Aquat Ecol (2018) 52:281–296

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

Trophic niches and feeding relationships of shorebirds in southern

Fernando Azevedo Faria . Ede´lti Faria Albertoni . Leandro Bugoni

Received: 18 October 2017 / Accepted: 19 October 2018 / Published online: 30 October 2018 Ó Springer Nature B.V. 2018

Abstract Niche theory predicts that sympatric community was sampled to determine potential prey species should differ in some ecological characteristic, and ascertain feeding preferences of . Coleoptera to allow co-existence and reduce competition for key was the most abundant taxon in the feces of all resources. Food is critical on wintering grounds and shorebirds. Trophic niche overlap in the diets was stopover areas for migratory species that need to high, with the widest trophic niche found for the buff- accumulate reserves in order to complete their migra- breasted sandpiper Calidris subruficollis. Isotopic tion. Wetlands of the Rio Grande do Sul coastal plain, mixing models indicated differences in the main food in southern Brazil, host several species of shorebirds sources of shorebirds. The isotopic niche breadth was with similar morphology, foraging methods and diet. widest for the American golden-plover Pluvialis When these species are in sympatry, some trophic dominica. These species, as well as the resident niche overlap is expected. Diets and trophic niches of southern chilensis, consumed some migratory and resident shorebirds were investigated prey in higher proportions over others, although they during the austral summer on Torotama Island, Lagoa had generalist diets. Migratory species with generalist dos Patos Estuary, Brazil. Complementary methods habits benefit from heterogeneous environments such were used to determine the trophic ecology of three as floodplains during the non-breeding season. shorebird species; diet was determined through anal- ysis of feces and food samples, using stable isotopes of Keywords Diet Á Feeding ecology Á carbon and nitrogen. The local Macroinvertebrates Á Plover Á Sandpiper Á Stable isotopes

Handling Editor: Piet Spaak.

F. A. Faria (&) Á L. Bugoni Introduction Laborato´rio de Aves Aqua´ticas e Tartarugas Marinhas, ˆ ´ Instituto de Ciencias Biologicas, Universidade Federal do During their annual cycle, migratory inhabit Rio Grande - FURG, Campus Carreiros, Rio Grande, RS 96203-900, Brazil and feed in different environments, where it is to their e-mail: [email protected] advantage to exploit a wide range of food resources (Skagen and Knopf 1994; Skagen and Oman 1996; F. A. Faria Á E. F. Albertoni Davis and Smith 1998). Shorebirds perform some of Laborato´rio de Limnologia, Instituto de Cieˆncias Biolo´gicas, Universidade Federal do Rio Grande - FURG, the longest migratory journeys on the planet (Johnson Campus Carreiros, Rio Grande, RS 96203-900, Brazil 123 282 Aquat Ecol (2018) 52:281–296

