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1Centro de Investigación Científica y de Educación Superior de Ensenada,. Carretera Tijuana-Ensenada, Km. 107; 22860 Ensenada, B.C., México. 2Unidad ...
Diurnal Abundance, Foraging Behavior and Habitat Use by Non-Breeding Marbled Godwits and Willets at Guerrero Negro, Baja California Sur, México JOSÉ ALFREDO CASTILLO-GUERRERO1*, GUILLERMO FERNÁNDEZ2, GUILLERMINA ARELLANO3 AND ERIC MELLINK1 1

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Centro de Investigación Científica y de Educación Superior de Ensenada, Carretera Tijuana-Ensenada, Km. 107; 22860 Ensenada, B.C., México

Unidad Académica Mazatlán, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Apartado Postal 811, 82040 Mazatlán, Sinaloa, México 3

Venustiano Carranza #291, 45400 Tonalá, Jalisco, México *Corresponding author; E-mail: [email protected]

Abstract.—Seasonal variation in abundance, time activity budgets and foraging behavior of non-breeding Marbled Godwits (Limosa fedoa) and Willets (Tringa semipalmata) were compared at four sites at the Laguna Ojo de Liebre—Guerrero Negro saltworks complex, Baja California, Mexico. Habitat use varied between species, seasons and sites. Marbled Godwits (182 ± 44.1 individuals per site) were more abundant than Willets (70 ± 16.1 individuals per site), reflecting their overall pattern in northwestern Mexico. Overall abundance diminished throughout the season (270 ± 69 individuals per site in Oct-Nov, 85 ± 21 in Dec-Jan and 60.2 ± 24 in Feb-Mar), although it remained high at mudflat. Consistent with bill length, Willets foraged mostly by pecking, while Marbled Godwits did so mostly by probing (proportion of pecks: 0.95 ± 0.17 and 0.4 ± 0.27, respectively). Marbled Godwits changed their time activity budgets through the wintering season: time devoted to vigilance changed from 8-23% in Oct-Nov, to 0.4-8% in Feb-Mar whereas time devoted to feeding changed from 12-40% in Oct-Nov to 59-74% in Feb-Mar. This pattern seems to reflect a change in priorities; surviving early in the season and accumulating energy to migrate, later. In both species, differences in use of habitat appeared to be related to site characteristics such as substrate hardness and risk of predation. The mudflat was the site most used and the saltmarsh, the least used. Some individuals in both species used the more risky saltmarsh, but increased the time devoted to vigilance. Thus, habitat quality for non-breeding shorebirds depended on both benefits and costs for foraging birds, and habitat choice by specific individuals was complex and probably involved condition- or state-dependent tradeoffs that balanced metabolic requirements, safety priorities, and, perhaps, social status or dominance. Received 10 September 2008, accepted 30 November 2008. Key words.—local distribution, seasonal variation, shorebirds, time activity budgets. Waterbirds 32(3): 400-407, 2009

The nonbreeding season is important in the life history of shorebirds as it can last for up to eight months of the year. During this time, their use of habitat is limited to discrete wetlands or wetland systems along their migratory corridors. However, wetlands have been diminishing rapidly (Myers et al. 1987; Bildstein et al. 1991), a fact that may explain the apparent reduction in many shorebird populations that breed in North America (Bart et al. 2007). Effective conservation of shorebirds depends on understanding how patterns of habitat distribution affect shorebird population dynamics during the nonbreeding season. Determining the factors responsible for these distributions is critical to predicting how shorebirds will respond to changes in their environment.

