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Sexual dimorphism and body condition of wintering White-rumped Sandpipers in southern BrazilAuthor(s): Angelo L. Scherer, Janete F. M. Scherer, Maria V. Petry, and VictorH. ValiatiSource: The Wilson Journal of Ornithology, 126(3):553-561. 2014.Published By: The Wilson Ornithological SocietyDOI: http://dx.doi.org/10.1676/13-121.1URL: http://www.bioone.org/doi/full/10.1676/13-121.1

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SEXUAL DIMORPHISM AND BODY CONDITION OF WINTERING

WHITE-RUMPED SANDPIPERS IN SOUTHERN BRAZIL

ANGELO L. SCHERER,1,3 JANETE F. M. SCHERER,1

MARIA V. PETRY,3 AND VICTOR H. VALIATI1

ABSTRACT.—We used discriminant function analysis (DFA) of a series of external morphometric measurements, with

confirmation by genetic methods, to develop a simple method to determine the sex of adult White-rumped Sandpipers

(Calidris fuscicollis) wintering in southern Brazil. In total, we evaluated the sexual size dimorphism (SSD) of 82 males and

102 females captured with mist nets during the non-breeding period from 2010–2012 using eight morphological

measurements. We found significant sex differences: females are significantly larger than males in bill and total head and

wing lengths (% SSD 1.0–6.2%). The SSD in skull and bill lengths showed a tendency to maximize the bill length in

females, while males exhibited a greater skull length than females (2.6%). Both males and females showed similar body

mass, and heavier birds were found in the fall before the northward migration. Body condition showed no difference

between the sexes but was higher in the fall than the spring. Molecular sexing showed that DFA would lead to

misclassification of sex. Given this, the use of morphological measurements for sexing non-breeding birds of this species in

the wintering area should be avoided.

Key words: biometrics, body size, Lagoa do Peixe National Park, molecular sexing, shorebirds, wintering site.

Among shorebirds, sexual dimorphism is a

common trait, frequently involving differences in

body size, in which males tend to be smaller than

females (Szekely et al. 2004, Lislevand et al.

2009). Sexual size dimorphism is generally

considered to be the result of intraspecific

competition, differential migration, social domi-

nance, or niche specialization because of morpho-

logical differences or behaviors (Bonduriansky

2007, Coyne et al. 2007, Chenoweth et al. 2008,

Catry et al. 2012). However, other studies have

shown that sexual size dimorphism in shorebirds is

determined by the intensity of sexual selection

acting on males and the agility of the males’

displays (Szekely et al. 2000, Szekely et al. 2004,

Raihani et al. 2006). Most studies of shorebirds are

carried out in breeding areas; however, many

shorebirds spend long periods away from the

breeding grounds, and little is known about how

body size is affected by selection outside of the

breeding season (Szekely et al. 2000).

White-rumped Sandpipers (Calidris fuscicollis)undertake one of the world’s most extreme long-distance migrations. They breed on the high arctic

tundra of northern Canada and Alaska and makeflights over the Atlantic Ocean to winter insouthern South America (Morrison and Roos

1989, Wennerberg et al. 2002, Blanco et al.2006) and even on Elephant Island in Antarctica

(Sander et al. 1988). In southern Brazil, thehighest abundances of the species were observedon the beaches and in the Lagoa do Peixe National

Park (LPNP) in the Rio Grande do Sul State(Resende and Leeuwenberg 1987, Scherer and

Petry 2012). The LPNP is a special site ofconservancy of migratory shorebirds, used as awintering area or stopover point for part of the

population that winters in areas farther south, suchas Patagonia (Morrison and Roos 1989, Harring-ton et al. 1991). White-rumped Sandpipers exhibit

no plumage dimorphism between the sexes.Juvenile females are larger than males, but

distributions in morphological measurements inboth sexes overlap to some extent (Wennerberget al. 2002). One way to solve this problem is to

use discriminant function analyses (DFA) toclassify shorebirds by sex. Birds sexed by DFA

can be used to address questions about intersexualdifferences in habitat use, migration chronology,foraging behavior, and occurrence of sex bias, and

can be used for individuals measured in the past(Durell and Goss-Custard 1996, McCloskey andThompson 2000, Catry et al. 2012). The bill

length has been nominated as the most appropriate

1 Universidade do Vale do Rio dos Sinos, Graduate

Program in Biology, Laboratory of Molecular Biology,

Room 2C116, Centre for Health Sciences, Av. Unisinos,

950, 93022-000, P. O. Box 275, Sao Leopoldo, Rio Grande

do Sul, Brazil.2 Universidade do Vale do Rio dos Sinos, Graduate

Program in Biology, Laboratory of Ornithology and Marine

Animals. Room 2D223, Centre for Health Sciences, Av.

