Trophic niches and feeding relationships of shorebirdsin southern Brazil

Fernando Azevedo Faria . Edélti Faria Albertoni . Leandro Bugoni

Received: 18 October 2017 /Accepted: 19 October 2018 / Published online: 30 October 2018

� Springer Nature B.V. 2018

Abstract Niche theory predicts that sympatric

species should differ in some ecological characteristic,

to allow co-existence and reduce competition for key

resources. Food is critical on wintering grounds and

stopover areas for migratory species that need to

accumulate reserves in order to complete their migra-

tion. Wetlands of the Rio Grande do Sul coastal plain,

in southern Brazil, host several species of shorebirds

with similar morphology, foraging methods and diet.

When these species are in sympatry, some trophic

niche overlap is expected. Diets and trophic niches of

migratory and resident shorebirds were investigated

during the austral summer on Torotama Island, Lagoa

dos Patos Estuary, Brazil. Complementary methods

were used to determine the trophic ecology of three

shorebird species; diet was determined through anal-

ysis of feces and food samples, using stable isotopes of

carbon and nitrogen. The local invertebrate

community was sampled to determine potential prey

and ascertain feeding preferences of birds. Coleoptera

was the most abundant taxon in the feces of all

shorebirds. Trophic niche overlap in the diets was

high, with the widest trophic niche found for the buff-

breasted sandpiper Calidris subruficollis. Isotopic

mixing models indicated differences in the main food

sources of shorebirds. The isotopic niche breadth was

widest for the American golden-plover Pluvialis

dominica. These species, as well as the resident

southern lapwing Vanellus chilensis, consumed some

prey in higher proportions over others, although they

had generalist diets. Migratory species with generalist

habits benefit from heterogeneous environments such

as floodplains during the non-breeding season.

Keywords Diet � Feeding ecology �Macroinvertebrates � Plover � Sandpiper �Stable isotopes

Introduction

During their annual cycle, migratory animals inhabit

and feed in different environments, where it is to their

advantage to exploit a wide range of food resources

(Skagen and Knopf 1994; Skagen and Oman 1996;

Davis and Smith 1998). Shorebirds perform some of

the longest migratory journeys on the planet (Johnson

Handling Editor: Piet Spaak.

F. A. Faria (&) � L. BugoniLaboratório de Aves Aquáticas e Tartarugas Marinhas,

Instituto de Ciências Biológicas, Universidade Federal do

Rio Grande - FURG, Campus Carreiros, Rio Grande,

RS 96203-900, Brazil

e-mail: fernandofariaf@yahoo.com.br

F. A. Faria � E. F. AlbertoniLaboratório de Limnologia, Instituto de Ciências

Biológicas, Universidade Federal do Rio Grande - FURG,

Campus Carreiros, Rio Grande, RS 96203-900, Brazil

123

Aquat Ecol (2018) 52:281–296

https://doi.org/10.1007/s10452-018-9663-6(0123456789().,-volV)(0123456789().,-volV)

http://orcid.org/0000-0002-7339-400Xhttp://orcid.org/0000-0001-5966-4686http://orcid.org/0000-0003-0689-7026http://crossmark.crossref.org/dialog/?doi=10.1007/s10452-018-9663-6&domain=pdfhttp://crossmark.crossref.org/dialog/?doi=10.1007/s10452-018-9663-6&domain=pdfhttps://doi.org/10.1007/s10452-018-9663-6

2003; Gill-Jr. et al. 2005). Several shorebird species

that breed in the Northern Hemisphere migrate south

to spend their non-breeding season in the Southern

Hemisphere during the austral summer. On their

wintering grounds, shorebirds rest, molt their feathers

and feed, storing energy for the next step of the

migration (Piersma et al. 1996; Piersma and Wiersma

1996).

Wetlands are the environments most intensively

used by migratory shorebirds during the staging and

wintering periods. Wetlands are dynamic habitats,

changing with variation in rainfall, tide and seasonal-

ity (Davis and Smith 2001). Commonly, wetlands are

also areas with high productivity and a diversity of

invertebrates (Anderson and Davis 2013). Due to the

dynamic nature of these environments, shorebirds

feeding at these sites probably encounter variations in

the availability of food resources. In response to these

characteristics, most migratory shorebirds are thought

to use generalist dietary regimes to supply their

nutritional requirements (Skagen and Knopf 1994;

Skagen and Oman 1996; Davis and Smith 1998). In

wintering areas, shorebirds must share resources with

resident species, i.e., those that remain in the area

throughout the year (Belton 1994; Piersma and

Wiersma 1996; Vooren 1998).

Coastal plains in the southern Brazilian state of Rio

Grande do Sul, including the estuarine region of the

Lagoa (= Lagoon) dos Patos, are important sites for

migrant birds (Vooren 1998; Bencke et al. 2006).

Previous studies suggest that the estuary is used as a

non-breeding area by thousands of shorebirds, espe-

cially Nearctic plovers and sandpipers (Vooren 1998;

Ferreira et al. 2005; Dias et al. 2017) that use the area

from late September to early March (Vooren and

Chiaradia 1990).

Shorebirds feed on several types of invertebrates

including annelids, insects, crustaceans and mollusks

(Brooks 1967; Isacch et al. 2005). However, it is

necessary to understand more clearly how these

resources are shared, and the importance of each prey

type for different shorebird species. One way to

characterize the structure of communities is through

the analysis of trophic niches (Bearhop et al. 2004).

Hutchinson (1957) defined the ecological niche of a

species as an n-dimensional hypervolume, where the

dimensions are environmental resources and condi-

tions. Occupied niches represent the use of resources

(Bearhop et al. 2004), and ecologists are interested in

how species of the same community utilize these

resources in different ways (Schoener 1974). Investi-

gations of resource partitioning are important to

understand the mechanisms that influence the struc-

ture of communities. If a given resource is superabun-

dant, even with high trophic niche overlap,

competition between different species will not occur

(Pianka 1981).

Several studies have analyzed the diet and trophic

niche of shorebirds by using fecal analysis (e.g., Smith

and Nol 2000; Gillings and Sutherland 2007; Lour-

enço 2007). This technique allows a large number of

samples to be collected with relatively limited effort

and minimal disturbance to the birds, although it may

underestimate the amounts of easily digestible food

items (Ralph et al. 1985).

Since the 1990s, studies on trophic relationships

have used stable isotope analysis (SIA) in tissues of

consumers and their potential prey as a complemen-

tary methodology to conventional dietary analysis

(Karnovsky et al. 2012). While conventional methods

such as fecal analysis provide information on recently

eaten food items, SIA indicates the food assimilated at

different timescales, depending on the turnover rates

of the tissues analyzed (Peterson and Fry 1987).

Stable isotopes of nitrogen (15N/14N, or d15N) provideinformation about the trophic level of individuals

(Hussey et al. 2014), while stable isotopes of carbon

(13C/12C, or d13C) are used to distinguish the origins offood resources, such as marine versus freshwater

environments (Fry 2006; Barrett et al. 2007). In recent

years, researchers have proposed the use of SIA as a

tool to answer questions on trophic niches of species

(e.g., Bearhop et al. 2004; Newsome et al. 2007, 2012;

Catry et al. 2015). Ecological studies using stable iso-

topes present their data in Cartesian spaces, where the

axes represent the relative abundance of each element

(Newsome et al. 2007). The area occupied in this space

is known as the ‘‘isotopic niche’’ and can be consid-

ered as an isotopic proxy for the ecological niche

(Pérez et al. 2008).