Although the major non-breeding sites of shorebirds along the western coast of North America have been documented and some information on feeding and habitat use by shorebirds exists, especially for California, U.S.A. (Warnock and Takekawa 1995; Dodd and Colwell 1996; Colwell and Dodd 1997; Danufsky and Colwell 2003; Shuford et al. 2004) information on winter ecology for many species at the more southern localities, where most shorebirds winter, is meager. Such is the case for Marbled Godwit (Limosa fedoa) and Willet (Tringa semipalmata), both of which spend eight-nine months at wintering sites (Kelly and Cogswell 1979; GrattoTrevor 2000; Lowther et al. 2001). One of the important wintering sites for these two species, and other shorebirds that

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use the Pacific Flyway, is the Laguna Ojo de Liebre—Guerrero Negro saltworks complex (Page et al. 1997; Danemann et al. 2002). Here, the Marbled Godwit and the Willet are the most abundant large shorebirds, with about 70,000 and 10,000 birds, respectively (Page et al. 1997). Although the site has the largest non-breeding congregation of the Marbled Godwit throughout its range (Page et al. 1997), no information is available on aspects that affect its distribution in the locality. No such information is available either for the Willet. At Guerrero Negro-Ojo de Liebre there are various types of habitat available to foraging shorebirds, including salt-ponds, mudflats, saltmarsh and sand-beaches. At other wintering sites, shorebirds can move between habitats, changing their foraging strategy, depending on habitat structure and availability, as well as on changes in feeding needs (Metcalfe and Furness 1984; Warnock and Takekawa 1995; McCaffery 1998). Also, some species of shorebirds exhibit age and/ or sex-related differences in habitat use (Zharikov and Skilleter 2002; Both et al. 2003; Fernández and Lank 2006). Studying the patterns of habitat use in an important non-breeding site, with a variety of habitats available, can yield information on the processes that affect shorebird distribution at the local level and their strategies for winter survival. In this study, we determined the abundance, time activity budgets, and foraging behavior of Marbled Godwits and Willets at four sites in the Guerrero NegroLaguna Ojo de Liebre wetland complex, in the middle of the peninsula of Baja California, Mexico. We compared seasonal variation and patterns of habitat use by both species. METHODS Study Area The Guerrero Negro-Ojo de Liebre wetland complex covers approximately 500 km2 on the Pacific coast of the Baja California Peninsula, within the Vizcaíno Desert. The area is composed of a diverse habitat mosaic, which includes an outer bay, marshes, salt flats, sand dunes, halophytic scrubland and 25,000 ha of saltpans (under operation by Exportadora de Sal, S.A. de C. V.). Salt production involves pumping seawater from the la-

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goon through a system of concentration ponds, where it evaporates through the action of the sun and wind. These ponds have islets, sand bars, mudflats and shallow water areas, which are used by shorebirds to roost and feed. Water levels and salinity are kept fairly stable as a requirement for the industrial production of salt. Shorebirds make use of even the most saline ponds in the system, where salinity reaches 250 ppm (Ewald 1997). We selected two natural and two artificial sites. The natural sites were a 2-km long mudflat and a 2.3-km long, 300-m wide strip of saltmarsh with a mix of glasswort (Salicornia spp.), seepweed (Suaeda spp.) and beachwort (Batis marítima) which covered up to 60% of the surface. Spring tides could cover the mudflat almost completely, whereas the saltmarsh included tidal creeks that emptied at low tide. The first artificial site was a 1.8 km2 mudflat, within the first salt pond (“pumping pond”), which received seawater directly to be distributed to the evaporative ponds, and where salt concentration was similar to that of seawater (35-38 ppm). It had small patches of marsh vegetation (same species as in the saltmarsh). Water level varied lightly, depending on water supply. The second site was a 1 km2 pond (“concentration pond”), with salinity as high as 250 ppm. The substrate was hardened by salts, but there were softer flats bordering the pond. Water level was relatively constant. Fieldwork We visited the area twice every month between October 2002 and March 2003. Each visit included a complete day at each site (08:00 to 18:00). All Marbled Godwits and Willets were counted at 3-hr intervals. We determined the maximum abundance of each species by using the highest count. We determined the diurnal time activity budgets of both species through focal observations of randomly selected individuals (Altman 1974). We considered six activities: feeding, moving, roosting, preening, vigilance and aggression (Davis and Smith 1998; de Leon and Smith 1999). We followed each selected individual for 2 min, through a spotting scope (15 × 50) or binoculars (8 × 35). During focal observations, we also recorded the foraging behavior of each species, including feeding method, foraging rates (number of foraging attempts per minute), and foraging success by feeding method (proportion of successful foraging events). Foraging success was inferred from observation of swallowing, as prey items were usually too small to see from our vantage point. Feeding method was categorized as pecking (single and multiple), with the bill just touching the substrate surface or taking prey in the water column; or probing (single and multiple), when the bill was inserted into the substrate (Barbosa and Moreno 1999). The proportion of pecks was used as an index of feeding technique and was expressed as the number of pecks out of the total number of foraging attempts (i.e. pecks + probes). Behavioral data were dictated into a tape recorder, timed with a stopwatch, and later transcribed. Statistical Analyses Data were analyzed for the four sites and three seasons, according to the migratory chronology of the area (Danemann et al. 2002): October-November (post-migratory), December-January (wintering), and February-