Unisinos, 950, 93022-000, P. O. Box 275, Sao Leopoldo,

Rio Grande do Sul, Brazil.3 Corresponding author; e-mail: alscherer1@gmail.com

The Wilson Journal of Ornithology 126(3):553–561, 2014

553

measure to distinguish the sexes of shorebirds;however, other measures such as wing length,head length, tarsus length, and body mass havealso been used (Harrington and Morrison 1979,Cartar 1984, Meissner 2005, Włodarczyk et al.2011).

The White-rumped Sandpiper is a polygynousspecies in which males display on arenas within alek and compete via dominance hierarchies forfemales; females visit leks for mating and providesole parental care (Szekely and Reynolds 1995,Szekely et al. 2000, Colwell 2010). In shorebirdspecies with reversed sexual size dimorphism(RSD), such as the White-rumped Sandpiper,males are better adapted for acrobatic aerialdisplay because of their smaller body size. Incontrast, females with relatively larger body sizeand longer bills efficiently accumulate energyreserves needed for egg production, incubation,and broad attendance (Jonsson and Alertam 1990,Szekely et al. 2000). Therefore, it is expected thatfemale White-rumped Sandpipers, which aloneprovide parental care, are more physiologicallydeprived of bodily energy stores, so they willarrive in the wintering areas with poorer bodycondition than males, which depart early from thebreeding site and had more time to stay and feedin stopover areas during the southward migration.However, when females leave for the breedingsites, they are larger and heavier than males, andhave better body condition.

Here, we use molecular techniques to determinethe sex of White-rumped Sandpipers from win-tering individuals in LPNP. This technique readilyprovides information about a bird’s sex, even inspecies in which sexual dimorphism in plumagecharacters is obscure or non-existent (Griffithset al. 1998). The main objectives were to: (1)evaluate the presence of SSD in genetically sexedWhite-rumped Sandpipers and determine if dis-criminant models based on biometric data areaccurate to sex adult non-breeding birds, and (2)determine if there are differences in bodycondition between male and female adult non-breeding White-rumped Sandpipers in the springand fall in southern Brazil.

METHODS

Study Area.—Fieldwork was conducted be-tween September 2010 and April 2012, on theRamsar area (Wetlands International 2013) atLPNP (31u 269 S, 51u 109 W and 31u 149 S,50u 549 W), Rio Grande do Sul state, southern

Brazil. This area is an important conservation site:it is part of the Western Hemisphere ShorebirdReserve Network International (WHSRNI) be-cause of its importance as a stopover andwintering site for neotropical migratory shorebirds(Resende and Leeuwenberg 1987, Serrano 2008).During the austral summer, flocks of up to 7,000White-rumped Sandpipers use LPNP as a feeding,molting, and resting area (Resende and Leuween-berg 1987, Morrison and Ross 1989).

Catches and Sampling.—Birds were caughtduring the austral spring (10–21 Sept 2010, 3–12Dec 2010, and 25 Oct–5 Nov 2011) and fall (30Mar–8 Apr 2011 and 17–28 Apr 2012) with mist-nets erected over shallow water at night during anew moon in LPNP. Each bird received a metalband, made of either stainless steel or aluminium,from the Centre for Research and Conservation ofWild Birds of Brazil (CEMAVE). Eight morpho-logical measures were collected from each bird:total head length (head + bill length), skull length(total head without bill), bill length, middle toelength, and tarsus length, (for this measure,Vernier callipers 60.1 mm were used), left winglength, tail length (measured with a ruler with61.0 mm accuracy), and body mass (measuredwith a Pesola scale with 60.1 g accuracy), asdescribed by Deutsche Ornithologen-Gesellschaft(2011). All body measurements of birds weretaken by the same researcher (ALS). All individ-uals captured during the austral summer had theirages determined according to O’Brien et al.(2006). DNA from red blood cells of all birdswas used to sex each individual. Red blood cellswere packaged in an Eppendorf tube containing1,500 ml of absolute ethanol and stored at roomtemperature until analyzed in the laboratory.