Based on the information above, the present study

aimed to describe and compare the trophic niches and

diets of one resident and two migratory shorebird

species in temporary flooded grasslands in an estuarine

area of southern Brazil, using the complementary

methods of fecal analysis and SIA. We hypothesized

that trophic niches of the three most common coex-

isting shorebirds overlap to some degree, making use

123

282 Aquat Ecol (2018) 52:281–296

of abundant food resources, and that these birds have

generalist habits as a consequence of their life strategy

and the need to adapt to different environments during

their annual cycle.

Materials and methods

Study area

The study was conducted in a 60-ha wet grassland area

on Torotama Island (31�550S; 052�100W), Lagoa dosPatos Estuary, in southern Brazil (Fig. 1). This estuary

has an area of approximately 970 km2 (Asmus 1998).

Lunar tides are only 0.5 m at maximum, and thus the

flooding regime is influenced by wind and rainfall

upstream, which ultimately affect the outflow and the

water level of the lagoon as a whole, as well as their

margins (Garcia 1998). Salt marshes occupy intertidal

zones of the estuary and its islands, including Toro-

tama Island. Most of the interior and shores of these

estuarine islands are periodically flooded salt marshes,

with Spartina densiflora and Bolboschoenus mar-

itimus predominating. The sampling site near the shore

of Torotama Island is characterized as intermittently

flooded grassland, where the vegetation is kept low by

intensive livestock grazing (Marangoni and Costa

2009). The study area harbors high density of plovers

and sandpipers, with the highest concentrations of

buff-breasted sandpiper Calidris subruficollis winter-

ing in Brazil (Lanctot et al. 2002; Dias et al. 2011),

specially from mid-October to early February

(Piersma et al. 1996).

Macroinvertebrate sampling

To determine the potential prey of shorebirds, the

macroinvertebrate community was sampled monthly

from December 2014 to February 2015 through

complementary methods to cover different microhab-

itats, aiming to sample most invertebrates available on

the soil surface, water and upper soil, also accounting

for efficiency of each trapping method to different

taxa. The study site was divided into three transects,

200 m apart. On each transect, 3 sampling points

200 m apart were established, with the three methods

used at each point. Each month, we installed a total of

10 pitfalls in each point to collect invertebrates that

move on the soil surface (Triplehorn and Johnson

2011). These traps consisted of plastic pots 6 cm in

diameter and 10 cm high, containing a solution of

water, ethanol and detergent; and remained active for

96 h before removal. We also collected 27 samples of

sediment each month, with a 5-cm-diameter corer, to a

depth of 5 cm (Brandimarte et al. 2004) to capture

benthic invertebrates; and 27 additional environmen-

tal samples with a kick-net (D-shaped, 30 cm wide,

250-lm mesh, covering 1 m; Maltchik et al. 2009) insmall puddles on the area to collect aquatic inverte-

brates such as mollusks, crustaceans and aquatic

insects. By using these three methods, we expected

to have a realistic picture of most invertebrates

available to shorebirds and their relative abundances,

as well as obtain samples for SIA of potential prey of

shorebirds (see below).

All samples were fixed in 70% ethanol-rose Bengal

stain solution. In the laboratory, samples were sieved

with 500-lm-mesh sieves and analyzed under astereoscope (80 9 magnification). Invertebrates were

quantified and identified to the lowest possible taxo-

nomic level, with identification guides (Merritt and

Cummins 1996; Pérez 1998; Mugnai et al. 2010;

Triplehorn and Johnson 2011). Due to small size and

body mass, at least five individuals of the same

taxonomic families had to be pooled for providing

enough material for SIA.

We measured the size of specimens in order to

convert prey size into biomass, measured as mg of ash-

free dry mass, hereafter AFDM. Individuals of known

size were dried to constant mass (60 �C for 48 h) and

Fig. 1 Map of Torotama Island, Lagoa dos Patos Estuary on theRio Grande do Sul coastal plain, southern Brazil. Black filled

circle indicates the study area

123

Aquat Ecol (2018) 52:281–296 283

then incinerated in a muffle furnace (2 h at 550 �C).Samples were weighed after drying and again after

incineration, and the AFDM was calculated as the

difference between dry mass and ash mass (Lourenço

et al. 2016). Values were then used to estimate

biomass available in the environment, as well as

contribution of prey types into the diet.

Sampling of shorebird blood and feces

During the same surveys, birds were trapped at night,

between 20:00 h and 06:00 h, with eight mist nets

(2.6 m high, 12 m long, 36-mm mesh) settled verti-

cally across the grassland. In addition to mist nets,

birds were actively captured by two researchers who

roamed the study area on foot, searching for birds.

When a shorebird was found, one researcher used a

flashlight with 1,000,000 candlepower to disorient it.

Once the bird became disoriented, another researcher

approached and threw a 1-m-diameter ring covered

with a 25-mm-mesh net over it. Approximately 0.1 ml

of blood was obtained with a syringe and needle from

the brachial or tarsal vein of each bird, which were

subsequently released. Blood samples were placed in

plastic vials, and frozen until SIA, as described below.

Diet composition was investigated by analyzing

shorebird droppings. Samples were obtained from

November 2014 to January 2015, after invertebrate

sampling, using visual monitoring (with the aid of

10 9 50 binoculars) of monospecific flocks foraging

during the day in the study area. This procedure ensured

that both fecal samples collected were from the correct

species and that macroinvertebrate sampling represented

potential prey for birds. Only fresh droppings, i.e., still

wet and with an intact shape, were collected, placed

individually in plastic vials with 70% ethanol solution,

and examined under a stereomicroscope.

Prey remains from droppings were identified using

a reference collection of invertebrates collected in the

study area, and with identification guides, as described

in the section on macroinvertebrate sampling. Undi-

gested structures (e.g., coleopteran elytra and mollusk

shells) were inspected, and prey items were identified

to the lowest possible taxonomic level.

Stable isotope analysis

For SIA, samples of whole blood from shorebirds and

potential prey were used. Isotopic values of

four potential sources were selected from a range of

other potential food items sampled and SIA carried

out, based on prey found in fecal and environmental

samples and because they cover aquatic and terrestrial

microhabitats: aquatic coleopterans Hydrophilidae,

grazer mollusks Planorbidae, caterpillars of Lepi-

doptera Noctuidae and Solenopsis invicta ants (Formi-

cidae) (Table 1). Because Lepidoptera and

Formicidae had similar isotopic values, analysis was

made combining both sources a posteriori, as sug-

gested by Phillips et al. (2014). Prey utilized in SI

mixing models also had similar sizes of prey collected

to potential prey analysis, ranging from 0.5 to 2 cm. In

the laboratory, lipids were extracted from the samples

with petroleum ether for 4 h in a Soxhlet apparatus

(Bugoni et al. 2010), assuring that all samples were

lipid-free and under the same standardized treatment.

All samples were then freeze-dried, ground and

homogenized, and * 1 mg of each sample wasplaced in tin capsules for analysis at the Analytical

Chemistry Laboratory at the University of Georgia,

USA. An isotope-ratio mass spectrometer coupled to

an elemental analyzer was used for the SIA of carbon

and nitrogen. Values are provided in delta notation (d),expressed in %, by Eq. 1 from Bond and Hobson(2012), as follows:

d13C or d15N &ð Þ ¼ Rsample=Rstandard� �

�1� �

ð1Þ

where R = 13C/12C or 15N/14N. The international

standard for carbon was Vienna Pee Dee Belemnite

and for nitrogen was atmospheric air. Internal labora-

tory standards were bovine (7.51 ± 0.10% for d15Nand - 21.25 ± 0.07% for d13C) and poplar(- 2.4 ± 0.21% for d15N and - 27.45 ± 0.04%for d13C). Standards were run for every 12 unknownsamples. The precision calculated from repeated

measures of internal standards was ± 0.1% for bothd15N and d13C.