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March (pre-migratory). We compared abundance through three-way analysis of variance (ANOVA), using species, site and season as independent variables. We analyzed time-activity data using multivariate analysis of variance (MANOVA). Species, site and season were independent factors in the MANOVA. We used MANOVA because the dependent variables (i.e. individual behaviors) were not independent of each other; as the amount of time engaged in one activity influences the amount of time engaged in other activities. Wilks’ lambda (λ) was the test criterion. When significant effects were found, we explored them further through one-way ANOVAs, complemented with Tukey tests. Although tides affect foraging behavior in shorebirds, especially in smaller species (Burger et al. 1977; Burger 1984; Maimone-Celorio and Mellink 2003), logistics precluded a sample size large enough to analyze all factors of our interest, and preliminary analysis did not uncover a significant effect of tide level in our data. We analyzed variation in feeding method, foraging rates, and foraging pecking or probing success using a three-way ANOVA to determine the effects of species, site and season. Since Willets did not use probing consistently, probing success was analyzed only for Marbled Godwit, using a two-way ANOVA to determine the effects of site and season. In all the analysis, we used only individuals who spent more than 10% of their time feeding. To produce normal distributions for parametric analyses, proportions were arcsine transformed. We considered statistical test results to be significant at P ≤ 0.05. If interaction terms were not significant, models were reduced to their most parsimonious form using Type III sum of squares. All values are given as mean (±SE). All statistical tests were performed with the Statistica 6.0 software (StatSoft, Inc., Tulsa, OK, 2002).

RESULTS Abundance Both species used all four sites, although with major differences in their abundance (Table 1). The interactions site-species, season-species and site-season-species were not significant (interaction terms: P > 0.10), but the interaction site-season was significant (F6, 64 = 2.36, P = 0.03): Abundance of birds in

the mudflat and the saltmarsh was uniform throughout the study, while the abundance in the pumping and concentration ponds decreased as the study progressed. Overall, both species were scarcer at the saltmarsh than at the other sites. The Marbled Godwit was more than twice as abundant as the Willet (182 ± 44.1 vs 70 ± 16.1; F1, 64 = 8.91, P = 0.003). Time Activity Budgets A three-way interaction (species-site-season: Wilks’ λ = 0.91, P = 0.02) occurred in the initial analyses of behavior, and there were significant differences in feeding, roosting, moving and vigilance. Overall, Marbled Godwits spent more time feeding than Willets, but less time moving and being vigilant (Fig. 1). Subsequent analyses were by species. Marbled Godwits exhibited a significant interaction between site and season, which affected the time devoted to feeding (F6,317 = 3.17, P =0.004), resting (F6,317 = 3.42, P = 0.003), and vigilance (F6,317 = 2.4, P = 0.02). The amount of time spent feeding increased throughout the study, especially at the concentration pond (Fig. 1). At the concentration pond, Godwits spent more time resting in Oct-Nov and Dec-Jan than at other sites. At the mudflat and saltmarsh, the amount of time spent vigilant decreased gradually as the study progressed, while it remained constant at the other sites (Fig. 1). Willets exhibited a more confused pattern in their time activity budgets. The amount of time spent feeding was not different among sites (F3, 231 = 0.3, P = 0.82), nor

Table 1. Average maximum abundance (±SE), of Willets and Marbled Godwits at four sites in the Guerrero NegroLaguna Ojo de Liebre wetland complex, during the nonbreeding season of 2003-2004. Number of sampling visits during each season is given in parentheses. Oct-Nov (6) Site Saltmarsh Mudflat Pumping pond Concentration pond