Genomic DNA was extracted from bloodsamples using the standard phenol/chloroformand proteinase K extraction followed by ethanolprecipitation (Sambrook et al. 2001). Thereafter,the chromo-helicase-DNA-binding 1 gene (CHD1)was amplified by polymerase chain reaction (PCR)using primers P2 and P8 (Griffiths et al. 1998).These primers amplify introns in the gene, which issituated on both sex chromosomes in birds: maleshave two Z chromosomes, whereas females haveone Z and one W chromosome. The amplifiedintrons on the two chromosomes differ in length.This leads to an amplification of two homologousinseparable bands in males, and two bands ofdifferent lengths in females, which can beseparated by electrophoresis.

554 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 126, No. 3, September 2014

PCR was carried out in 25-ml volumes contain-ing 1 ml of template DNA (100 ng/ml), 0.8 mM ofeach primer and 10.0 mM of PCR Master Mix 2X(Fermentas, Lithuania). The reactions were car-ried out under the following conditions: 94 uC for4 mins, 55 uC for 30 secs, and 72 uC for 1 min,followed by 34 cycles of 92 uC for 30 secs, 50 uCfor 30 secs, 72 uC for 45 secs, and a finalextension in 72 uC for 5 mins. The PCR productswere separated by gel electrophoresis in 10%polyacrylamide gels containing ethidium bromide,using a 1-kb DNA ladder (Life Technologies), andthe gel was scanned using a FluorImager.

Statistical Analysis.—To provide a measure ofthe sexual size dimorphism, the Storer’s index(SI) (Storer 1966) was calculated for eachmeasure following the formula: SI~(Vf {Vm)=½(Vf zVm) � 0:5�, where Vf and Vm are themean values of a measurement in adult femalesand males, respectively. A Student’s t-test wasapplied to evaluate morphological differencesbetween sexes of the wintering birds. Theinteraction effect between sex and season wasassessed using two-way analysis of variance(ANOVA) (Zar 1999), and DFA was applied todata of adult birds of known sex. The performanceof each morphological measurement was evaluat-ed using Wilks’ Lambda, which decreases asdiscriminatory power increases and with theallocation rate of the model (the percentage ofindividuals correctly identified for each sex). Themeasurements that best discriminated betweensexes of White-rumped Sandpipers were selectedto derive a discriminant function model (stepwiseprocedure). For each DFA, the associated cuttingscore (cut-off value) was calculated. White-rumped Sandpipers with a score higher than thecut-off value were classified as females, and thosewith a lower score were classified as males. Thesuccess rate of the classification was assessedapplying the jackknife procedure in which eachcase is classified using a DFA based on all casesexcept the given one (Tabachnick and Fidell1996) and had high accuracy (Dechaume-Mon-charmont et al. 2011). The analyses were applied,even though some of the variables were notnormally distributed, as there is evidence that thisviolation does not inflate the significance of theDFA (Hair et al. 1995). We evaluated the bodycondition of the White-rumped Sandpipers afterthey arrived in the wintering area in the spring andbefore their departure in the fall. We used theresidual body mass from a regression between

body mass (dependent variable) and the cube billlength of each sex as a measure of the bird’s bodycondition (Lislevand et al. 2009). The differencein body condition between sexes and in eachseason was calculated using two-way analysis ofvariance (ANOVA) (Zar 1999). Greater bodycondition indicates higher individual energystores, and these birds are more competitive toperform migration between breeding and winter-ing areas and successfully mate and breed (Choi etal. 2009). All analyses were performed usingSPSS 18.0 (SPSS Inc. 2010), and test differenceswere considered significant when P # 0.05.

RESULTS

Sexual Dimorphism.—Genetic sexing showedthat 82 males and 102 females were represented inthe sample of adult White-rumped Sandpipers thatwere netted. RSD was observed in the adult birds,i.e., females are significantly larger than males inbill length (DSI 6.2%), total head length (DSI1.9%), and wing length (DSI 1.0%). The six othermeasurements showed no significant size differ-ences between sexes. The species showed SSD inskull length, with males being larger than females(DSI 2.6%). Therefore, bill length was negativelycorrelated with skull length (r 5 20.289, P ,

0.001, n 5 184). The difference in total headlength (skull + bill) was mainly caused by largerbill length of females and larger skull length ofmales than females.