Data analysis

To characterize the invertebrate community of the

study area and assess their relative availability,

invertebrates were identified to the lowest possible

taxonomic level. For the analysis of bird diets,

invertebrates were kept at higher taxonomic levels

(family or order), due to high fragmentation of main

items. In order to convert prey into biomass, measured

123

284 Aquat Ecol (2018) 52:281–296

as mg of AFDM, mean body mass of invertebrate

species collected in environment from the major

groups present in feces were used and prepared as

detailed above.

The relative abundance of food items in the

shorebird diets was compared with one-way ANOVA.

Niche width was calculated using Levin’s measure (B;

Krebs 1999) as in Eq. 2:

B ¼ 1Pp2j

ð2Þ

where pj is the proportion of prey category j in the diet,

based on all fecal samples. Results were standardized

using the method proposed by Hurlbert (1978) for

easier comparison with other studies, as in Eq. 3:

Bst ¼B� 1ð Þn� 1ð Þ ð3Þ

where Bst is the standardized Levin’s measure and

varies between 0 and 1, and n is the number of prey

types found in all shorebird fecal samples. To evaluate

trophic niche overlap, the Schoener index (D;

Schoener 1968) was used, as in Eq. 4:

Dxy ¼ 1�1

2ðRjpxi � pyijÞ ð4Þ

where Dxy = Schoener index; pxi = proportion of

resource i by the total of resources used by species x;

pyi = proportion of resource i by the total of resources

used by species y. This index ranges from 0 (no

overlap) to 1 (complete overlap), and values[ 0.6 aregenerally considered as biologically significant

dietary overlap (Schoener 1968). The average propor-

tion of numerical frequency and the consumed

biomass of each prey were used for calculation both

Bst and Dxy (Lourenço et al. 2016). To calculate mean

values and confidence intervals for both Bst and Dxy,

we first utilized 1000 bootstraps (with replacement),

resampling from biomass values in samples. Levins’s

index calculated for the proportion of every sample

was generated and then standardized. From the pool of

calculated index, standard deviation and confidence

intervals were calculated. Bootstrap for Schoener

index was obtained in spaa package (Zhang 2016).

Themean values were the mean of 1000 estimates, and

confidence intervals were estimated as the 0.025 and

0.975 quantiles of the distribution of index.

The shorebirds’ prey consumption relative to the

biomass of the prey in the environment was deter-

mined based on Manly index (Krebs 1999):

a ¼ ri=pið Þ 1=X

ri=pið Þ� �

; i ¼ 1; 2; . . .;m ð5Þ

where ri = proportion of prey i consumed; pi = pro-

portion of prey i in the environment; and m = number

of prey items in the environment. When a[ (1/m),then prey species i is preferred by the consumer.

Conversely, if a\ (1/m), prey species i is avoided. Todetermine biomass proportion of food ingested, data

from the different methods of invertebrate sampling

were grouped.

Feeding strategies of shorebirds were analyzed

using the graphical method of Costello (1990),

modified by Amundsen et al. (1996). In this method,

information about the feeding ecology of species is

Table 1 Isotopic values of the three potential food items used in Bayesian isotopic mixing models and blood of shorebirds sampledon Torotama Island, Lagoa dos Patos Estuary, southern Brazil, in summer 2014–2015

Taxon d13C (%) d15N (%)

Potential food sources

Mollusca - 17.00 3.97

Coleoptera - 24.70 2.70

Formicidaea - 20.74 9.58

Lepidopteraa - 20.91 9.27

Shorebirds

Buff-breasted sandpiper (n = 10) - 20.25 ± 1.6 9.25 ± 0.6

American golden-plover (n = 6) - 18.28 ± 1.7 10.11 ± 1.2

Southern lapwing (n = 5) - 19.23 ± 1.8 8.93 ± 1.2

aLepidoptera and Formicidae were them grouped a posteriori for analysis, as detailed in stable isotope analysis

123

Aquat Ecol (2018) 52:281–296 285

obtained through the relationship between prey-speci-

fic abundance (Pi) and frequency of occurrence (Fi), as

Eqs. 6 and 7:

%Pi ¼ RSi=RStið Þ � 100 ð6Þ

where Si = number of samples with only prey i;

Sti = total of samples with prey i.

%Fi ¼ Ni=Nð Þ � 100 ð7Þ

where Ni = number of individuals with prey i in

samples; N = total number of samples.

The d15N and d13C values were used to estimate thecontribution of each food item in the shorebird diets.

Bayesian isotopic mixing models were generated in R

software, using the simmr package (Parnell and Inger

2016). Consumer-diet discrimination values used in

the models were 2.9 ± 0.16% and 1.3 ± 0.07%, ford15N and d13C, respectively, based on the discrimina-tion factors for dunlin Calidris alpina in a controlled

experiment (Ogden et al. 2004).

To determine the isotopic niches of shorebirds,

Stable Isotope Bayesian Ellipses in R (SIBER; Jack-

son et al. 2011) were used. Standard ellipse areas

adjusted for small sample sizes (SEAc) were used as a

measure of isotopic niche in d15N and d13C space. Theoverlap area between paired SEAc’s and the respec-

tive percentage of overlap area was calculated man-

ually for each pair of species (Jackson et al. 2011).

Results

A total of 5875 individuals from 29 taxa were

identified in the field collections of macroinvertebrates

(Table 2). The taxonomic groups of Formicidae,

Diptera and Arachnida together comprised 91.3% of

the invertebrates present in the pitfall traps. These

three taxa were also the most frequent in pitfalls

(frequency of occurrence - FO% = 76.7, 67.8 and

55.6, respectively). In kick-net samples, Mollusca

Planorbidae and Hydrobidae were the most frequent

and abundant groups (FO% = 85.2 and 44.4, and

N% = 27.7 and 64.6, respectively). Coleoptera and

Diptera were also frequent in kick-net samples,

present in 63% and 51.8% of samples, respectively.

In sediment samples, Mollusca Planorbidae and

Hydrobidae were again the most abundant groups

(N% = 39.1 and 22.6, respectively), followed by

Crustacea (N% = 13.7), Oligochaeta (N% = 10.1)

and Hirudinea (N% = 7.4).

A total of 112 droppings were collected from the

three selected shorebird species: the resident southern

lapwing Vanellus chilensis (n = 27), migratory Amer-

ican golden-plover Pluvialis dominica (n = 30) and

buff-breasted sandpiper (n = 55). Through undigested

structures, a total of 539 invertebrates of 14 taxa, then

grouped in family or order, were identified in fecal

samples (Table 3). Coleoptera was the most abundant

taxon in the feces of all shorebird species. In addition

to Coleoptera, Formicidae composed 33.5% of items

present in the feces of southern lapwings and lepi-

dopteran larvae (caterpillar) were the second most

abundant item in the American golden-plover

(N% = 25.4) and buff-breasted sandpiper (22.7%)

diets. Seeds were present in samples from all shorebird

species (Table 3). The abundance of items in the feces

did not differ significantly among the species

(F = 0.0093, df = 2, p = 0.99).

