SciELO - Scientific Electronic Library Online

 
vol.19 número1Dinámica de la estructura y composición de la comunidad de aves acuáticas de Ensenada del Jato, Cayo Sabinal, CubaAlfonso L. Herrera y la formación de ligas ornitófilas en México (1902-1926) índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • No hay artículos similaresSimilares en SciELO

Compartir


Huitzil

versión On-line ISSN 1870-7459

Huitzil vol.19 no.1 Omitlán ene./jun. 2018

http://dx.doi.org/10.28947/hrmo.2018.19.1.308 

Artículos originales

Non-breeding distribution, density and population structure of American Avocet (Recurvirostra americana , Gmelin 1789) in Marismas Nacionales, Nayarit, Mexico

Distribución invernal, densidad y estructura poblaciona de Avoceta americana (Recurvirostra americana, Gmelin 1789) en Marismas Nacionales, Nayarit, México

David Molina1  5  * 

John Cavitt2 

Roberto Carmona3 

Miguel Cruz-Nieto4 

1 Posgrado en Ciencias Marinas y Costeras, Universidad Autónoma de Baja California Sur. Carretera al Sur km 5.5., C.P. 23080, La Paz, Baja California Sur, México.

2 Avian Ecology Lab, Weber State University. 3848 Harrison Blvd, Ogden, UT, 84408, EUA.

3 Departamento de Biología Marina, Universidad Autónoma de Baja California Sur. Carretera al Sur km 5.5., C.P. 23080, La Paz, Baja California Sur, México.

4 Programa de Conservación de Aves, Pronatura Noroeste, A.C. Calle Décima 60, C.P. 22800, Ensenada, Baja California, México.

5 Coras-BIO Consultores, S.C. Cristóbal Colón 152, Col. Moctezuma, C.P. 63180, Tepic, Nayarit, México.

Abstract

The Marismas Nacionales wetland system (Nayarit, Mexico) is a Site of International Importance as designated by the Western Hemispheric Shorebird Reserve Network. The American Avocet (Recurvirostra americana) is one of the most numerous shorebirds in the area; nevertheless, there is little information about its overwintering stay at Marismas Nacionales, despite part of the site being decreed as a Biosphere Reserve. In order to clarify some aspects of American Avocet winter ecology, we used transects and scanning sampling method during the winter: to determine distribution and abundance in the Marismas Nacionales (2010-2011), as well as density and population structure in one of the sectors of the Biosphere Reserve (2011-2013). The American Avocet wintering population in the Biosphere Reserve was calculated to be about 26,000 individuals (5.7% of the world’s population), but approximately 36% of avocet wintering population in Marismas Nacionales was outside of the reserve, also there was a certain preference for some wetlands. Evidence suggests that spring migration starts during the first weeks of March. We observed some spatial segregation between sexes, but our results, although valid, are inconclusive because of difficulties in sexing individuals in the field. In spite of local changes in these wetlands, American Avocet winter population has apparently been relatively stable over the last twenty years. Therefore, Marismas Nacionales remains a key wetland for American Avocet in North America.

Keywords: Recurvirostridae; shorebirds; wintering; North America; wetlands

Resumen

El sistema estuarino-lagunar Marismas Nacionales (México) es un Sitio de Importancia Internacional designado por la Red Hemisférica de Reservas de Aves Playeras. La Avoceta americana (Recurvirostra americana) es una de las aves playeras invernantes más numerosas en el área. Sin embargo hay poca información sobre su estancia invernal en el sitio, a pesar de que el sitio fue decretado Reserva de la Biosfera. En este estudio determinamos, a través de trayectos y muestreo de barrido durante el invierno (noviembre-marzo), la distribución y abundancia en las Marismas Nacionales (2010-2011), así como densidad y estructura de población en uno de los sectores de la Reserva de la Biosfera durante 2011-2013. Estimamos en 26,000 individuos la población invernante de Avoceta Americana en la Reserva de la Biosfera (5.7% de la población mundial), pero aproximadamente el 36% de la población invernante la observamos en sitios fuera del polígono de la reserva. La evidencia sugiere que la migración de primavera comenzó durante las primeras semanas de marzo. Hemos observado alguna segregación espacial entre los sexos, pero nuestros resultados, aunque válidos, no son concluyentes debido a la dificultad de identificación de los sexos en algunos individuos. A pesar de los cambios en estos humedales, la población invernante de Avoceta americana ha permanecido relativamente estable en los últimos veinte años. Por lo que Marismas Nacionales sigue siendo un humedal clave para la Avoceta americana en Norteamérica.

Palabras clave: Recurvirostridae; aves playeras; invernación; Norteamérica; humedales

Editor asociado: José Luis Alcántara

Introduction

The American Avocet is a migratory shorebird with blue-gray legs, slightly webbed feet and wing plumage with a chevron pattern. This bird inhabits a wide variety of wetlands, freshwater and brackish, preferably shallow, and with fine sediment (Hamilton 1975, Robinson et al. 1997, Danufsky and Colwell 2003); it preys upon a variety of invertebrates with its long, slender, recurved bill. During prealternate molt, the head becomes progressively cinnamon while the rest of the plumage remains light gray (Prater et al. 1977). Its total length is around 47 cm, with a 72 cm wingspan and an average weight of 360 g (275-440 g). Overall, sexes have similar plumage but show a certain degree of dimorphism regarding body size and bill shape (Hamilton 1975, Robinson et al. 1997).

This species’ breeding range encompasses western, central and southern North America, whereas winter distribution extends on the Pacific coast from northern and interior of California, south, along the western coast of Mexico to Central America, where the species decreases markedly, and in the Atlantic coast from Virginia to the Yucatan Peninsula and inland from Chihuahua to the central valley of Mexico (Howell and Webb 1995, Robinson et al. 1997, AOU 1998). Most research about American Avocet addresses breeding biology aspects (Ackerman et al. 2013) and to a lesser extent the non-breeding period, although the latter mainly in the southern United States (Colwell 1994, Shuford et al. 1998, Page et al. 1999, Colwell et al. 2001, Shuford et al. 2007).