No significant differences were observed be-tween seasons in bill and total head and winglengths of White-rumped Sandpipers (P . 0.05)(Fig. 1A–C). Skull (F1,180 5 4.5, P , 0.05) andtarsus length (F1,180 5 11.2, P , 0.001) showedan interaction effect of sex and season. Male skulllengths were longer than that of females only inthe fall, and female tarsus lengths were longerthan that of males in the fall of 2011 than in thefall of 2012 (Fig. 1D, E). No significant differ-ence in body mass or tail or toe length wasobserved between the sexes during the study andin each season. However, gathering the data fromall birds, body mass was higher (F3,176 5 224.8, P, 0.001) in the fall of 2012 than in the othersthree seasons, and in the fall of 2011 than in thetwo spring seasons (Fig. 1F). We used regressionto analyze body mass and date of birds capture; nosignificant differences in bird’s weights wereobserved during the spring in both sexes(Fig. 2A). In the fall months, birds start toincrease in body mass later in March and are

Scherer et al. N SEXUAL DIMORPHISM AND BODY CONDITION 555

FIG. 1. Morphological measurements (means 6 SE) of 184 sexed adult White-rumped Sandpipers captured in the

spring (n 5 41) and fall (n 5 143) in the Lagoa do Peixe National Park, southern Brazil.

556 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 126, No. 3, September 2014

significantly heavier later in April before thenorthward migration to the breeding grounds(Fig. 2B). The mean body mass of males washigher than females in spring and fall (notsignificantly), with males exhibiting a highercorrelation coefficient in the regression. InSeptember 2010, only five individuals werecaptured during migration, and they were alladults sexed as males. Tail length of both sexeswas higher in the fall than in the spring (Fig. 1G)

(F1,176 5 11.6, P , 0.001), and toe length wasonly higher in fall 2011 than fall 2012 (Fig. 1H)(F3,176 5 5.3, P , 0.001).

Discriminant Function Analysis.—Molecularsexing showed that DFA would lead to misclas-sification. Only bill length contributed signifi-cantly to the DFA to identify the sex (Wilks’Lambda 5 0.617, x2 5 87.758, P , 0.001, n 5

184). Based on this single variable, the DFAcorrectly classified 78.8% (95% confidence

FIG. 2. Simple regression of body mass (g) and catch date of sexed adult White-rumped Sandpipers (n 5 184)

wintering in the Lagoa do Peixe National Park, southern Brazil. (A) Bird captures between September–December (spring),

and (B) captures between March–April (fall).

Scherer et al. N SEXUAL DIMORPHISM AND BODY CONDITION 557

interval [CI]: 75.3–82.3%) of all adult White-rumped Sandpipers: 80.4% (CI: 76.8–84.0%) offemales and 76.8% (CI: 73.5–80.3%) of males.The DFA obtained was: DFA 5 1.06 * (billlength) 2 25.547. The cut-off value of this DFAwas 24.10 mm (Fig. 2). A bird with a bill lengthlonger than the cut-off value was classified asfemale, and a bird with a bill length shorter thanthat value was classified as a male. The jackknifevalidation method classified adult birds with thesame accuracy (78.8%) (CI: 75.3–82.3%).

When data were analyzed separately in eachseason, only bill length contributed significantlyto the discriminant function in both. In the spring,the DFA (Wilks’ Lambda 5 0.588, x2 5 20.435,P , 0.001, n 5 41) correctly classified 82.9%(CI: 79.2–86.9%) of all adult birds: 86.4% (CI:82.6–90.5%) of females and 78.9% (CI: 74.9–82.4%) of males. The DFA obtained in springwas: DFA spring 5 1.108 * (bill length) 2

26.489. The cut-off value of the DFA is 23.90 mm.In the fall, the DFA (Wilks’ Lambda 5 0.622, x2

5 66.599, P , 0.001, n 5 143) correctlyclassified 78.3% (CI: 74.8–81.8%) of all adultbirds: 82.5% (CI: 78.8–86.5%) of females and73.0% (CI: 69.4–76.4%) of males. The DFA

obtained in the fall 5 1.047 * (bill length) 2

25.303. The cut-off value of the DFA was24.17 mm. The jackknife validation methodclassified adult birds with the same accuracy ineach season (82.9% [CI: 79.2–86.9%] and 78.3%[CI: 74.9–82.0%], respectively).