The highest trophic niche breadth was found for

buff-breasted sandpiper (Bst = 0.397 and 0.235 con-

sidering numerical frequency and biomass, respec-

tively). The lowest trophic niche breadth was found for

the resident southern lapwing (Bst = 0.212) consider-

ing numerical frequency data. However, using bio-

mass data, American golden-plover had the lowest

trophic niche breath (Bst = 0.172, Table 4). Dietary

similarities ranged from 41 to 79%, and highest

overlap was found between buff-breasted sandpiper

and American golden-plover (Dxy = 0.79 and Dxy-= 0.78 using frequency and biomass data, respec-

tively; Table 4). Based on Manly index values, all

shorebird species consumed some prey items in higher

proportions over others. All species fed on coleopter-

ans in a higher proportion than the proportion of this

taxon in the environment. Caterpillars (Lepidoptera)

had values of a[ 1/m for American golden-ploverand buff-breasted sandpiper. For all shorebird species,

mollusks were consumed in lower proportions than its

abundance in the environment (Table 5).

The graphical method (Amundsen et al. 1996)

indicated a generalist diet for southern lapwing,

American golden-plover and buff-breasted sandpiper,

with most food items placed in the lower left quadrant

of the diagrams (Fig. 2). Coleoptera was located in the

upper right of the graphs for all species, indicating that

shorebird species consumed this taxon in higher

proportions.

123

286 Aquat Ecol (2018) 52:281–296

Between December 2014 and February 2015, 21

shorebirds were captured: southern lapwing (n = 5),

American golden-plover (n = 6) and buff-breasted

sandpiper (n = 10). Nitrogen isotopic values of blood

ranged from d15N = 8.9 ± 1.2% (mean ± 1 SD) forsouthern lapwing to d15N = 10.1 ± 1.2% for Amer-ican golden-plover. Carbon isotope values ranged

from d13C = - 20.25 ± 1.6% (n = 10) for buff-breasted sandpiper to d13C = - 18.3 ± 1.7%(n = 6) for American golden-plover (Table 1;

Fig. 3). The mixing model in simmr indicated that

southern lapwing utilized all potential sources in

similar proportions. However, both migratory species

utilized food sources in different proportions. Both

had a combination of ants and lepidopterans as the

main food sources, but differed in relation to other

sources. While coleopterans were important to buff-

breasted sandpiper, mollusks were important to Amer-

ican golden-plover (Fig. 4).

Table 2 Relative (%) andabsolute abundances

(N) and frequency of

occurrence (FO) of

composition of the

macroinvertebrate

community sampled with

pitfalls, kick-net and

corer samples collected on

Torotama Island, Lagoa dos

Patos Estuary, southern

Brazil, in summer

2014–2015

Taxa Pitfall (90) Kick-net (27) Corer (27)

N N% FO FO% N N% FO FO% N N% FO FO%

Arachnida 134 7.5 61 67.8 8 0.22 5 18.5 5 1.3 2 7.4

Coleoptera 35 2 25 27.8 45 1.25 17 63 8 2.1 5 18.5

Crysomelidae 1 0.1 1 1.1 0 0 0 0 0 0 0 0

Curculionidae 2 0.1 2 2.2 0 0 0 0 0 0 0 0

Dryopidae 0 0 0 0 0 0 0 0 2 0.5 2 7.4

Dytiscidae 6 0.3 5 5.5 22 0.6 8 29.6 0 0 0 0

Elmidae 14 0.8 10 11.1 0 0 0 0 1 0.3 1 3.7

Hydrophilidae 4 0.2 2 2.2 22 0.6 11 40.7 5 1.3 5 18.5

Lampiridae 3 0.2 2 2.2 0 0 0 0 0 0 0 0

Noteridae 0 0 0 0 1 0.03 1 3.7 0 0 0 0

Staphylinidae 5 0.3 5 5.5 0 0 0 0 0 0 0 0

Collembola 4 0.2 3 3.3 0 0 0 0 0 0 0 0

Crustacea 1 0.1 1 1.1 89 2.4 6 0 54 13.7 11 40.7

Diptera 216 12 50 55.6 58 1.57 14 51.8 12 3 7 25.9

Hemiptera 83 4.5 31 34.4 24 0.65 6 22.2 0 0 0 0

Hymenoptera 1288 71.8 69 76.7 1 0.03 1 3.7 3 0.7 3 11.1

Formicidae 1288 71.8 69 76.7 1 0.03 1 3.7 3 0.7 3 11.1

Lepidoptera 14 0.8 10 11.1 1 0.03 1 3.7 0 0 0 0

Noctuidae 14 0.8 10 11.1 1 0.03 1 3.7 0 0 0 0

Mollusca 5 0.3 4 4.4 3414 92.6 24 88.9 243 61.7 17 63

Planorbidae 5 0.3 4 4.4 1020 27.7 23 85.2 154 39.1 16 59.2

Hydrobidae 0 0 0 0 2381 64.6 12 44.4 89 22.6 11 40.7

Ampularidae 0 0 0 0 3 0.08 2 7.4 0 0 0 0

Ancylidae 0 0 0 0 8 0.2 3 11.1 0 0 0 0

Lymneidae 0 0 0 0 1 0.03 1 3.7 0 0 0 0

Physidae 0 0 0 0 1 0.03 1 3.7 0 0 0 0

Orthoptera 6 0.3 6 6.7 0 0 0 0 0 0 0 0

Psocoptera 1 0.1 1 1.1 0 0 0 0 0 0 0 0

Trichoptera 1 0.1 1 1.1 0 0 0 0 0 0 0 0

Zoraptera 6 0.3 4 4.4 0 0 0 0 0 0 0 0

Hirudinea 0 0 0 0 25 0.66 4 14.8 29 7.4 5 18.5

Oligochaeta 0 0 0 0 18 0.47 4 14.8 40 10.1 8 29.6

Odonata 0 0 0 0 4 0.1 3 11.1 0 0 0 0

123

Aquat Ecol (2018) 52:281–296 287

Table

3Absolute

andrelative(%

)abundance

(N),frequency

ofoccurrence

(FO)andbiomass(B)offooditem

sin

fecalsamplesofshorebirdsonTorotamaIsland,Lagoados

PatosEstuary,southernBrazil,betweenDecem

ber

2014andFebruary2015

Taxa

Southernlapwing(n

=27)

American

golden-plover

(n=30)

Buff-breastedsandpiper

(n=55)