In Mexico, a number of studies have documented the presence of small local nesting colonies throughout the country (Valles-Rosales 1986, Palacios and Alfaro 1991, Mellink and Palacios 1993, Mellink et al. 1996, Carmona et al. 2000, Mellink et al. 2002, Erickson et al. 2007, Ayala-Pérez et al. 2014, Venegas-Holguín et al. 2015); however, during the winter season the greatest numbers have been reported on the Pacific coast, particularly in the Northwest region including the wetlands of Sinaloa and Nayarit (Morrison et al. 1992, Harrington 1993, Morrison et al. 1994, Engilis et al. 1998, Morrison and Ross 2009, Carmona and Danemann 2013). In the state of Nayarit, where the Marismas Nacionales estuarine system is located, the American Avocet has been determined to be one of the most numerous winter shorebirds (Morrison et al. 1994, Morrison and Ross 2009). Because of its importance to shorebirds, Marismas Nacionales was recognized as a Site of International Importance (WHSRN 1992). Later in 1995, it was identified as a Ramsar site (Ramsar Convention 1995) and in 1998 as an Important Bird Area (Arizmendi and Márquez-Valdelamar 2000). Also, its ecological features, biodiversity, and natural resource richness led that part of the wetland to be decreed as a Biosphere Reserve by the Mexican federal government (DOF 2010, CONANP 2013).

Nonetheless, there are few studies supporting the wintering, breeding or migrating importance of Marismas Nacionales for shorebirds (Ortega-Solís 2011, Ortega-Solís et al. 2017). Therefore, the aims of this study were to estimate American Avocet relative abundance and distribution at Marismas Nacionales, and specifically, to determine density and population structure (sex and age proportion) at El Chumbeño lagoon during three winter periods, because this wetland is considered as the numerically most important site for the species in the Biosphere Reserve (Ortega-Solís 2011). This provides information for stakeholders for monitoring, management and conservation practices in the Biosphere Reserve.

Methods

Study area

Marismas Nacionales has an estimated area of 350,000 hm2 (Bojórquez-Tapia et al. 2001) and lies between northwestern Nayarit and southern Sinaloa. The climate is humid and subtropical. The average precipitation is around 1,200 mm (Blanco et al. 2011), which gives the region a marked seasonality and affects ecosystem salinity and productivity (Blanco et al. 2011). This marshland (Figure 1) includes diverse landscapes such as 70,000-85,000 hm2 of mangrove cover forest (Laguncularia racemosa, Rhizophora mangle, Avicennia germinans and Conocarpus erectus), but also important areas of floodplains, mudflats, sandbars, marshes, and coastal lagoons (Bojórquez et al. 2006, Ruiz-Luna et al. 2006, CONABIO 2009, Berlanga-Robles et al. 2010). The region supports important artisanal fisheries (e.g., white shrimp, oysters, and snook) and aquaculture farms, so a strong pressure on natural resources exists (González et al. 2009, CONANP 2013).

Figure 1 Marismas Nacionales wetlands ecosystem, it is located northwest of Nayarit and south of Sinaloa states. The Biosphere Reserve boundaries are indicated in blue, and only was decreed in Nayarit portion. Study sites are the green dots. 

Fieldwork

In order to estimate American Avocet winter population in Marismas Nacionales (i.e. abundance), we surveyed 12 wetland-sites (Table I). The selection of these wetlands was based on the results of previous counts of shorebirds in the Marismas Nacionales wetland complex (Ortega-Solís 2011, Carmona et al. 2012), where was noted that these wetlands support the largest population of shorebirds during the non-breeding period. Also, we assessed the density and population structure at El Chumbeño lagoon (3,900 hm2). This is a shallow body of water and it is located 32 km from the coastline (1 m elevation); water level fluctuations at shoreline favors mudflat exposure and an annual mean salinity of 20.3±19.2 ppm (Güemez-Álvarez 2011). We chose this lagoon because previous counts in Marismas Nacionales indicated the importance of the site, in numerical terms, for the American Avocet (Ortega-Solís 2011) and because the greater relative abundance of avocets observed in winter 2010-2011.

Table I Sampled locations in Marismas Nacionales, Nayarit, visited during the 2010-2011 winter period to estimate American Avocet population numbers. 

Wetland Area covered (hm) Transect mode (lenght in km) Habitat type
Zoquipan 200 Boat (2.5) Freshwater and estuarine lagoon; red mangrove forest, freshwater marsh.
Las Vírgenes 100 Boat (2.6) Permanent small lagoons, with red mangrove forest and pickleweed beds (Salicornia).
Mexcaltitán 950 Boat (14.2) Brackish shallow lagoon system. White mangrove and freshwater vegetation (Typha, Eichhornia).
Los Espejos 135 Walk (2.2) Seasonal wetland; white and black mangrove forest, pickleweed beds, mudflats.
Las Cañadas 2800 Automobile (13.0) Extensive shallow-brackish lagoons; sandbars, white mangrove patches, pickleweed beds (mainly Batis).
Las Haciendas 1850 Automobile (9.45) Seasonal and permanent shallow brackish lagoons; white mangrove patches, pickleweed beds, mudflats.
El Chumbeño 2600 Boat, Walk (19.2) Permanent shallow brackish lagoon; sparsely white mangrove bushes, mudflats.
La Zolyata 315 Boat (4.5) Permanent shallow brackish lagoon; dense white mangrove forest, marshes.
Valle Los Patos 850 Boat (7.35) Permanent brackish shallow waters; dense white mangrove forest.
Las Garzas 1530 Walk (15.8) Shallow brackish lagoon; mudflats, pickleweed marsh, button mangrove patches.
Los Pericos 830 Walk (8.5) Extensive estuarine shallow waters. Sparse mangrove cover, marsh pickleweed beds.
La Polca-Estacada 7100 Boat, Walk (34.5) Permanent shallow brackish lagoon. Button mangrove patches, mudflats.