Marbled Godwit 14 ± 6 386 ± 49 523 ± 208 573 ± 463

Dec-Jan (8)

Feb-Mar (8)

Willet

Marbled Godwit

Willet

Marbled Godwit

Willet

43 ± 14 121 ± 16 347 ± 122 156 ± 97

6±7 155 ± 37 95 ± 29 281 ± 125

21 ± 9 38 ± 4 37 ± 21 50 ± 6

11 ± 10 312 ± 152 10 ± 4 18 ± 17

24 ± 13 65 ± 29 36 ± 20 4±2

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Figure 2. Proportion of pecks (±SE) of Marbled Godwits (open squares) and Willets (filled circles) in the Guerrero Negro-Laguna Ojo de Liebre wetland complex, during the nonbreeding season of 2003-2004. Sample sizes are given above the x axis (Willets/Marbled Godwits). Figure 1. Proportion of time (±SE) devoted to different activities by Marbled Godwit and Willet at four sites in the Guerrero Negro-Laguna Ojo de Liebre wetland complex, during the nonbreeding season of 2003-2004. Sample sizes are given under the x-axis.

among seasons (F2,231 = 1.06, P = 0.34). Although time devoted to roosting exhibited great variation, differences were not significant among sites (F3, 231 = 0.77, P = 0.51), nor among periods (F2,231 = 2.17, P = 0.11). Only the amount of time spent vigilant was significantly affected by site and season (F6,231 = 2.69, P = 0.01). More time was devoted to vigilance in the saltmarsh, where it remained uniform throughout the study. In the mudflat and pumping pond, the amount of time spent vigilant was significantly lower during Feb-Mar than during Oct-Nov. There were no seasonal differences in the concentration pond (Fig. 1).

proportion of pecking decreased throughout the study (Oct-Nov = 0.56 ± 0.05, n = 49; Dec-Jan = 0.42 ± 0.04, n = 67; Feb-Mar = 0.24 ± 0.03, n= 54), while in Willets the use of pecking increased slightly (Oct-Nov = 0.87 ± 0.04, n = 41; Dec-Jan = 0.97 ± 0.02, n = 33; Feb-Mar = 1 ± 0, n = 51). Only Marbled Godwits exhibited differences in the proportion of pecks among sites, and at the concentration pond they used mostly pecking (Fig. 2).

Foraging Behavior The species differed in foraging behavior. Willets were about twice as likely to peck as Marbled Godwits (Fig. 2). Proportion of pecking was affected significantly by species and sites (F3,271 = 4.9, P = 0.002) and by species and seasons (F2,271 = 10.8, P < 0.001). Both species exhibited seasonal differences in the use of pecking. In Marbled Godwits,

Figure 3. Foraging rate (±SE) of Marbled Godwits (open squares) and Willets (filled circles) at four sites in the Guerrero Negro-Laguna Ojo de Liebre wetland complex, during the nonbreeding season of 2003-2004. Sample sizes are given above the x axis (Willets/Marbled Godwits).

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Feeding rate was affected only by the interaction of species and site (F3,271 = 6.2, P < 0.001). Overall, the feeding rate of Willets was more variable among habitats than that of Marbled Godwits. Willets foraged at a higher rate than Marbled Godwits in the mudflat and saltmarsh, while the foraging rate of both species did not differ in the pumping and concentration ponds (Fig. 3). Pecking success was significantly different among seasons (F2,240 = 9.73, P = 0.0001), and affected by the interaction of species and site (F3,240 = 3.6, P = 0.01). Both species had slightly higher pecking success in Dec-Jan than in the other seasons (Willet: Oct-Nov = 0.65 ± 0.04, Dec-Jan = 0.79± 0.03, Feb-Mar = 0.65± 0.03; Marbled Godwit: Oct-Nov = 0.41 ± 0.05, DecJan = 0.54 ± 0.04, Feb-Mar = 0.36 ± 0.05). Marbled Godwits had a similar pecking success at all sites, while Willets had a higher pecking success at the mudflat and saltmarsh (Fig. 4). Probing success of Marbled Godwits was significantly affected by site and season (F6,132 = 3.31, P = 0.004). Although sample size was small (two to eight observations per period in the saltmarsh and pumping pond), probing success varied between seasons at the saltmarsh and concentration pond, while it remained similar throughout the study at the mudflat and pumping pond (Fig. 5).