FO

NB

FO

NB

FO

NB

FO

FO%

NN%

BB%

FO

FO%

NN%

BB%

FO

FO%

NN%

BB%

Gastropoda

518.5

62.7

3.7

26

723.3

75.3

5.40

31.0

10

18.2

10

4.4

13.70

39.3

GastropodaNI

518.5

62.7

3.7

26

723.3

65.3

4.44

26.5

916.4

94

6.66

19.2

Hydrobidae

00

00

00

00

10

0.76

4.5

11.8

10.4

720.2

Arachnida

414.8

41.8

0.2

1.4

516.7

54.4

0.25

1.5

611

62.7

0.29

0.8

Coleoptera

26

96.3

125

56.6

8.78

61.7

28

93.3

50

47.4

3.80

22.8

48

87.3

113

47.5

7.40

21,4

Coleoptera

NI

10

37.0

27

12.2

2.09

14.7

11

36.7

33

32.5

2.66

15.9

19

34.5

47

18.2

2.95

8.5

Hydrophilidae

829.6

63

28.5

4.25

29.8

930

10

8.8

0.67

4.0

20

36.4

26

11.6

1.75

5.0

Dytiscidae

933.3

15

6.8

1.01

7.1

310

32.6

0.20

1.2

19

34.5

28

12.4

1.88

5.4

Curculionidae

27.4

20.9

0.14

11

3.3

10.9

0.07

0.4

712.7

73.1

0.50

1.5

Ceram

bycidae

27.4

20.9

0.14

13

10

32.6

0.22

1.3

59.1

52.2

0.36

1

Elm

idae

13.7

16

7.2

1.15

8.1

00

00

00

00

00

00

Lepidoptera

311.1

31.4

0.77

5.4

16

53.3

30

25.4

7.41

44.2

21

38.1

52

22.7

13.03

37.5

Diptera

622.2

62.7

0.26

5.3

620

65.3

00.3

712.7

73.9

0.13

0.4

Diptera

NI

622.2

41.8

0.17

1.2

620

65.3

0.04

0.3

59.1

53.1

0.04

0.1

Muscidae

00

00

00

00

00

00

11.8

10.4

0.04

0.1

Chironomidae

27.4

20.9

0.09

0.6

00

00

00

11.8

10.4

0.04

0.1

Form

icidae

830

74

33.5

0.49

3.5

516.7

76.1

0.05

0.3

14

25.4

22

9.8

0.15

0.4

Odonata

27.4

20.9

0.03

0.2

00

00

00

23.6

20.9

0.03

0.1

Hebridae

13.7

10.5

0.01

0.1

00

00

00

00

00

00

Trichoptera

00

00

00

00

00

00

11.8

10.4

0.01

0

Bold

values

arehigher

taxonomic

levels

123

288 Aquat Ecol (2018) 52:281–296

Southern lapwing had 78% probability of consum-

ing mollusks in higher proportions than buff-breasted

sandpiper. In contrast, buff-breasted sandpiper had

75% probability of consuming beetles in higher

proportions than southern lapwing. American

golden-plover had 82% probability of consuming

more ants/lepidopterans than southern lapwing, while

southern lapwing had 82% probability of consuming

more beetles. Finally, buff-breasted sandpiper had

98% probability of consuming more beetles than

American golden-plover, while American golden-

plover had 80% probability of consuming more ants/

lepidopterans.

The highest isotopic niche breath was found for

American golden-plover (SEAc = 7.1), while southern

lapwing and buff-breasted sandpiper had similar values

(SEAc’s 3.12 and 3.38, respectively; Fig. 5). Overall, the

isotopic niche areas overlapped by 35.9% between

American golden-plover SEAc and southern lapwing

SEAc, to 89.3%, between buff-breasted sandpiper SEAc

and American golden-plover SEAc (Table 6).

Discussion

Coleopterans, gastropod mollusks, lepidopteran cater-

pillars and ants were the main food items of the three

shorebirds studied, as inferred by both fecal samples

and SIA in whole blood. Overall, the three shorebirds

had generalist feeding habitats, with 42–79% niche

overlap. Niche partitioning seems to occur mainly on

secondary, but important food items.

Diet of shorebirds inferred by fecal analysis

The three species of shorebirds in this study consumed

some prey items in higher proportions over others, and

preyed on more coleopterans in comparison with the

Table 4 Estimates of standardized Levin’s (Bst) niche breadthand Schoener’s (Dxy) niche overlap based on 1000 bootstrap

samples of the proportion of both estimated frequency (F) and

biomass (B) from prey found in droppings of shorebirds

sampled on Torotama Island, southern Brazil, in summer

2014–2015

Southern lapwing Buff-breasted sandpiper Mean Bst ± SD Bst 95% CI

Buff-breasted sandpiper

F 0.533 (0.401–0.783) – 0.397 ± 0.07 0.238–0.559

B 0.472 (0.243–0.803) 0. 235 ± 0.08 0.105–0.378

American golden-plover

F 0.416 (0.305–0.740) 0.793* (0.638–0.920) 0.285 ± 0.08 0.137–0.529

B 0. 546 (0.239–0.795) 0.777* (0.573–0.950) 0.172 ± 0.007 0.064–0.309

Southern lapwing

F – – 0.212 ± 0.06 0.089–0.347

B 0.283 ± 0.09 0.142–0.432

SD standard deviation, CI confidence interval

The ‘‘*’’ indicates biologically significant dietary overlap (Dxy[ 0.6)

Table 5 Manly selectivity index (a) of the diets of shorebirds on Torotama Island, southern Brazil, in summer 2014–2015

Shorebirds Coleoptera Lepidoptera Hemiptera Diptera Odonata Gastropoda Arachnida Hymenoptera

Southern lapwing 0.733 0.101 0.016 0.039 0.1817 0.001 0.004 0.007

American golden-plover 0.234 0.756 – 0.126 – 0.002 0.004 0.001

Buff-breasted sandpiper 0.260 0.734 – 0.051 0.206 0.001 0.002 0.001

Values of a consider the proportion of macroinvertebrates collected with all sampling methods: kick-net (D-net), pitfalls and corer.Bold values indicate consumption by shorebirds in higher proportions than sampled in environment

123

Aquat Ecol (2018) 52:281–296 289

proportion of this taxon in the environment.

Coleopterans were also the dominant food item in

the diet of Nearctic shorebirds during the non-breed-

ing season in Argentina (Isacch et al. 2005) and in the

diet of upland sandpiper Bartramia longicauda stud-

ied in grasslands in Uruguay (Alfaro et al. 2015).

Although this pattern was found for all species

analyzed, the secondary prey groups were different for

each shorebird species. While ants were frequent on

feces of southern lapwings, lepidopterans were impor-

tant in the diets of American golden-plovers and buff-

breasted sandpipers. Ants were also important food

items for southern lapwings in Uruguay (Caballero-

Sadi et al. 2007). Although in different proportions, all

species consumed seeds. This item is commonly found

in the diet of Charadriiformes inhabiting flooded

grasslands in South America (e.g., Beltzer 1991;

Montalti et al. 2003; Isacch et al. 2005; Alfaro et al.

2015), in addition to leaves and roots, which were

absent in the samples analyzed in this study. Although

common in pitfall samples, ants were avoided by

American golden-plovers and buff-breasted sand-

pipers, possibly because of their production of formic

acid (Isacch et al. 2005), or their high undigestible, and

low calorific content, unsuitable for species aiming to

accumulate fat stores for migration. The consumption

of mollusks in lower proportions than would be

expected from their availability in the environment

may be due to the feeding strategy and bill morphol-

ogy of the shorebirds, which although able to use

different foraging tactics, fed mostly on prey moving

on the soil surface.

Fecal analysis proved to be effective in describing

the feeding ecology of these shorebirds. It was

possible to identify 14 different prey groups, even

soft-bodied prey, and a substantial number of samples

were obtained with minimal disturbance to the birds.

The low vegetation and exposed soil also facilitated

collection of droppings. Although this method enables

prey to be identified, due to high fragmentation and

diversity of items it was not possible to estimate the

body mass and length of items consumed. Moreover,

we found similar results and conclusions regarding

the main food items (and calculated indices in the

current case study) using both frequency and biomass

data, a finding also reported by Lourenço et al. (2016).

Recently, several studies have described members

of Charadriiformes consuming biofilm and seagrass

(phanerogams, genus Zostera), which would hardly be

found in fecal analyses (Lourenço et al. 2017). These

results demonstrate the existence of gaps in our

knowledge of the feeding ecology of shorebirds,

probably due to the limitations of this technique.

These results also make evident the importance of

using methods that complement conventional diet

Fig. 2 Graphical interpretation of food items in the diet ofshorebirds determined by fecal analysis on Torotama Island,

summer 2014–2015. Points represent different taxa found in the

diets: Gas = Mollusca (Gastropoda); Col = Coleoptera;

For = Hymenoptera (Formicidae); Lep = Lepidoptera;

Odo = Odonata; Dip = Diptera; Sem = Seed; Ara = Arach-

nida; Tri = Trichoptera; Hem = Hemiptera

123

290 Aquat Ecol (2018) 52:281–296

analysis, such as SIA (Kuwae et al. 2008, 2012; Robin

et al. 2013; Catry et al. 2015; Lourenço et al. 2016) and

DNA (Gerwing et al. 2016).