The boundaries of selected wetlands are variable and, within each wetland, the habitat portion suitable for American Avocet varies depending on the month; because of this, sampling effort was stratified, as it was focused on the habitat portions suitable for avocets, like shallow waters and mudflats. The numbers of avocets were estimated between November 2010 and June 2011, and we conducted 96 surveys in total (eight months and twelve sites, Table I). The count of avocets was done through transects. Due to the peculiar characteristics of each site the observations were carried out walking, on a boat or in a terrestrial motor vehicle, these latter two at low speed (5-10 km/h). The implementation of each transect was systematic in each wetland. Also, transect total length depended on the size of the wetland, trying to maximize the estimation of avocets in the suitable habitat area. Transects were adjusted to the shoreline or along the middle of the body of water of the wetlands. It is important to note that during the non-breeding period, shorebirds usually congregate in mixed and sometimes extensive flocks, which makes it difficult to count groups. So when we crossed the sites, we tried to count carefully the abundance of birds, meaning that when the number of American Avocet was low, a one by one count was possible, but when this is not possible, i.e. when the size of the group was too large (≥300 birds) we stopped and made an estimate of “blocks of the flock”, that is, a portion of the group was counted, and that “block”, was extrapolated to the rest of the group (Howes and Bakewell 1989, Kasprzyk and Harrington 1989).

Because the estimates are inaccurate counts, it is appropriate to point out that it is rather a relative estimation index between wetlands. Counts were made by two experienced observers, each in a two man team and these efforts were systematic. A single observer may find it difficult to count and record large numbers of birds without the aid of the second observer who records this in a field notebook and allows discussion on numbers estimated and identification by a second observer (Howes and Bakewell 1989).

In this site, tide has a very low daily variation and apparently has a no effect or influence on American Avocet numbers; we did not take it into account for sampling. We began surveying one hour after sunrise (around 07:00-07:30 h) and although the end of the counts varied according to the wetlands and avocets present, it was normally around 11:00-12:00 h which is when the temperature is higher and the apparent activity of birds decreases. It is important to indicate that during the counts the total area of the wetlands was not covered, in addition to the fact that the boundaries of some sites are not fully defined.

Likewise, in El Chumbeño lagoon we carried out observations in two later winter seasons (Nov 2011- Mar 2012 and Nov 2012- Mar 2013) to determine density and population structure. Based on previous observations in the lagoon, the habitat available to shorebirds and specific to the American Avocet is restricted to two portions of the wetland: one towards the inner part of the lagoon known as Pescadero and the other at the outer portion, named El Fraile; so the observation effort was concentrated in these two areas. Both areas have extensive and relatively shallow waters, with little variation in water level.

In order to estimate the population density in the lagoon, we delimited seven sampling subunits in each of the two areas (Pescadero and El Fraile). The selection, although random, was related to previous observations in the mentioned areas and the delimitation of the subunits was a function of landscape features, such as sandbars, channels or mangrove rows. These subunits covered a total area of 950 hm2 (500 hm2 at Pescadero and 450 hm2 in El Fraile). To estimate the density we used D=N/A, where D=mean density at the area, N=number of avocets per subunit and A=subunit size. Because of this, we consider it a good estimate of the density of avocets in the available habitat.

We determined sex using bill shape. Avocets with relatively straight bills were classified as males and those with markedly recurved bills were recorded as females (Hamilton 1975, Prater et al. 1977). Sometimes we could not determine individual sex for three reasons: 1) some birds have a slightly recurved bill and it is difficult to establish the sex; 2) resting avocets conceal the bill between flight feathers, so it was impossible to us determine sex, and 3) related to the distance between bird and observer, visual distortions due to evaporation and/or light reflection make determination difficult.

Age was determined based on plumage characteristics (color and wear) but it was limited to November since at later dates, molting of the plumage hinders the separation of age classes. In late autumn-early winter, adult avocets are characterized by more marked and sharp tones in plumage, head coloration is practically light gray and superficially show less worn and molting feathers. Conversely immature individuals show a paler shade of plumage, more worn and less consolidated appearance (more brownish to black), and it has been pointed out that part of the immature population maintains pink tones in the plumage of the head, even at the end of the autumn period (Hamilton 1975, Pyle 2008). Counts in all wetlands were made with the aid of a 20-60x scope, field data were captured by a handheld recorder or by a second observer in a notebook; it should be noted that the observations at the Chumbeño lagoon were carried out by the same observer team.

Data analysis

Temporal and spatial variations of the number of avocets estimated were analyzed through a two-way analysis of variance. In each case, controlling variables were months and wetlands. Also, to be able to compare the relative abundances among wetlands, a kilometric abundance index (KAI) was determined, which is the number of avocets observed per kilometer surveyed (Sánchez-Bon et al. 2010).

To evaluate the linkage between months, population structure, and sites (i.e. Pescadero and El Fraile), we implemented a Xi 2 multiple independent test, where variables were months and sites. Age was compared by Xi 2 independent test, considering winter seasons as treatments (Zar 2010); however, we only could determine the age at early winter. Confidence level was set at 95% in all cases (α=0.05). To perform analyses and visualize results we used Minitab 16.1 (Minitab 2010) and Statistica 9.0 (StatSoft Inc. 2007).