Figure 5. Seasonal differences in probing success (±SE) of Marbled Godwits at four sites in the Guerrero NegroLaguna Ojo de Liebre wetland complex, during the nonbreeding season of 2003-2004. Sample sizes are given under the x axis.

In most cases, specific types of prey could not be identified because the items were small and were handled quickly (~1 s). However, evident prey items observed in the substrate surface and water column during the work were halophytic flies, polychaetes, bivalves and snails at the mudflat; mostly crabs at the saltmarsh; halophytic flies, bivalves and snails in the pumping pond; and Artemia and halophytic flies in the concentration pond. DISCUSSION

Figure 4. Pecking success (± E) of Marbled Godwits and Willets at four sites in the Guerrero Negro-Laguna Ojo de Liebre wetland complex, during the nonbreeding season of 2003-2004. Sample sizes are given above the x axis (Willets/Marbled Godwits).

At the Guerrero Negro-Laguna Ojo de Liebre wetland complex, Marbled Godwits were more abundant than Willets, reflecting their overall pattern in northwestern Mexico (Mellink et al. 1997; Page et al. 1997; Engilis et al. 1998). For both species, the wintering season is from October to March; individuals start to migrate to their breeding areas, in the north, between March and May, and their peak southward migration is between June and July (Gratto-Trevor 2000; Lowther et al. 2001). Given the patterns of shorebird abundance at Guerrero Negro (Danemann et al. 2002), some mixing of migrant and wintering birds may have occurred in OctoberNovember. This could have influenced some of our results, but our data do not suggest a major effect.

HABITAT USE BY MARBLED GODWIT AND WILLET

In shorebirds, bill morphology influences foraging behavior, prey handling, diet and microhabitat selection (Baker 1979; Gerritsen and van Heezik 1985; Whitfield 1990; Boettcher et al. 1995) and, overall, longbilled species use probing more than shortbilled species (Barbosa and Moreno 1999; Durell 2000). However, sometimes variation in diet and foraging technique cannot be linked to bill morphology (e.g., Eurasian Oystercatchers Haematopus ostralegus, Durell et al. 1993; Ruddy Turnstones Arenaria interpres, Whitfield 1990), and individual differences in foraging skills may arise from genetic, learning and/or competitive pressures (Durell 2000). In our study, Marbled Godwits devoted a greater proportion of time to feeding than Willets, and foraged mostly by probing, suggesting that they rely more heavily on tactile food detection. Willets used a greater proportion of pecking, thus foraging more visually. This difference is in agreement with the proportional size of their bills, which are longer in Marbled Godwits. Foraging technique used by shorebirds can vary among sites due to differences in food abundance and feeding substrate (Whitfield 1990; Barbosa and Moreno 1999). Marbled Godwits foraging at the concentration pond devoted less time to feeding, and pecked proportionally more than individuals using the other sites. These differences in godwits’ foraging behavior may be caused by the hard substrate of crystallizing salts, in which probing is more difficult. Some godwits, at this pond, pecked successfully at halophytic flies and Artemia. Sexual differences in bill length have been associated with differences in foraging behavior and habitat use (Durell 2000). Female Marbled Godwits have bills about 22% longer than males (Gratto-Trevor 2000), and might have affected foraging patterns at our sites, but we did not study sex-mediated differences in habitat use. Willets can use different feeding techniques throughout the non-breeding distribution (Lowther et al. 2001), but at Guerrero Negro, in contrast to Marbled Godwits, they did not exhibit differences in foraging technique, although capture suc-