Diet of shorebirds inferred by stable isotope

analysis

Mixing models indicated differences in the assimila-

tion of resources by the three species analyzed. For

buff-breasted sandpiper, insects represented by bee-

tles, lepidopterans and/or ants (as sources were

pooled) were the main food sources assimilated,

corroborating the information obtained with the fecal

analyses. For American golden-plovers, sources rep-

resented by lepidopterans and/or ants were important,

corroborating the fecal analysis, in which lepidopter-

ans were the second most frequent taxon. The mixing

model also indicated mollusks (Planorbidae) as an

important source. The mixing model utilized for

southern lapwing also indicated that this species

assimilated all food sources in similar proportions.

Based on fecal analysis, assimilation values of com-

bined sources in mixing models probably reflect the

ingestion of ants.

The fact that mollusks were an important source for

southern lapwings and American golden-plovers,

although less frequent in fecal analyses, suggests that

this source may have been consumed in adjacent

environments such as mudflats, sandy beaches or rice

fields. In this case, blood analysis could have detected

the importance of a source with isotopic values similar

to mollusks used in the model, on a wider geographical

scale.

Trophic and isotopic niches

Fecal and stable isotope analyses indicated niche

overlap between migratory and resident shorebirds

during the non-breeding season on Torotama Island.

However, some resource partitioning, especially for

secondary food sources, was observed. These results

suggest that the area provides different resources that

Fig. 3 Values of d15N and d13C (in %) of potential food items and values in whole blood of shorebirds on Torotama Island. Sourcevalues were corrected for a consumer-diet discrimination factor (2.9% for d15N and 1.3% for d13C)

123

Aquat Ecol (2018) 52:281–296 291

Fig. 4 Output of Bayesianstable isotope mixing

models in simmr package

with intervals of credibility

of 95% (lines) and 50%

(colored symbols). Graphs

show the estimated

contribution of different

potential food sources for

the isotopic values measured

in the whole blood of three

shorebird species on

Torotama Island, southern

Brazil. (Color figure online)

123

292 Aquat Ecol (2018) 52:281–296

can be used by a suite of species. Birds in the same area

but using different microhabitats can have differences

in diet and isotopic signatures in tissues. In some

cases, the use of different microhabitats can be

observed even in the same shorebird species, through

sexual segregation (Catry et al. 2012).

Similar to our findings, Holmes and Pitelka (1968)

found high trophic niche overlap between Calidris

species in a breeding area in Alaska. Davis and Smith

(2001) found high trophic niche overlap in four

shorebirds with similar body sizes during the non-

breeding season, and Kober and Bairlein (2009) also

found strong diet overlap in a study with shorebirds in

the Amazon River delta. However, shorebird commu-

nities in staging and wintering areas in Europe and

Africa had little overlap between isotopic niches

(Catry et al. 2015; Lourenço et al. 2016; Schwemmer

et al. 2016).

We found similar isotopic niche overlap between

species (35–89%), in comparison with 41–79% over-

lap found through fecal analyses. However, fecal

analysis and isotopic mixture models presented some

differences. One possible explanation could be the

timescale of the methods used: while feces reflect the

most recent diet (h), blood has a turnover time of

approximately 2 weeks in shorebirds (Ogden et al.

2004). Therefore, the timescale represented by the

analysis should be taken into account, especially in the

case of migratory animals (Schwemmer et al. 2016). A

tissue with a faster turnover time may reflect a change

in diet based on the availability of food items, which

although abundant can be ephemeral and available at

different timescales. Another possibility is that blood

tissue still reflects food consumed at another foraging

site, as differences in the timing of migration may

represent an important niche-segregation mechanism

between shorebirds (Novcic 2016). In this case, buff-

breasted sandpiper would present high fidelity to the

feeding area, which can be corroborated by the

similarity in the results found through the analysis of

feces and blood. In addition, this species had the

lowest variability in d13C values, used to distinguishthe origins of food resources (Fig. 5; Fry 2006).

Finally, for the analysis of trophic niches, food items

were classified to family or order levels. We therefore

cannot rule out the possibility that segregation might

have been detected in the dietary analysis if prey had

been identified to genus or species level, which would

require a genetic-based approach for fecal analysis.

Based on these results, we concluded that the

resident and both Nearctic migrant shorebirds had

generalist habits during the non-breeding period at our

study site and shared the main food sources. However,

some degree in resource partitioning was evident,

especially in secondary food sources. This strategy

seems to be advantageous for migratory shorebirds, as

they feed in several regions during their annual cycle

and must adapt to the consumption of different prey, in

contrasting environments, and often share resources

with other species (Skagen and Oman 1996; Davis and

Smith 1998; Alfaro et al. 2015).

Notwithstanding, the dietary overlap could poten-

tially be reduced if certain variables not considered in

this study were to be analyzed, such as the prey sizes

and the time of day used for foraging. It is well known

that some shorebird species may feed on the same

Fig. 5 Isotopic niche of shorebirds in delta space (d, in %),based on standard ellipse areas adjusted for small sample sizes

(SEAc) using Stable Isotope Bayesian Ellipses in R (SIBER)

Table 6 Standard ellipse areas for small sample sizes (SEAc), overlap area (%2) and proportion (%) of overlap between shorebirdspecies on Torotama Island, southern Brazil, in summer 2014–2015

Species SEAc Species 1 Species 2 Overlap area (%2) % of Sp. 1 area % of Sp. 2 area

Buff-breasted sandpiper (Csub) 3.38 Csub Vchi 12.5 44.96 48.71

American golden-plover (Pdom) 7.71 Csub Pdom 13.2 89.23 39.09

Southern lapwing (Vchi) 3.12 Pdom Vchi 17.0 35.93 88.86

123

Aquat Ecol (2018) 52:281–296 293

prey, but of different sizes (Lifjeld 1984). However,

even feeding on similar prey, when analyzing resource

use in a larger timescale with stable isotopes, assim-

ilation of different food sources was evident, mainly

by both migratory species. Besides some dietary

overlap, the reliance of shorebirds on a wide diversity

of prey, such as beetles, mollusks, caterpillars and

ants, also reduces the risk of interspecific competition

(Davis and Smith 2001).

This study provided new information on the feeding

ecology of one resident and two migratory species of

shorebirds during the non-breeding season on an

estuarine island in southern Brazil. There is still

limited information on the feeding ecology of Nearctic

migrants during the non-breeding season in South

American grasslands (Kober and Bairlein 2009;

Martı́nez-Curci et al. 2015), and no trophic study has

been conducted in southern Brazilian grasslands. In

addition, the current study was based on the use of

complementary dietary approaches: diets were

inferred both from fecal analysis and from SIA of

blood carbon and nitrogen effectively assimilated

from food sources. SIA, although widely used in

ecological studies of different animal groups, includ-

ing shorebirds (e.g., Catry et al. 2012, 2015; Schwem-

mer et al. 2016), has not previously been used to assess

the feeding ecology of shorebirds in South America.

SIA proved to be an important tool for trophic ecology

studies of shorebirds, particularly when combined

with conventional analyses (Bocher et al. 2014). By

analyzing blood samples, we also obtained informa-

tion on the diet at different timescales, supporting and

complementing the information obtained from fecal

analyses.

In addition to the ecological approach, these results

are important for the conservation of shorebirds in the

Western Hemisphere flyways. Cattle grazing provides

a permanently short-grass feeding area, essential for

some species. The heterogeneity of this area creates

distinct microhabitats and supports a high diversity of

macroinvertebrates, allowing resource partitioning by

their consumers.