Results

Distribution and abundance. The estimated cumulative abundance of American Avocet reached 138,164 individuals (November 2010 - June 2011). Numerically, the most important wetland was El Chumbeño (50.2% of cumulative recorded avocets), followed by La Polca (31.3%) and Las Garzas-Chahuin (7.5%) (Table II). We found that estimated abundance between localities and along winter months varies, not only temporally but also spatially (F7,11=8.68; P<0.05).

Table II Monthly and cumulative abundance of American Avocet in Marismas Nacionales, Mexico (2010-2011 winter season). 

Month /Wetland Nov Dec Jan Feb Mar Apr May Jun Cumulative abundance
El Chumbeño 19869 21056 17476 8710 2010 122 99 60 69,402
La Polca-Estacada 4007 11676 15924 10785 682 22 108 0 43,204
Garzas- Chahuin 2406 2272 3623 1682 129 27 144 27 10,310
Valle de Los Patos 329 58 1921 570 440 875 429 0 4,622
Las Haciendas 1063 1461 154 261 2 44 108 33 3,126
Cañadas 525 452 503 1503 17 57 0 1 3,058
Estero Pericos 1554 52 40 75 20 0 0 0 1,741
Laguna Zoyata 207 520 113 94 63 315 93 0 1,405
Las Vírgenes 40 29 130 261 257 0 81 0 798
Los Espejos 147 102 23 6 3 0 0 0 281
Mexcaltitan 44 50 5 7 2 2 0 0 110
Zoquipan 0 3 35 66 3 0 0 0 107
Total 30191 37731 39947 24020 3628 1464 1062 121 138,164

We estimated the highest numbers during the middle of the winter (January, at least 39,000 wintering American Avocets) and the lowest in summer (121 individuals). Avocets were well represented in November, increased markedly from December through January, when the highest winter population size was estimated, followed by a 40% decreased in February; this trend continuing until reaching minimum values in June.

Likewise, the KAI showed differences between months and sites. On average, in Marismas Nacionales the KAI highest value occurred during January (168.5 avocets/kilometer), while the lowest value was in June (0.70 avocets/kilometer) (Figure 2). The Chumbeño lagoon presented the highest KAI during most of the months, that is, from November to March, with the maximum values between November and January. The Polca lagoon had, in general, the KAI of second major importance, with maximum values in December through January. However, at the end of the non-breeding season, between April and June, sites such as Valle de Los Patos, La Zolyata and Las Haciendas become relatively important.

Figure 2 Spatial and temporal variation of the Kilometer Abundance Index (KAI) of American Avocets in Marismas Nacionales over the winter. (CHUM=Chumbeño, GARZ=Las Garzas, LSHC=Las Haciendas, EPER=Estero Pericos, LSVG=Las Vírgenes, MEXC=Mexcaltitán, POLC=La Polca, VAPT=Valle de los Patos, CÑDS=Cañadas, LGZY=La Zolyata, LSEP=Los Espejos and ZOQU=Zoquipan). 

American Avocet density and population structure in El Chumbeño. Average density was 5.29 avocets/hm2 ±3.78 (range 0-15.12 avocets/hm2) at El Chumbeño lagoon during the study period (November-March). The highest density occurred during winter and less in migratory periods (F4,65=12.8, P<0.05) (Figure 3). However, no difference was detected between Pescadero (5.15 avocets/hm2 ±4.24, inner coast) and El Fraile (5.44 avocets/hm2 ±3.30, outer coast) areas (F1,78=0.10, P=0.75).

Figure 3 American Avocet density at El Chumbeño lagoon during winter season, two winter periods pooled (2011-2013; mean bar, EE line). 

In relation to the population structure, and combining the observations of both winter periods, males accounted for 53.2% and females 46.8%. Under a local spatial framework, we detected a slight predominance of females at Pescadero, that is, in the innermost section of the lagoon (Xi 2 6=12.8, P=0.04), and a stronger male presence in the outermost zone (Xi 2 6=227.3, P<0.01). Also, apparently females tended to leave the area first (Xi 2 3=97.9, P<0.01) (Figure 4A). Taking into account the age, American Avocet population in El Chumbeño lagoon was dominated by adults (80%, n=1,021) and winter season did not affect the immature proportion (Xi 2 1=1.3, P=0.25) (Figure 4B).

Figure 4 A) Temporal variation of males and females proportion within El Chumbeño lagoon, Marismas Nacionales (winter periods 2011-2012 and 2012-2013). B) Interannual variation of adults and immatures proportion within El Chumbeño lagoon, Marismas Nacionales (winter periods 2011-2012 and 2012-2013). 

Discussion

In the present study, we estimate a wintering population of at least 39,000 American Avocets in Marismas Nacionales (8.7% of the whole population; Andres et al. 2012). Although this abundance is greater than previously reported for the region: 25,400 (Morrison et al. 1994), 20,500 (Ortega-Solís 2011) and 27,000 (Carmona and Danemann 2013), it is important to mention that estimates of wintering groups have been under different methods of estimation and covered different surface area (e.g. we include Sinaloa wetland), some surveys were aerial (Morrison et al. 1994) and some on foot and vehicle (Ortega-Solís 2011, this study), also were temporarily restricted (Morrison et al. 1994, Carmona and Danemann 2013) while others sampled over the winter (Ortega-Solís 2011, Carmona et al. 2012), thus this limits comparison (Figure 5).

Figure 5 Comparison of American Avocets wintering numbers in Marismas Nacionales, Nayarit. This study (red circles), Ortega-Solís (yellow circles), Carmona et al. 2012 (white circles), Morrison et al. 1994 (black bar), Carmona and Danemann 2013 (white bar). 