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cess varied among sites. Willets had greater foraging effort and higher capture success at the mudflats and the saltmarsh, suggesting that there were differences in prey availability among sites. Habitat selection by birds is affected by several factors, and individuals choose among habitats not only in function of prey availability, but also of competition and predation risk (Goss-Custard 1980). Individuals that are more vulnerable or have lower energetic demands may accept lower energetic returns in order to forage in habitats that are safer (Cresswell 1994; Ydenberg et al. 2002; Whitfield 2003). Mudflats supported the highest numbers of Marbled Godwits and Willets. In contrast, at the saltmarsh, population numbers of both species were lowest and birds tended to be more vigilant than at the other sites. The most obvious difference between these sites was the vegetation, the saltmarsh being more enclosed by vegetation, and thus, potentially having a higher risk of predation for shorebirds (Whitfield 2003). One potential explanation for some individuals to use the saltmarsh, with a presumed higher risk of predation, is that it resulted from competitive exclusion of subdominant individuals from the sites that provided greater benefits (e.g., food intake or lower risk of predation). We have no direct information about differences in prey densities among sites, but the foraging success of both species at the saltmarsh was not significantly different from those foraging at the other sites. At all sites, the birds generally foraged in loose flocks of varying individual membership with little obvious dominance structure and conspicuous social interactions among birds were unusual. Interference competition, therefore, did not seem to explain the use of the less “desirable” saltmarsh by some birds. On the other hand, birds with different attributes might specialize in different sites (Ydenberg et al. 2002; Zharikov and Skilleter 2002), and it is possible that some individuals selected the saltmarsh because they were more able to evade predators, benefitting from reduced overall competition there.

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Whereas the activity budgets and foraging strategy of Willets remained uniform throughout the study, Marbled Godwits increased foraging at the expense of vigilance and increased probing over pecking as the season progressed. Previous to northward migration, shorebirds increase their body mass in order to migrate to their breeding grounds (Pienkowsky and Evans 1984), and feeding is a priority over other activities (Metcalfe and Furness 1984). However, changes in time activity budgets can also reflect changes in habitat quality. As the season progresses, foraging by shorebirds can cause depletion of resources or of prey availability, to which birds could adjust by spending more time foraging. Prey depletion does not appear to be the reason for Marbled Godwits’ increase in foraging time and use of probing, as there was no seasonal pattern in foraging success. Rather, a change in priorities during the season might have been the cause of such changes. The lack of seasonal differences in Willets is intriguing. Although diurnal feeding is overall more important for shorebirds (Lourenço et al. 2008), some species engage in, or increase, nocturnal foraging when they need to increase energy acquisition (Pienkowski 1983; Robert and McNeil 1989; Rompré and McNeil 1994; Rojas et al. 1999; Lourenço et al. 2008). It is possible that lack of increased diurnal foraging by Willets resulted from increased nocturnal feeding (logistical aspects prevented us from evaluating this). In this study, Marbled Godwit and Willet, two similarly-sized shorebird species, had different patterns of habitat use and foraging behavior at an important wintering site. Nocturnal foraging, food and predation by sex and age classes might also affect habitat use by these species, and must be studied to fully understand local habitat use and population numbers and, ultimately, provide the capacity to predict the effects of habitat change on these populations. Our study suggests that habitat quality for non-breeding shorebirds depends on both benefits and costs for foraging birds, and that habitat choice by specific individuals is complex and involves condi-