2003; Gill-Jr. et al. 2005). Several shorebird species how species of the same community utilize these that breed in the Northern Hemisphere migrate south resources in different ways (Schoener 1974). Investi- to spend their non-breeding season in the Southern gations of resource partitioning are important to Hemisphere during the austral summer. On their understand the mechanisms that influence the struc- wintering grounds, shorebirds rest, molt their feathers ture of communities. If a given resource is superabun- and feed, storing energy for the next step of the dant, even with high trophic niche overlap, migration (Piersma et al. 1996; Piersma and Wiersma competition between different species will not occur 1996). (Pianka 1981). Wetlands are the environments most intensively Several studies have analyzed the diet and trophic used by migratory shorebirds during the staging and niche of shorebirds by using fecal analysis (e.g., Smith wintering periods. Wetlands are dynamic habitats, and Nol 2000; Gillings and Sutherland 2007; Lour- changing with variation in rainfall, tide and seasonal- enc¸o 2007). This technique allows a large number of ity (Davis and Smith 2001). Commonly, wetlands are samples to be collected with relatively limited effort also areas with high productivity and a diversity of and minimal disturbance to the birds, although it may (Anderson and Davis 2013). Due to the underestimate the amounts of easily digestible food dynamic nature of these environments, shorebirds items (Ralph et al. 1985). feeding at these sites probably encounter variations in Since the 1990s, studies on trophic relationships the availability of food resources. In response to these have used stable isotope analysis (SIA) in tissues of characteristics, most migratory shorebirds are thought consumers and their potential prey as a complemen- to use generalist dietary regimes to supply their tary methodology to conventional dietary analysis nutritional requirements (Skagen and Knopf 1994; (Karnovsky et al. 2012). While conventional methods Skagen and Oman 1996; Davis and Smith 1998). In such as fecal analysis provide information on recently wintering areas, shorebirds must share resources with eaten food items, SIA indicates the food assimilated at resident species, i.e., those that remain in the area different timescales, depending on the turnover rates throughout the year (Belton 1994; Piersma and of the tissues analyzed (Peterson and Fry 1987). Wiersma 1996; Vooren 1998). Stable isotopes of nitrogen (15N/14N, or d15N) provide Coastal plains in the southern Brazilian state of Rio information about the trophic level of individuals Grande do Sul, including the estuarine region of the (Hussey et al. 2014), while stable isotopes of carbon Lagoa (= Lagoon) dos Patos, are important sites for (13C/12C, or d13C) are used to distinguish the origins of migrant birds (Vooren 1998; Bencke et al. 2006). food resources, such as marine versus freshwater Previous studies suggest that the estuary is used as a environments (Fry 2006; Barrett et al. 2007). In recent non-breeding area by thousands of shorebirds, espe- years, researchers have proposed the use of SIA as a cially Nearctic plovers and sandpipers (Vooren 1998; tool to answer questions on trophic niches of species Ferreira et al. 2005; Dias et al. 2017) that use the area (e.g., Bearhop et al. 2004; Newsome et al. 2007, 2012; from late September to early March (Vooren and Catry et al. 2015). Ecological studies using stable iso- Chiaradia 1990). topes present their data in Cartesian spaces, where the Shorebirds feed on several types of invertebrates axes represent the relative abundance of each element including annelids, , crustaceans and mollusks (Newsome et al. 2007). The area occupied in this space (Brooks 1967; Isacch et al. 2005). However, it is is known as the ‘‘isotopic niche’’ and can be consid- necessary to understand more clearly how these ered as an isotopic proxy for the ecological niche resources are shared, and the importance of each prey (Pe´rez et al. 2008). type for different shorebird species. One way to Based on the information above, the present study characterize the structure of communities is through aimed to describe and compare the trophic niches and the analysis of trophic niches (Bearhop et al. 2004). diets of one resident and two migratory shorebird Hutchinson (1957) defined the ecological niche of a species in temporary flooded grasslands in an estuarine species as an n-dimensional hypervolume, where the area of southern Brazil, using the complementary dimensions are environmental resources and condi- methods of fecal analysis and SIA. We hypothesized tions. Occupied niches represent the use of resources that trophic niches of the three most common coex- (Bearhop et al. 2004), and ecologists are interested in isting shorebirds overlap to some degree, making use 123 Aquat Ecol (2018) 52:281–296 283 of abundant food resources, and that these birds have specially from mid-October to early February generalist habits as a consequence of their life strategy (Piersma et al. 1996). and the need to adapt to different environments during their annual cycle. Macroinvertebrate sampling