However, taking into account only the sites in Marismas Nacionales (Nayarit), the present study estimated a wintering population of at least 26,000 American Avocets, which despite the differences in the estimation methods employed, is in agreement with the previous estimates. In this sense, these studies and the present one emphasize the importance of the Marismas Nacionales Biosphere Reserve for avocets, since it holds at least 5.7% of whole population.

These showed that winter population of American Avocet over last twenty years in Marismas Nacionales has apparently been relatively stable, despite local changes in environment, i.e. an increase in aquaculture area (loss of 8% of mangrove cover) and altered flood dynamics (Blanco et al. 2011). In this study Marismas Nacionales was apparently used primarily as an overwintering site. From February through June no increases in avocet numbers were observed; although wintering groups of thousands of individuals have been reported south of Marismas Nacionales (Morrison and Ross 2009). Ortega-Solís (2011) notes that Marismas Nacionales might be more used as a passage area for birds heading north, instead of an overwintering site. It is noteworthy that Ortega-Solís (2011) did not include wetlands located in the Sinaloa portion, but even excluding those sites the use pattern remains as an overwintering area. A subsequent unpublished study (Carmona et al. 2012) is consistent with the pattern shown here: higher abundance during November through January, and a subsequent decrease.

However there are many factors that can affect count results, like climatic events, observer experience, dating, human disturbance, and presence of predators, among others. Besides that the avocet’s abundance could vary seasonally (Ackerman et al. 2013). To analyze this, long-term studies are needed (Ackerman et al. 2013), and either way counts do not provide information about turnover rate (Reed et al. 1996).

Beyond these differences, in agreement with Ortega-Solís (2011) among others (Carmona et al. 2012, Carmona and Danemann 2013), is that El Chumbeño lagoon was, based on numbers, the most important site for American Avocet on the Biosphere Reserve (Figure 6). We determined that at least 21,000 American Avocets used this wetland during winter, which represents 80% of the avocet wintering population among the sites visited within the Biosphere Reserve. This lagoon is a sedimentation wetland (Blanco et al. 2011), and this is consistent with what American Avocet prefers: sites with finer sediments, because their bill is very sensitive (Colwell et al. 2001, Danufsky and Colwell 2003, Ackerman et al. 2013).

Figure 6 American Avocet relative abundance in Marismas Nacionales wetlands during winter stay; diameter of circle it is a representation of relative abundance. Biosphere Reserve surface it is indicated in blue shape. 

The general greatest KIA of American Avocet in El Chumbeño and La Polca-Estacada lagoons, is presumed to be related to its character of being perennial coastal wetlands, with a wide range of depths (0 to >20 cm). This is because it is assumed that American Avocet prefers non-tidal wetlands and deeper areas than other shorebirds (Boettcher et al. 1994, Boettcher et al. 1995, Robinson et al. 1997).

During winter American Avocet displayed regional movements, which results in temporal and spatial changes in abundance among wetlands (Demers et al. 2010). The preference for certain sites could be reflected in the population density at those wetlands. Shuford et al. (2007) in the Central Valley of California, considered that higher avocet density is associated with lack of tidal effect and constant availability of foraging habitat. In El Chumbeño lagoon tidal fluctuation caused null changes in water levels (Blanco et al. 2011), so foraging areas are not restricted and remain available. In addition, energy cost associated with movements between resting and feeding areas is important in site selection (Farmer and Parent 1997), in this wetland both type of areas are close, and so this energy expenditure is reduced.

The major departure of avocets to breeding areas started in the first two weeks of March (Ortega-Solís 2011, Carmona et al. 2012, this study), linked with the fact that nesting typically begins in April (Cavitt 2007, Ackerman et al. 2013), and at the same time, it is noted that there is a decrease in trophic resources in these wetlands, i.e. invertebrates (Molina et al. 2013).

The sexual dimorphism in shorebirds, it has been linked with competition for resources (Myers 1981), and in some species it is indicated as a driver in geographical segregation patterns between sexes (Nebel et al. 2002, Nebel 2005). In this study, we observed similar sex proportion, so there is nothing that suggest us to assume geographic segregation. However, American Avocet sex ratio (1:0.88 in favor males), probably it is associated with reduced competition. Also, avocets are not strictly territorial, because breeding grounds are unpredictable in terms of resources (Plissner et al. 1999, Ackerman et al. 2013), so latitudinal sex segregation is not advantageous. Therefore, in this case, individuals, regardless of sex, tend to be concentrated in favorable areas.

The observed lowest female’ proportion in March apparently indicates an early sex-biased departure to the north, but Gibson (1971) mentioned that both sexes come “simultaneously” and coupled to breeding sites, this is because mating does not have a territorial component (Sordahl 1984, Ackerman et al. 2013); in addition, the sample size in this study during March was too small and could not be representative of the whole wintering population. Due to the above, we can only indicate a similar proportion of males and females in El Chumbeño.

Robinson and Oring (1996) indicated that American Avocet adults preferably occupy inland wetlands and immature classes are excluded to less profitable areas, like coastal sites. El Chumbeño is an internal wetland (32 km distance from the coastline), not subject to tidal fluctuations, with extensive shallow waters and constant prey availability (Blanco et al. 2011, Molina et al. 2013). This factors could explain the predominance of adults in this lagoon (Robinson and Oring 1996, Robinson et al. 1997, Colwell et al. 2001) and like other shorebird species (Fernández and Lank 2006, Van den Hout et al. 2014), point out a spatial segregation related to age. Although it is possible to be valid, our observations was temporarily and spatially restricted. In addition, it is possible that a lower proportion of immature avocets derived from natural processes of mortality in this age group.

The above implies that Marismas Nacionales still is a profitable winter wetland for American Avocet in North America. The origin of American Avocet winter population definitely implies several breeding colonies (Robinson and Oring 1996). According to this, it is noteworthy to mention that although data are scarce, there is a certain migratory connectivity between the Intermountain West and Marismas Nacionales regions (Robinson and Oring 1996, Utah Linking Communities 2015).

