flavipes Tringa semipalmata Tringa melanoleuca Larus delawarensis Columba livia Streptopelia decaocto Columbina inca Zenaida macroura Zenaida asiatica Geococcyx californianus Coccyzus americanus Tyto furcata Megascops kennicottii Bubo virginianus Athene cunicularia Chordeiles acutipennis Chordeiles minor Phalaenoptilus nuttallii Aeronautes saxatalis Archilochus alexandri Selasphorus platycercus Selasphorus rufus Chloroceryle americana Megaceryle alcyon Melanerpes aurifrons Sphyrapicus nuchalis Dryobates scalaris Colaptes auratus Caracara cheriway Falco sparverius Falco columbarius Falco mexicanus Falco peregrinus Sayornis phoebe Sayornis nigricans Sayornis saya Contopus cooperi Contopus sordidulus Empidonax traillii Empidonax wrightii Pyrocephalus obscurus Tyrannus vociferans Tyrannus verticalis Myiarchus cinerascens Lanius ludovicianus Vireo bellii Vireo plumbeus Vireo cassinii Vireo gilvus Corvus corax Corvus cryptoleucus Bombycilla cedrorum Phainopepla nitens Auriparus flaviceps Eremophila alpestris Tachycineta bicolor Tachycineta thalassina Stelgidopteryx serripennis Hirundo rustica Petrochelidon pyrrhonota Regulus calendula Campylorhynchus brunneicapillus Salpinctes obsoletus Catherpes mexicanus Cistothorus palustris

English name Least Sandpiper Western Sandpiper Long-billed Dowitcher Wilson’s Snipe Wilson’s Phalarope Spotted Sandpiper Solitary Sandpiper Lesser Yellowlegs Willet Greater Yellowlegs Ring-billed Gull Rock Dove Eurasian Collared Dove Inca Dove Mourning Dove White-winged Dove Greater Roadrunner Yellow-billed Cuckoo American Barn Owl Western Screech Owl Great Horned Owl Burrowing Owl Lesser Nighthawk Common Nighthawk Common Poorwill White-throated Swift Black-chinned Hummingbird Broad-tailed Hummingbird Rufous Hummingbird Green Kingfisher Belted Kingfisher Golden-fronted Woodpecker Red-naped Sapsucker Ladder-backed Woodpecker Northern Flicker Northern Crested Caracara American Kestrel Merlin Prairie Falcon Peregrine Falcon Eastern Phoebe Black Phoebe Say’s Phoebe Olive-sided Flycatcher Western Wood Pewee Willow Flycatcher American Grey Flycatcher Vermilion Flycatcher Cassin’s Kingbird Western Kingbird Ash-throated Flycatcher Loggerhead Shrike Bell’s Vireo Plumbeous Vireo Cassin’s Vireo Warbling Vireo Northern Raven Chihuahuan Raven Cedar Waxwing Phainopepla Verdin Horned Lark Tree Swallow Violet-green Swallow Northern Rough-winged Swallow Barn Swallow American Cliff Swallow Ruby-crowned Kinglet Cactus Wren Rock Wren Canyon Wren Marsh Wren

11

NOM Season WV WV WV WV T WV T WV T WV WV PR PR PR PR PR PR SR PR PR PR Sp PR SR T SR PR SR T T PR WV PR WV PR PR T PR WV Sp PR Sp PR WV PR PR T T T T PR SR SR SR PR SR WV T T PR PR WV PR PR PR T SR T SR SR WV PR PR PR WV (Continued)

12



Appendix 1 Family/scientific name Thryomanes bewickii Troglodytes aedon Polioptila caerulea Polioptila melanura Mimus polyglottos Toxostoma curvirostre Toxostoma crissale Sturnus vulgaris Sialia sialis Turdus migratorius Passer domesticus Anthus rubescens Anthus spragueii Haemorhous mexicanus Spinus psaltria Spinus pinus Mniotilta varia Leiothlypis celata Leiothlypis ruficapilla Geothlypis tolmiei Geothlypis trichas Setophaga ruticilla Setophaga aestiva Setophaga coronata Setophaga auduboni Cardellina pusilla Icteria virens Xanthocephalus xanthocephalus Sturnella neglecta Sturnella magna

English name Bewick’s Wren House Wren Blue-grey Gnatcatcher Black-tailed Gnatcatcher Northern Mockingbird Curve-billed Thrasher Crissal Thrasher Common Starling Eastern Bluebird American Robin House Sparrow Buff-bellied Pipit Sprague’s Pipit House Finch Lesser Goldfinch Pine Siskin Black-and-white Warbler Orange-crowned Warbler Nashville Warbler MacGillivray’s Warbler Common Yellowthroat American Redstart American Yellow Warbler Myrtle Warbler Audubon’s Warbler Wilson’s Warbler Yellow-breasted Chat Yellow-headed Blackbird Western Meadowlark Eastern Meadowlark

NOM Season WV WV WV PR PR PR PR PR WV WV PR WV WV PR PR WV WV WV WV T PR WV T WV WV T SR WV PR PR

Family/scientific name Icterus parisorum Icterus bullockii Icterus cucullatus Agelaius phoeniceus Molothrus aeneus Molothrus ater Euphagus cyanocephalus Quiscalus mexicanus Calamospiza melanocorys Melospiza melodia Melospiza lincolnii Melospiza georgiana Zonotrichia leucophrys Passerculus sandwichensis Ammodramus savannarum Spizella passerina Spizella atrogularis Pooecetes gramineus Chondestes grammacus Amphispiza bilineata Peucaea cassinii Melozone fusca Piranga rubra Piranga ludoviciana Pheucticus melanocephalus Cardinalis cardinalis Cardinalis sinuatus Passerina caerulea Passerina amoena Passerina versicolor Passerina ciris

English name Scott’s Oriole Bullock’s Oriole Hooded Oriole Red-winged Blackbird Bronzed Cowbird Brown-headed Cowbird Brewer’s Blackbird Great-tailed Grackle Lark Bunting Song Sparrow Lincoln’s Sparrow Swamp Sparrow White-crowned Sparrow Savannah Sparrow Grasshopper Sparrow Chipping Sparrow Black-chinned Sparrow Vesper Sparrow Lark Sparrow Black-throated Sparrow Cassin’s Sparrow Canyon Towhee Summer Tanager Western Tanager Black-headed Grosbeak Northern Cardinal Pyrrhuloxia Blue Grosbeak Lazuli Bunting Varied Bunting Painted Bunting

NOM Season SR SR SR PR PR PR WV PR WV WV WV WV WV WV WV WV WV WV PR PR SR PR SR T T PR PR SR T SR Sp T