Body Condition.—When data from both sexesof White-rumped Sandpipers were pooled, bodymass was significantly correlated with the cube ofbill length (n 5 184, P , 0.001). We found nosignificant difference in the body condition ofmale (mean 5 20.15 6 10.6) and female (mean5 0.12 6 10.0) birds (P 5 0.70). However,significant differences were observed betweenseasons, with birds in better body condition in thefall of 2011 and 2012 than in the spring of 2011and 2012 (F3,176 5 224.1, P , 0.001) (Fig. 3).

DISCUSSION

The White-rumped Sandpiper is a shorebirdwith sexual size dimorphism, i.e., females arelarger than males in bill and total head and winglength in the wintering areas. These findings arein accordance with a study of juveniles in thespecies’ breeding areas of Canada (Wennerberget al. 2002) where they showed some morpholog-

FIG. 3. Body condition (residuals of body mass/cube of bill length) of adult White-rumped Sandpipers (n 5 184)

between spring 2010 to fall 2012 wintering in the Lagoa do Peixe National Park, southern Brazil.

558 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 126, No. 3, September 2014

ical differences across the Arctic tundra, and it ispossible that the captured birds were from theseareas (Antas 1983, Morrison and Roos 1989, ALS,unpubl. data). Studies have reported that sexualsize dimorphism decreases with size whenfemales are the larger sex (Rensch’s rule), suchas in White-rumped Sandpipers, and is determinedby a combination of sexual competition and maleagility (Jonsson and Alertam 1990, Blomqvistet al. 1997, Szekely et al. 2004, Szekely et al.2004). Our results showed low RSD in thespecies, with the highest values observed in billlength (6.2%) and no differences in the body massof both sexes. Additionally, our results of bill andskull SSD showed a pressure to maximize billlength in females, while males exhibited a higherskull length than females. Nebel and Thompson(2011) evaluated the evolution of sexual bill-sizedimorphism in 151 shorebird species and foundthat SSD is more pronounced in bill length as aresource-exploiting trophic character than non-trophic traits such as tarsus and wing length andbody mass. The authors suggest that the compar-ative approach reveals that these patterns are notstrictly the result of contemporary natural orsexual selection but rather reflect the sharedancestry of extant species.

Body mass and tail length overlapped in allmeasurements and did not show any significantdifference between sexes. In the fall, White-rumped Sandpipers were found to be heavier andto have longer tail lengths than in the spring.These differences were mainly caused by moltingprocesses, with the growth of new feathersreplacing those that were old and worn-out byflight, as well as the increase in body weight as aresult of fat accumulation during the stay in thewintering area before the northward migration

(Resende and Leeuwenberg 1987, Harringtonet al. 1991). In the spring months, birds spendtheir energies in molting old flight feathers, andthe body mass of both sexes remain unchanged(Fig. 2A). However in the fall, after molting, thebirds accumulate energies to perform the north-ward migration (Fig. 2B). Therefore, birds havebeen found to be 33.3% heavier in early fall thanwhen they arrive in the wintering area in thespring. As a result, it is known that low foodavailability during the entire feather growthperiod may reduce wing length (Pehrsson 1987)and may compromise the accumulation of energyrequired for the northward migration and repro-duction. As males do not have parental careresponsibilities in the breeding areas, they leavefor the wintering areas before females, shortlyafter egg laying (O’Brien et al. 2006). We wereable to corroborate our findings by observingmales (but no females) of the birds we sexed inSeptember 2010 who arrived in the wintering areain early spring. We suggest the use of themolecular sexing method to evaluate the sex ofnon-breeding White-rumped Sandpipers in thewintering area because of the low accuracy ofDFA. The possibility of using DFA to classifybirds in the spring and again in the fall increasedthe power of bird sex classification of the models.However, males would have often been errone-ously classified (21.1%, 27.0%, respectively) bysimply relating bill length to the cut-off limit thatwas described. In fact, despite bill length showingthe largest SSD (6.2%) compared with othermorphological measurements, this value is stilllow, but similar in size dimorphism and discrim-inant power to other studies of Calidris species(Baker et al. 1999, Meissner 2005, Rodrigueset al. 2008, Lislevand et al. 2009). Dechaume-

TABLE 1. Morphometric measurements for each sex of all White-rumped Sandpipers captured in Lagoa do Peixe

National Park, southern Brazil. Storer’s Index (SI) expressed in percentage; sample number (n); Student’s t-test (t). With the

exception of body mass, for which the unit is grams, all values are given in millimetres. Significant P-values in bold.