Acknowledgements

We want to thanks to all supporters of the project: The Kennecott Utah Copper Corporation, the Rio Tinto-Bird Life Program, Utah Linking Communities Program and CONACYT. This work was partially supported by the North American Wetland Conservation Act Project. To the Marismas Nacionales Biosphere Reserve (CONANP) staff and Pancho Villa community. To Pronatura Noroeste A.C., especially Tepic branch office. To Avian Lab members (Universidad Autonoma de Baja California Sur) and to S. Villagómez, E. Miramontes, C. Sierra Beltrán for field assistant; to M. Corona for figure maps. As well as to reviewers who improved the manuscript with their valuable and accurate comments.

Literature cited

Ackerman, J., A. Hartman, M. Herzog, J.A. Robinson, L.W. Oring, J.P. Skorupa, R. Boettcher. 2013. American Avocet (Recurvirostra americana), The Birds of North America Online (A. Poole, ed.). Ithaca: Cornell Lab of Ornithology, EUA. DOI: https://doi.org/10.2173/bna.275Links ]

Andres, B., P. Smith, R.I.G. Morrison, C. Gratto-Trevor, S. Brown, C. Friis. 2012. Population estimates of North American shorebirds, 2012. Wader Study Group Bulletin 119(3):178-194 [ Links ]

AOU (American Ornithologist’s Union). 1998. Check-list of North American birds. 7th edition. American Ornithologists’ Union, Washington, D.C., EUA. [ Links ]

Arizmendi, M. del C., L. Márquez-Valdelamar (eds.). 2000. Áreas de importancia para la conservación de aves en México. FMCN, CONABIO, CCA, CIPAMEX. México, D.F. [ Links ]

Ayala-Pérez, V., R. Carmona, N. Arce, J. Rivera. 2014. First nesting records of the American Avocet (Recurvirostra americana) and White Ibis (Eudocimus albus) at Laguna Ojo de Liebre, BCS, México. CICIMAR Oceánides 29(1):19-22. [ Links ]

Berlanga-Robles, C., R.R. García-Campos, J. López-Blanco, A. Ruiz-Luna. 2010. Patrones de cambio de coberturas y usos del suelo en la región costa norte de Nayarit (1973-2000). Investigaciones Geográficas 72:7-22. [ Links ]

Blanco, M., F. Flores-Verdugo, M. Ortiz-Pérez, G. de la Lanza, J. López-Portillo, I. Valdéz-Hernández, C. Agraz-Hernández, S. Czitrom, E. Rivera-Arriaga, A. Orozco, G. Jiménez, D. Benítez, J. Gómez, A. González, M. Soria-Barreto, G. Otis-Krus, E. Jacobo-Sapien, G. López-Cano, H. Blanco-Fuentes, R. Blanco-Fuentes. 2011. Diagnóstico funcional de Marismas Nacionales. Universidad Autónoma de Nayarit, Comisión Nacional Forestal. Tepic, México. [ Links ]

Boettcher, R., S. Haig, W. Bridges Jr. 1994. Behavioral patterns and nearest neighbor distance among non-breeding American Avocets. The Condor 96(4):973-986. [ Links ]

Boettcher, R., S. Haig, W. Bridges Jr. 1995. Habitat related factors affecting the distribution of non-breeding American Avocets in coastal South Carolina. The Condor 97(1):68-81. [ Links ]

Bojórquez, I., O. Nájera, A. Hernández, F. Flores, A. González, D. García, A. Madueño-Molina. 2006. Particularidades de formación y principales suelos de la Llanura Costera Norte del estado de Nayarit, México. Cultivos Tropicales 27(4):19-26. [ Links ]

Bojórquez-Tapia, L.A., S. Díaz-Mondragón, E. Ezcurra. 2001. GIS-based approach for participatory decision making and land suitability assessment. International Journal of Geographical Information Science 15(2):129-151. [ Links ]

Carmona, R., C. Carmona-Islas, J.A. Castillo-Guerrero, E.M. Zamora-Orozco. 2000. Nesting records of American Avocet and Black-necked Stilt in Baja California Sur, México. The Southwestern Naturalist 45(4):523-524. [ Links ]

Carmona, R., M.A. Cruz-Nieto, J.M. Bustamante, J. Coronado, E. Cortés, P. Martínez, L.F. Mendoza, E. Miramontes-Medina, D. Molina, L. Ortega-Solís, C. Rodríguez, G. Rubio, J. Salcedo, J. Vargas-Vega, T. Yáñez. 2012. Planificación de mecanismos para la conservación legal y restauración de las poblaciones de aves acuáticas migratorias invernales en Marismas Nacionales, Nayarit, México. Reporte Final NAWCA. Pronatura Noroeste, Universidad Autónoma de Baja California Sur, Universidad Autónoma de Nayarit, Instituto Tecnológico de Bahía de Banderas. México. [ Links ]

Carmona, R., G. Danemann. 2013. Monitoreo de aves playeras migratorias en 11 sitios prioritarios del Noroeste de México y reconocimiento invernal de cinco sitios adicionales. Reporte Final para la Comisión Nacional de Áreas Naturales Protegidas. México. [ Links ]

Cavitt, J. 2007. Productivity and Foraging ecology of two coexis ting shorebird species breeding at Great Salt Lake, Utah 2005-2006. Report Weber State University. Utah Department of Environmental Quality, Division of Water Quality. EUA. [ Links ]

Colwell, M. 1994. Shorebirds of Humboldt Bay, California: abundance estimates and conservation implications. Western Birds 25:137-145. [ Links ]