tion- or state-dependent tradeoffs that balance metabolic requirements, safety priorities, and, perhaps, social status or dominance. ACKNOWLEDGMENTS This work was made possible due to financial and logistical support from CICESE and Exportadora de Sal, S. A., respectively. We specially thank M. Domínguez and M. García, who where instrumental during field work. While involved in this work, GA was a student at the University of Guadalajara. We appreciate the improvements in English made by S. McKean. Two anonymous reviewers greatly improved our manuscript. LITERATURE CITED Altman, J. 1974. Observational study of behavior: sampling methods. Behaviour 49: 227-267. Baker, M. C. 1979. Morphological correlates of habitat selection in a community of shorebirds (Charadriiformes). Oikos 33: 121-126. Barbosa, A. and E. Moreno. 1999. Evolution of foraging strategies in shorebirds: An ecomorphological approach. Auk 116: 712-725. Bart, J., S. Brown, B. Harrington and R. I. G. Morrison. 2007. Survey trends of North American shorebirds: population declines or shifting distributions? Journal of Avian Biology 38: 73-82. Bildstein, K. L., G. T. Bancroft, P. J. Dugan, D. H. Gordon, R. M. Erwin, E. Nol, L. X. Payne and S. E. Senner. 1991. Approaches to the conservation of coastal wetlands in the western hemisphere. Wilson Bulletin 103: 218-254. Boettcher, R., S. M. Haig and W. C. Bridges. 1995. Habitat-related factors affecting the distribution of nonbreeding American Avocets in coastal South Carolina. Condor 97: 68-81. Both, C., P. Edelaar and W. Renema. 2003. Interference between the sexes in foraging Bar-tailed Godwits Limosa lapponica. Ardea 91: 268-272. Burger, J., M. A. Howe, D. C. Hahn and J. Chase. 1977. Effects of tide cycles on habitat selection and habitat partitioning by migrating shorebirds. Auk 94: 743758. Burger, J. 1984. Abiotic factors affecting migrant shorebirds. Pages 1-72 in Shorebirds: migration and foraging behaviour (J. Burger and B. L. Olla, Eds.). Behaviour of Marine Animals 6, Plenum, New York. Colwell, M. A. and S. L. Dodd. 1997. Environmental and habitat correlates of pasture use by nonbreeding shorebirds. Condor 99: 337-344. Cresswell, W. 1994. Age-dependent choice of Redshank (Tringa totanus) feeding location: profitability or risk? Journal of Animal Ecology 63: 589-600. Danemann, G., R. Carmona and G. Fernández. 2002. Migratory shorebirds in the Guerrero Negro Saltworks, Baja California Sur, México. Wader Study Group Bulletin 97: 36-41. Danufsky, T. and M. A. Colwell. 2003. Winter shorebird communities and tidal flat characteristics at Humboldt Bay, California. Condor 105: 117-129.

HABITAT USE BY MARBLED GODWIT AND WILLET Davis, C. A. and L. M. Smith. 1998. Behavior of migrant shorebirds in Playas of the Southern High Plains, Texas. Condor 100: 266-276. de Leon, M. T. and L. M. Smith. 1999. Behavior of migrating shorebirds at North Dakota Prairie Potholes. Condor 101: 645-654. Dodd, S. L. and M. A. Colwell. 1996. Seasonal variation in nocturnal and diurnal distributions of nonbreeding shorebirds at North Humboldt Bay, California. Condor 98: 196-207. Durell, S. E. A. Le V. dit, J. D. Goss-Custard and R. W. G. Cladow. 1993. Sex-related differences in diet and feeding method in the Oystercatcher Haematopus ostralegus. Journal of Animal Ecology 62: 205-215. Durell, S. E. A. Le V. dit. 2000. Individual feeding specialization in shorebirds: population consequences and conservation implications. Biological Reviews 75: 503-518. Engilis, A. Jr., L. W. Oring, E. Carrera, J. W. Nelson and A. Martinez-Lopez. 1998. Shorebird surveys in Ensenada Pabellones and Bahia Santa Maria, Sinaloa, Mexico: Critical winter habitats for Pacific Flyway shorebirds. Wilson Bulletin 110: 332-341. Ewald, U. 1997. La industria salinera de México 15601994. Fondo de Cultura Económica. México D.F. Fernández, G. and D. B. Lank. 2006. Sex, age, and body size distributions of Western Sandpipers during the nonbreeding season with respect to local habitat. Condor 108: 547-557. Gerritsen, A. F. C. and Y. M. Van Heezik. 1985. Substrate preference and substrate related foraging behaviour in three Calidris species. Netherlands Journal of Zoology 35: 671-692. Goss-Custard, J. D. 1980. Competition for food and interference among waders. Ardea 68: 31-52. Gratto-Trevor, C. L. 2000. Marbled Godwit (Limosa fedoa). In The Birds of North America, No. 492 (A. Poole and F. Gill, Eds.). The Birds of North America, Inc., Philadelphia, Pennsylvania. Kelly, P. R. and H. L. Cogswell. 1979. Movements and habitat use by wintering populations of Willets and Marbled Godwits. Studies in Avian Biology 2: 69-82. Lourenço, P. M., A. Silva, C. D. Santos, A. C. Miranda, J. P. Granadeiro and J. M. Palmeirim. 2008. The energetic importance of night foraging for waders wintering in a temperate estuary. Acta Oecologica 34: 122-129. Lowther, P. E., H. D. Douglas III and C. L. Gratto-Trevor. 2001. Willet (Catoptrophorus semipalmatus). In The Birds of North America, No. 579 (A. Poole and F. Gill, Eds.). The Birds of North America, Inc., Philadelphia, Pennsylvania. Maimone-Celorio, M.R. and E. Mellink. 2003. Shorebirds and benthic fauna of tidal mudflats in Estero de Punta Banda, Baja California, México. Bulletin of the Southern California Academy of Sciences 102: 26-38. McCaffery, B. J. 1998. Implications of frequent habitat switches in foraging Bar-tailed Godwits. Auk 115: 494-497.