Acknowledgements The authors are grateful to theircolleagues for support in field and laboratory work. We thank

Dr. Daiane Carrasco Chaves who helped to identify ants. We are

also grateful to Sandro and Jorge for allowing the collection of

samples on their properties on Torotama Island. The Instituto

Chico Mendes de Conservação da Biodiversidade (ICMBio)

allowed the study to be carried out through License SISBIO No.

44683-2. CEMAVE/ICMBio provided metal bands. Finally, we

are grateful to Dr. Juan Pablo Isacch and Dr. Fabiana Schneck,

and three anonymous reviewers, for their critical review of a

previous version of this paper, and Dr. Silvina Botta for insights

into SIBER analysis. L. Bugoni is a research fellow from the

Brazilian CNPq (Proc. No. 310550/2015-7).

References

Alfaro M, Sandercock BK, Liguori L, Arim M (2015) The diet

of upland sandpipers (Bartramia longicauda) in managed

farmland in their Neotropical non-breeding grounds.

Ornitol Neotrop 26:337–347

Amundsen PA, Gabler HM, Staldvik FJ (1996) A new approach

to graphical analysis of feeding strategy from stomach

contents data—modification of the Costello (1990)

method. J Fish Biol 48:607–614

Anderson JT, Davis CA (2013) Wetland techniques. Springer,

New York

Asmus ML (1998) A Planı́cie Costeira e a Lagoa dos Patos. In:

Seeliger U, Odebrecht C, Castello JP (eds) Os ecossistemas

costeiro e marinho do extremo sul do Brasil. Ecoscientia,

Rio Grande, pp 7–12

Barrett RT, Camphuysen K, Anker-Nilssen T et al (2007) Diet

studies of seabirds: a review and recommendations. ICES J

Mar Sci 64:1675–1691

Bearhop S, Adams CE, Waldron S et al (2004) Determining

trophic niche width: a novel approach using stable isotope

analysis. J Anim Ecol 73:1007–1012

Belton W (1994) Aves do Rio Grande do Sul: distribuição e

biologia. Unisinos, São Leopoldo

Beltzer AH (1991) Aspects of the foraging ecology of the

waders Tringa flavipes,Calidris fuscicollis andCharadrius

collaris (Aves: Scolopacidae; Charadriidae) in Del Cristal

Pond (Santa Fé, Argentine). Stud Neotrop Fauna Environ

26:65–73

Bencke GA, Maurı́cio GN, Develey PF, Goerck JM (eds) (2006)

Áreas importantes para a conservação das aves no Brasil.

Parte I - estados do domı́nio da Mata Atlântica. SAVE

Brasil, São Paulo

Bocher P, Robin F, Kojadinovic J et al (2014) Trophic resource

partitioning within a shorebird community feeding on

intertidal mudflat habitats. J Sea Res 92:115–124

Bond AL, Hobson KA (2012) Reporting stable-isotope ratios in

ecology: recommended terminology, guidelines and best

practices. Waterbirds 35:324–331

Brandimarte AL, Shimizu GY, Anaya M, Kuhlmann ML (2004)

Amostragem de invertebrados bentônicos. In: Bicudo

CEM, Bicudo DC (eds) Amostragem em limnologia. Rima,

São Carlos, pp 213–230

Brooks WS (1967) Organisms consumed by various migrating

shorebirds. Auk 84:128–130

Bugoni L, McGill RAR, Furness RW (2010) The importance of

pelagic longline fishery discards for a seabird community

determined through stable isotope analysis. J Exp Mar Bio

Ecol 391:190–200

Caballero-Sadi D, Rocca P, Achaval F, ClaraM (2007) Dieta del

tero Vanellus chilensis y abundancia de presas en el

Aeropuerto Internacional de Carrasco, Canelones,

123

294 Aquat Ecol (2018) 52:281–296

Uruguay. Inf Técnico No 2 Para el Com Nac Peligro

Aviario 16 pp

Catry T, Alves JA, Gill JA et al (2012) Sex promotes spatial and

dietary segregation in a migratory shorebird during the

non-breeding season. PLoS ONE 7:e33811

Catry T, Lourenço PM, Lopes RJ et al (2015) Structure and

functioning of intertidal food webs along an avian flyway: a

comparative approach using stable isotopes. Funct Ecol

30:468–478

Costello MJ (1990) Predator feeding strategy and prey impor-

tance: a new graphical analysis. J Fish Biol 36:261–263

Davis CA, Smith LM (1998) Behavior of migrant shorebirds in

playas of the Southern High Plains, Texas. Condor

100:266–276

Davis CA, Smith LM (2001) Foraging strategies and niche

dynamics of coexisting shorebirds at stopover sites in the

Southern Great Plains. Auk 118:484–495

Dias RA, Gianuca D, Gianuca AT et al (2011) Estuário da Lagoa

dos Patos. In: Valente RM, Silva JMC, Straube FC,

Nascimento JLX (eds) Conservação de aves migratórias

Neárticas no Brasil. Conservation International Brasil,

Belém, pp 335–341

Dias RA, Maurı́cio GN, Bugoni L (2017) Birds of the Patos

Lagoon Estuary and adjacent coastal waters, southern

Brazil: species assemblages and conservation implications.

Mar Biol Res 13:108–120

Ferreira WLS, Bemvenuti CE, Rosa LC (2005) Effects of the

shorebirds predation on the estuarine macrofauna of the

Patos Lagoon, south Brazil. Thalassas 21:77–82

Fry B (2006) Stable isotope ecology. Springer, New York

Garcia CAE (1998) Caraterı́sticas hidrográficas. In: Seeliger U,

Odebrecht C, Castello JP (eds) Os ecossistemas costeiro e

marinho do extremo sul do Brasil. Ecoscientia, Rio Grande,

pp 18–21

Gerwing TG, Kim J, Hamilton DJ et al (2016) Diet recon-

struction using next-generation sequencing increases the

known ecosystem usage by a shorebird. Auk 133:168–177

Gillings S, Sutherland WJ (2007) Comparative diurnal and

nocturnal diet and foraging in Eurasian golden plovers

Pluvialis apricaria and northern lapwings Vanellus

vanellus wintering on arable farmland. Ardea 95:243–257

Gill-Jr RE, Piersma T, Hufford G et al (2005) Crossing the

ultimate ecological barrier: evidence for an 11000-km-long

nonstop flight from Alaska to New Zealand and eastern

Australia by bar-tailed godwits. Condor 107:1–20

Holmes RT, Pitelka FA (1968) Food overlap among coexisting

sandpipers on northern Alaskan tundra. Syst Zool

17:305–318

Hurlbert SH (1978) The measurement of niche overlap and

some relatives. Ecology 59:67–77

Hussey NE, MacNeil MA, McMeans BC et al (2014) Rescaling

the trophic structure of marine food webs. Ecol Lett

17:239–250

Hutchinson GE (1957) Concluding remarks. Cold Spring Harb

Symp Quant Biol 22:415–427

Isacch JP, Darrieu CA, Martı́nez MM (2005) Food abundance

and dietary relationships among migratory shorebirds

using grasslands during the non-breeding season. Water-

birds 28:238–245

Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing

isotopic niche widths among and within communities:

SIBER—Stable Isotope Bayesian ellipses in R. J Anim

Ecol 80:595–602

Johnson OW (2003) Pacific and American golden-plovers:

reflections on conservation needs. Wader Study Gr Bull

100:10–13

Karnovsky NJ, Hobson KA, Iverson SJ (2012) From lavage to

lipids: estimating diets of seabirds. Mar Ecol Prog Ser

451:263–284

Kober K, Bairlein F (2009) Habitat choice and niche charac-

teristics under poor food conditions. A study on migratory

Nearctic shorebirds in the intertidal flats of Brazil. Ardea

97:31–42

Krebs CJ (1999) Ecological methodology. Addison Wesley

Educational Publishers, California

Kuwae T, Beninger PG, Decottignies P et al (2008) Biofilm

grazing in a higher vertebrate: the western sandpiper,

Calidris mauri. Ecology 89:599–606

Kuwae T, Miyoshi E, Hosokawa S et al (2012) Variable and

complex food web structures revealed by exploring miss-

ing trophic links between birds and biofilm. Ecol Lett

15:347–356

Lanctot RB, Blanco DE, Dias RA et al (2002) Conservation

status of the buff-breasted sandpiper: historic and con-

temporary distribution and abundance in South America.