Colwell, M., T. Danufsky, R. Mathis, S.W. Harris. 2001. Historical changes in the abundance and distribution of the American Avocet at the northern limit of its winter range. Western Birds 32:1-12. [ Links ]

CONABIO. 2009. Manglares de México: Extensión y distribución. 2a ed. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. México, D.F. [ Links ]

CONANP. 2013. Programa de Manejo. Reserva de la Biosfera Marismas Nacionales, Nayarit. Secretaría de Medio Ambiente y Recursos Naturales. Comisión Nacional de Áreas Naturales Protegidas. México, D.F. [ Links ]

Danufsky, T., M. Colwell. 2003. Winter shorebird communities and tidal flat characteristics at Humboldt Bay, California. The Condor 105(1):117-129. [ Links ]

Demers, S., J. Takekawa, J. Ackerman, N. Warnock, D. Athearn. 2010. Space use and habitat selection of migrant and resident American Avocets in San Francisco Bay. The Condor 112(3):511-520. [ Links ]

Diario Oficial de la Federación (DOF). 2010. Decreto por el que se declara como área natural protegida, con el carácter de reserva de la biosfera, la región conocida como Marismas Nacionales Nayarit. Ciudad de México a 12 de mayo del año 2010, pp. 13-54. [ Links ]

Engilis, A., L.W. Oring, E. Carrera, J.W. Nelson, A. Martínez-López. 1998. Shorebird surveys in Ensenada Pabellones and Bahía Santa María, Sinaloa, México; Critical winter habitats for Pacific flyway shorebirds. The Wilson Bulletin 110:332-341. [ Links ]

Erickson, R., R. Hamilton, R. Carmona, G. Ruiz-Campos. 2007. Baja California Peninsula. North American Birds 60(4):582-583. [ Links ]

Farmer, A., A. Parent. 1997. Effects of the landscape on shorebird movements at spring migration stopovers. The Condor 99(3):698-707. [ Links ]

Fernández, G., D. Lank. 2006. Sex, age, and body size distributions of Western Sandpipers during the nonbreeding season with respect to local habitat. The Condor 108(3):547-557. [ Links ]

Gibson, F. 1971. The breeding biology of the American Avocet (Recurvirostra americana) in central Oregon. The Condor 73(4):444-454. [ Links ]

González, A., J.I. Bojórquez, O. Nájera-González, J. García-Paredes, A. Madueño-Molina, F. Flores-Vilchez. 2009. Regionalización ecológica de la llanura costera norte de Nayarit, México. Investigaciones Geográficas 69:21-39. [ Links ]

Güemez-Álvarez, C. 2011. Abundancia de las poblaciones de camarones peneidos en las localidades de Antonio Laureles y El Pescadero, del Sistema Lagunar de Agua Brava, Nayarit. Memorias de Residencia Profesional. Instituto Tecnológico de Bahía de Banderas. La Cruz de Huanacaxtle, Nayarit, México. [ Links ]

Hamilton, R. 1975. Comparative behavior of the American Avocet and the Black-necked Stilt (Recurvirostridae). Ornithological Monographs 17:1-98. [ Links ]

Harrington, B.A. 1993. A coastal aerial winter shorebird survey on the Sonora and Sinaloa coasts of Mexico, January 1992. Wader Study Group Bulletin 67:44-49. [ Links ]

Howell, S.N.G., S. Webb. 1995. A guide to the birds of México and Northern Central America. Oxford University Press. New York, EUA. [ Links ]

Howes, J., D. Bakewell. 1989. Shorebirds studies manual. Asian Wetland Bureau. No. 55. Kuala Lumpur, Malasia. [ Links ]

Kasprzyk, M., B. Harrington. 1989. Manual de campo para el estudio de las aves playeras. Western Hemispheric Shorebird Reserve Network. Manomet. [ Links ]

Mellink, E., E. Palacios. 1993. Notes on breeding coastal waterbirds in Northwestern Sonora. Western Birds 24:29-37. [ Links ]

Mellink, E., E. Palacios, S. González. 1996. Notes of nesting birds of the Ciénega de Santa Clara saltflat, Northwestern Sonora, México. Western Birds 27:202-203. [ Links ]

Mellink, E., A. Castillo-Guerrero, A. de la Cerda. 2002. Noteworthy waterbird records in the Delta of the Colorado, Mexico, 2002. Western Birds 33:249-253. [ Links ]

Minitab Inc. 2010. Minitab 16.1.0. [ Links ]

Molina, D., R. Carmona, J. Cavitt, M.A. Cruz-Nieto. 2013. Wintering use patterns of American Avocet (Recurvirostra americana) in Marismas Nacionales, Nayarit, México. Memories fifth Western Hemisphere Shorebird Group Meeting. Santa Marta, Colombia. [ Links ]

Morrison, R.I.G., R.K. Ross. 2009. Atlas of Nearctic shorebirds on the coast of Mexico. Canadian Wildlife Service. Ottawa, Canada. [ Links ]

Morrison, R.I.G., R.K. Ross, J. Guzmán-Poo. 1994. Preliminary results of surveys of the southern half of the Pacific coast, states of Chiapas to Sinaloa. Canadian Wildlife Service. Ottawa, Canada. [ Links ]

Morrison, R.I.G., R.K. Ross, S. Torres. 1992. Aerial surveys of Nearctic shorebirds wintering in Mexico: Some preliminary results. Canadian Wildlife Service Progress Notes 201:1-11. [ Links ]

Myers J.P. 1981. A test of three hypotheses for latitudinal segregation of the sexes in wintering birds. Canadian Journal of Zoology 59:1527-1534. [ Links ]

Nebel, S. 2005. Latitudinal clines in bill length and sex ratio in a migratory shorebird: a case of resource partitioning? Acta Oecologica 28:33-38. [ Links ]