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Mellink. E., E. Palacios and S. González. 1997. Nonbreeding waterbirds of the Delta of the Río Colorado, México. Journal of Field Ornithology 68: 113123. Metcalfe, N. B. and R. W. Furness. 1984. Changing priorities: the effect of pre-migratory fattening on the trade-off between foraging and vigilance. Behavioral Ecology and Sociobiology 15: 203-206. Myers, J. P., R. I. G. Morrison, P. Z. Antas, B. A. Harrington, T. E. Lovejo., M. Sallaberry, S. E. Senner and A. Tarak. 1987. Conservation strategy for migratory species. American Scientist 75: 19-26. Page, G. W., E. Palacios, L. Alfaro, S. González, L. E. Stenzel and M. Jungers. 1997. Numbers of wintering shorebirds in coastal wetlands of Baja California. Journal of Field Ornithology 68: 562-574. Pienkowski, M. W. 1983. Changes in the foraging patterns of plovers in relation to environmental factors. Animal Behavior 31: 244-264. Pienkowsky, M. R. and P. R. Evans. 1984. Migratory behaviour of shorebirds in the western paleartic. Pages 73-123 in Shorebirds: migration and foraging behaviour (J. Burger and B. L. Olla, Eds.). Behaviour of Marine Animals 6, Plenum, New York. Robert, M. and R. McNeil. 1989. Comparative day and night feeding strategies of shorebird species in a tropical environment. Ibis 131: 69-79. Rojas, L. M., R. McNeil, T. Cabana and P. Lachapelle. 1999. Diurnal and nocturnal visual capabilities in shorebirds as a function of their feeding strategies. Brain Behavior and Evolution 53: 29-43. Rompre, G. and R. McNeil. 1994. Seasonal changes in day and night foraging of willets in northeastern Venezuela. Condor 96: 734-738. Shuford, W. D., N. Warnock and R. L. McKernan. 2004. Patterns of shorebird use of the Salton Sea and adjacent Imperial Valley, California. Studies in Avian Biology 27: 61-77. Warnock, S. E. and J. Y. Takekawa. 1995. Habitat preferences of wintering shorebirds in a temporally changing environment: Western Sandpipers in the San Francisco Bay estuary. Auk 112: 920-930. Whitfield, D. P. 1990. Individual feeding specializations of wintering Turnstone Arenaria interpres. Journal of Animal Ecology 59: 193-211. Whitfield, D. P. 2003. Predation by Eurasian Sparrowhawks produces density-dependent mortality of wintering Redshanks. Journal of Animal Ecology 72: 27-35. Ydenberg, R. C., R. W. Butler, D. B. Lank, C. G. Guglielmo, M. Lemon and N. Wolf. 2002. Trade-offs, condition dependence and stopover site selection by migrating sandpipers. Journal of Avian Biology 33: 47-55. Zharikov, Y. and G. A. Skilleter. 2002. Sex-specific intertidal habitat use in subtropically wintering Bar-tailed Godwits. Canadian Journal of Zoology 80: 19181929.