Wilson Bull 114:44–72

Lifjeld JT (1984) Prey selection in relation to body size and bill

length of five species of waders feeding in the same habitat.

Ornis Scand 15:217–226

Lourenço PM (2007) Analysing faecal samples of ragworm

predators: not just a matter of counting mandibles. Ardea

95:151–155

Lourenço PM, Catry T, Piersma T, Granadeiro JP (2016)

Comparative feeding ecology of shorebirds wintering at

Banc d’Arguin, Mauritania. Estuaries Coast 39:855–865

Lourenço PM, Catry T, Lopes RJ et al (2017) Invisible trophic

links? Quantifying the importance of non-standard food

sources for key intertidal avian predators in the eastern

Atlantic. Mar Ecol Prog Ser 563:219–232

Maltchik L, Stenert C, Spies MR, Siegloch AE (2009) Diversity

and distribution of Ephemeroptera and Trichoptera in

southern Brazil wetlands. J Kansas Entomol Soc

82:160–173

Marangoni JC, Costa CSB (2009) Diagnóstico ambiental das

marismas no estuário da Lagoa dos Patos - RS. Atlântica

31:85–98

Martı́nez-Curci NS, Azpiroz AB, Isacch JP, Elı́as R (2015)

Dietary relationships among Nearctic and Neotropical

migratory shorebirds in a key coastal wetland of South

America. Emu 115:326–334

Merritt RW, Cummins KW (eds) (1996) Aquatic insects of

North America. Kendal/Hunt Publishing Company,

Dubuque

Montalti D, Arambarri AM, Soave GE et al (2003) Seeds in the

diet of the white-rumped sandpiper in Argentina. Water-

birds 26:166–168

Mugnai R, Nessimian JL, Baptista DF (eds) (2010) Manual de

identificação de macroinvertebrados aquáticos do estado

do Rio de Janeiro. Technical Books, Rio de Janeiro

Newsome SD, Del-Rio CM, Bearhop S, Phillips DL (2007) A

niche for isotopic ecology. Front Ecol Environ 5:429–436

123

Aquat Ecol (2018) 52:281–296 295

Newsome SD, Yeakel JD, Wheatley PV, Tinker MT (2012)

Tools for quantifying isotopic niche space and dietary

variation at the individual and population level. J Mammal

93:329–341

Novcic I (2016) Niche dynamics of shorebirds in Delaware Bay:

foraging behavior, habitat choice and migration timing.

Acta Oecol 75:68–76

Ogden LJE, Hobson KA, Lank DB (2004) Blood isotopic (d13Cand d15N) turnover and diet-tissue fractionation factors incaptive dunlin (Calidris alpina pacifica). Auk

121:170–177

Parnell A, Inger R (2016) Stable isotope mixing models in R

with Simmr. https://cran.rproject.org/web/packages/

simmr/simmr.pdf. Accessed 28 Sep 2018

Pérez GR (ed) (1998) Guı́a para el estudio de los macroinver-

tebrados del Departamento de Antioquia. Editorial Pres-

encia Ltda, Bogotá

Pérez GE, Schondube JE, Del-Rio CM (2008) Isótopos esta-

bles en ornitologı́a: una introducción breve. Ornitol Neo-

trop 19:95–112

Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies.

Annu Rev Ecol Syst 18:293–320

Phillips DL, Inger R, Bearhop S et al (2014) Best practices for

use of stable isotope mixing models in food-web studies.

Can J Zool 92:823–835

Pianka ER (1981) Competition and niche theory. In: May RM

(ed) Theoretical ecology principles and applications.

Blackwell, Hoboken, pp 167–196

Piersma T,Wiersma P (1996) Family Charadriidae (plovers). In:

del Hoyo J, Elliot A, Sargatal J (eds) Handbook of the birds

of the world (vol. 3): hoatzin to auks. Lynx Edicions,

Barcelona, pp 384–442

Piersma T, Van-Gils J, Wiersma P (1996) Family Scolopacidae

(sandpipers, snipes and phalaropes). In: del Hoyo J, Elliot

A, Sargatal J (eds) Handbook of the birds of the world (vol.

3): hoatzin to auks. Lynx Edicions, Barcelona, pp 444–526

Ralph CP, Nagata SE, Ralph CJ (1985) Analysis of droppings to

describe diets of small birds. J Field Ornithol 56:165–174

Robin F, Piersma T, Meunier F, Bocher P (2013) Expansion into

an herbivorous niche by a customary carnivore: black-

tailed godwits feeding on rhizomes of Zostera at a newly

established wintering site. Condor 115:340–347

Schoener T (1968) The Anolis lizards of Bimini: resource par-

titioning in a complex fauna. Ecology 49:704–726

Schoener T (1974) Resource partitioning in ecological com-

munities. Science 85:27–39

Schwemmer P, Voigt CC, Corman A et al (2016) Body mass

change and diet switch tracked by stable isotopes indicate

time spent at a stopover site during autumn migration in

dunlins Calidris alpina alpina. J Avian Biol 47:806–814

Skagen SK, Knopf FL (1994) Migrating shorebirds and habitat

dynamics at a prairie wetland complex. Wilson Bull

106:91–105

Skagen SK, Oman HD (1996) Dietary flexibility of shorebirds in

the Western Hemisphere. Can Field-Nat 110:419–444

Smith AC, Nol E (2000) Winter foraging behavior and prey

selection of the semipalmated plover in coastal Venezuela.

Wilson Bull 112:467–472

Triplehorn CA, Johnson NF (eds) (2011) Estudo dos insetos.

Cengage Learning, São Paulo

Vooren CM (1998) Aves marinhas e costeiras. In: Seeliger U,

Odebrecht C, Castello JP (eds) Os ecossistemas costeiro e

marinho do extremo sul do Brasil. Ecoscientia, Rio Grande,

pp 170–176

Vooren CM, Chiaradia A (1990) Seasonal abundance and

behavior of coastal birds on Cassino Beach, Brazil. Ornitol

Neotrop 1:9–24

Zhang J (2016) spaa: SPecies Association Analysis. R package

version 0.2.2. https://cran.r-project.org/web/packages/

spaa/index.html. Accessed 02 Oct 2018

123

296 Aquat Ecol (2018) 52:281–296

https://cran.rproject.org/web/packages/simmr/simmr.pdfhttps://cran.rproject.org/web/packages/simmr/simmr.pdfhttps://cran.r-project.org/web/packages/spaa/index.htmlhttps://cran.r-project.org/web/packages/spaa/index.html

Trophic niches and feeding relationships of shorebirds in southern BrazilAbstractIntroductionMaterials and methodsStudy areaMacroinvertebrate samplingSampling of shorebird blood and fecesStable isotope analysisData analysis

ResultsDiscussionDiet of shorebirds inferred by fecal analysisDiet of shorebirds inferred by stable isotope analysisTrophic and isotopic niches

AcknowledgementsReferences