Nebel, S., D. Lank, P. O’Hara, G. Fernández, B. Haase, F. Delgado, F.A. Estela, L.J. Evans-Ogden, B. Harrington, B.E. Kus, J.E. Lyons, F. Mercier, B. Ortego, J.Y. Takekawa, N. Warnock, S.E. Warnock. 2002. Western Sandpipers (Calidris mauri) during the nonbreeding season: spatial segregation on a hemispheric scale. The Auk 119(4):922-928. [ Links ]

Ortega-Solís, L. 2011. Distribución espacial y temporal de las aves playeras invernantes en la Reserva de la Biosfera Marismas Nacionales, Nayarit. Tesis de licenciatura, Universidad Autónoma de Nayarit. Tepic, Nayarit, México. [ Links ]

Ortega-Solís, L., U. Rosales-Huerta, E.M. Figueroa-Esquivel, F. Puebla-Olivares. 2017. Primer registro de anidación del chorlo de collar (Charadrius collaris) en la Reserva de la Biosfera Marismas Nacionales, Nayarit. Huitzil 18(1):1-6. [ Links ]

Page, G., L. Stenzel, J. Kjelmyr. 1999. Overview of shorebird abundance and distribution in wetlands of the Pacific coast of the contiguous United States. The Condor 101(3):461-471. [ Links ]

Palacios, E., L. Alfaro. 1991. Breeding birds of laguna Figueroa and La Pinta pond, Baja California, México. Western Birds 22:27-32. [ Links ]

Plissner, J., S. Haig, L. Oring. 1999. Within-and between-year dispersal of American Avocets among multiple Western Great Basin wetlands. The Wilson Bulletin 111(3):314-320. [ Links ]

Prater, A.J., J.H. Marchant, J. Vuorinen. 1977. Guide to the identification and ageing of Holarctic Waders. British Trust for Ornithology Guide. Thetford, U.K. [ Links ]

Pyle, P. 2008. Identification Guide to North American Birds. Part II. Slate Creek Press. Bolinas, California, EUA. [ Links ]

Ramsar Convention. 1995. Marismas Nacionales. Online: < Online: http://ramsar.conanp.gob.mx/docs/sitios/FIR_RAMSAR/Nayarit/Marismas_Nacionales/Actualizacion_2013/CERTIFICADO_MARISMAS_NACIONALES.pdf > (consultado el 7 junio de 2013). [ Links ]

Reed, J.M., N. Warnock, L. Oring. 1996. Censusing shorebirds in the western Great Basin of North America. International Wader Studies 9:29-36. [ Links ]

Robinson, J.A., L.W. Oring. 1996. Natal and breeding dispersal in American Avocets. The Auk 114(3):416-430. [ Links ]

Robinson, J.A., L.W. Oring, J.P. Skorupa, R. Boettcher. 1997. American Avocet (Recurvirostra americana), The Birds of North America Online (A. Poole, ed.). Ithaca: Cornell Lab of Ornithology, EUA. DOI: https://doi.org/10.2173/bna.275Links ]

Ruiz-Luna, A., C. Berlanga-Robles, J. Acosta-Velázquez. 2005. Bases para el ordenamiento ecológico de la zona costera del norte de Nayarit, México. Semana Geomática Barcelona: Los sensores de alta resolución y sus aplicaciones, Barcelona, España. [ Links ]

Sánchez-Bon, G., G. Fernández, D. Escobedo-Urías, J. Torres-Torner, J.C. Cid-Becerra. 2010. Composición espacial y temporal de la avifauna de las islas de barra del complejo lagunar San Ignacio-Navachiste-Macapule, Sinaloa, México. Ciencias Marinas 36(4):355-370. [ Links ]

StatSoft, Inc. 2007. STATISTICA, version 8.0. [ Links ]

Shuford, D., G. Page, J. Kjelmyr. 1998. Patterns and dynamics of shorebird use of California’s Central Valley. The Condor 100(2):227-244. [ Links ]

Shuford, D., J. Humphrey, R.B. Hansen, G. Page, L. Stenzel, C. Hickey. 2007. Summer distribution abundance and habitat use of Black-necked Stilt and American Avocets in California’s Central Valley. Western Birds 38:11-28. [ Links ]

Sordahl, T. 1984. Observations on breeding site fidelity and pair formation in American Avocets and Black-necked Stilts. North American Bird Bander 9(2):8-11. [ Links ]

Utah Linking Communities. 2015. American Avocets, Ambassadors of the Intermountain West. Online: < http://www.utahlinking.org/news-events/item/28-avocet-ambassadors > (consultado el 6 de julio de 2016). [ Links ]

Valles-Rosales, E. 1986. Estudio de algunos aspectos de la ecología de las aves de ribera en el exlago de Texcoco. Tesis de licenciatura, Universidad Nacional Autónoma de México, Ciudad de México, México. [ Links ]

Van den Hout, P.J., J. Van-Gils, F. Robin, M. van der Geest, A. Dekkinga, T. Piersma. 2014. Interference from adults forces young Red Knots to forage for longer and in dangerous places. Animal Behaviour 88:137-146. [ Links ]

Venegas-Holguín, D., M.E. Díaz-Tengler, J. Cruz-Nieto. 2015. Avoceta americana (Recurvirostra americana): primeros registros reproductivos en Chihuahua, México. Huitzil 16(1):28-32. [ Links ]

WHSRN (Western Hemospheric Shorebird Reserve Network). 1992. Online: < http://www.whsrn.org/site-profile/marismas-nacionales > (consultado el 10 de enero de 2010). [ Links ]

Zar, J. 2010. Biostatistical Analysis. 5th edition. Pearson Prentice Hall. New Jersey, EUA. [ Links ]

Received: March 06, 2017; Accepted: August 23, 2017

* Correo electrónico: biol.davidmt@gmail.com

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License