Males Females

Measurements Range Mean (SD) n Range Mean (SD) n t P SI (%)

Bill 19.7–25.3 23.28 (1.04) 82 21.3–28.1 24.77 (0.86) 102 10.64 ,0.001 26.2

Body mass 30.0–64.0 43.52 (10.56) 82 28.0–66.0 43.62 (10.04) 102 0.06 0.95 20.2

Total head 35.4–57.2 47.01 (2.18) 82 44.2–52.2 47.89 (1.13) 102 3.30 ,0.01 21.9

Toe 17.0–21.2 19.32 (0.85) 82 15.5–21.2 19.42 (1.01) 102 0.72 0.48 20.5

Tail 43.0–55.0 48.98 (2.68) 82 30.0–61.0 49.31 (3.18) 102 0.77 0.44 20.7

Tarsus 21.6–29.0 25.62 (1.20) 82 19.0–28.0 25.77 (1.64) 102 0.70 0.48 20.6

Wing 112.0–128.0 121.4 (3.52) 82 115.0–131.0 122.6 (2.82) 102 2.34 ,0.05 21.0

Skull 13.2–34.2 23.73 (2.09) 82 19.4–27.7 23.12 (1.09) 102 2.41 ,0.05 2.6

Scherer et al. N SEXUAL DIMORPHISM AND BODY CONDITION 559

Moncharmont et al. (2011) showed that the

discriminant rate increased significantly with

relative sexual dimorphism, and our results are

in line with the described pattern. Given the small

sexual size dimorphism of White-rumped Sand-

pipers, the use of morphological measurements

for sexing non-breeding individuals in the win-

tering areas should be avoided, where different

breeding populations or only one population with

some morphological differences may be repre-

sented (Wennerberg et al. 2002), resulting in

overlapping values between sexes.

Contrary to what we expected, body condition

of both males and females was similar but with

higher values in the fall than in the spring. This is

likely in anticipation of the longer traveling

distance after leaving LPNP during the northward

migration and is more pronounced in species with

long-distance nonstop flights (Choi et al. 2009). In

the fall, both sexes are prepared to have a long

migration to the breeding areas with few stopover

points in northern South America and areas in

United States (e.g., Cheyenne Bottoms, Kansas)

(Antas 1983, Harrington et al. 1986, Canevari

et al. 2001). Our study underscores the importance

of using genetic sexing for sexing White-rumped

Sandpipers because of low sexual size dimor-

phism. Despite the presence of some morpholog-

ical differences between the sexes, both males and

females show similar body mass and body

conditions, with heavier birds found in the fall

before the northward migration. Understanding

the ecology of White-rumped Sandpipers in the

wintering area is of great value in behavioral and

population studies and in the establishment of

an international management plan for species

conservation.

ACKNOWLEDGMENTS

We thank the CEMAVE staff and ICMBio Lagoa do

Peixe National Park staff for their help in the fieldwork and

providing samples of some shorebirds. The research was

funded by FAPERGS (Foundation for the Support of

Research of the State of Rio Grande do Sul). UNISINOS

provided logistical support. Janete de Fatima Martins

Scherer is supported by a fellowship from Conselho

Nacional de Pesquisa e Desenvolvimento (CNPq) and

Angelo Luıs Scherer is supported by a fellowship from

Coordenacao de Aperfeicoamento de Pessoal de Nıvel

Superior (CAPES). The authors are grateful to laboratory

operator Igor Radames de Oliveira (UNISINOS) for the

technical assistance provided, and A. M. Tozetti and L. R.

Oliveira for helpful comments and reviews. White-rumped

Sandpipers were banded with a steel ring with CEMAVE

permission no. 221/2010. Blood samples were taken with

ICMBio permission no. 3159/2010.

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