To determine the potential prey of shorebirds, the Materials and methods macroinvertebrate community was sampled monthly from December 2014 to February 2015 through Study area complementary methods to cover different microhab- itats, aiming to sample most invertebrates available on The study was conducted in a 60-ha wet grassland area the soil surface, water and upper soil, also accounting on Torotama Island (31°550S; 052°100W), Lagoa dos for efficiency of each trapping method to different Patos Estuary, in southern Brazil (Fig. 1). This estuary taxa. The study site was divided into three transects, has an area of approximately 970 km2 (Asmus 1998). 200 m apart. On each transect, 3 sampling points Lunar tides are only 0.5 m at maximum, and thus the 200 m apart were established, with the three methods flooding regime is influenced by wind and rainfall used at each point. Each month, we installed a total of upstream, which ultimately affect the outflow and the 10 pitfalls in each point to collect invertebrates that water level of the lagoon as a whole, as well as their move on the soil surface (Triplehorn and Johnson margins (Garcia 1998). Salt marshes occupy intertidal 2011). These traps consisted of plastic pots 6 cm in zones of the estuary and its islands, including Toro- diameter and 10 cm high, containing a solution of tama Island. Most of the interior and shores of these water, ethanol and detergent; and remained active for estuarine islands are periodically flooded salt marshes, 96 h before removal. We also collected 27 samples of with Spartina densiflora and Bolboschoenus mar- sediment each month, with a 5-cm-diameter corer, to a itimus predominating. The sampling site near the shore depth of 5 cm (Brandimarte et al. 2004) to capture of Torotama Island is characterized as intermittently benthic invertebrates; and 27 additional environmen- flooded grassland, where the vegetation is kept low by tal samples with a kick-net (D-shaped, 30 cm wide, intensive livestock grazing (Marangoni and Costa 250-lm mesh, covering 1 m; Maltchik et al. 2009)in 2009). The study area harbors high density of plovers small puddles on the area to collect aquatic inverte- and sandpipers, with the highest concentrations of brates such as mollusks, crustaceans and aquatic buff-breasted sandpiper Calidris subruficollis winter- insects. By using these three methods, we expected ing in Brazil (Lanctot et al. 2002; Dias et al. 2011), 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 a stereoscope (80 9 magnification). Invertebrates were quantified and identified to the lowest possible taxo- nomic level, with identification guides (Merritt and Cummins 1996;Pe´rez 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- Fig. 1 Map of Torotama Island, Lagoa dos Patos Estuary on the Rio Grande do Sul coastal plain, southern Brazil. Black filled free dry mass, hereafter AFDM. Individuals of known circle indicates the study area size were dried to constant mass (60 °C for 48 h) and 123 284 Aquat Ecol (2018) 52:281–296 then incinerated in a muffle furnace (2 h at 550 °C). four potential sources were selected from a range of Samples were weighed after drying and again after other potential food items sampled and SIA carried incineration, and the AFDM was calculated as the out, based on prey found in fecal and environmental difference between dry mass and ash mass (Lourenc¸o samples and because they cover aquatic and terrestrial et al. 2016). Values were then used to estimate microhabitats: aquatic coleopterans Hydrophilidae, biomass available in the environment, as well as grazer mollusks Planorbidae, caterpillars of Lepi- contribution of prey types into the diet. doptera Noctuidae and Solenopsis invicta ants (Formi- cidae) (Table 1). Because Lepidoptera and Sampling of shorebird blood and feces Formicidae had similar isotopic values, analysis was made combining both sources a posteriori, as sug- During the same surveys, birds were trapped at night, gested by Phillips et al. (2014). Prey utilized in SI between 20:00 h and 06:00 h, with eight mist nets mixing models also had similar sizes of prey collected (2.6 m high, 12 m long, 36-mm mesh) settled verti- to potential prey analysis, ranging from 0.5 to 2 cm. In cally across the grassland. In addition to mist nets, the laboratory, lipids were extracted from the samples birds were actively captured by two researchers who with petroleum ether for 4 h in a Soxhlet apparatus roamed the study area on foot, searching for birds. (Bugoni et al. 2010), assuring that all samples were When a shorebird was found, one researcher used a lipid-free and under the same standardized treatment. flashlight with 1,000,000 candlepower to disorient it. All samples were then freeze-dried, ground and Once the became disoriented, another researcher homogenized, and * 1 mg of each sample was approached and threw a 1-m-diameter ring covered placed in tin capsules for analysis at the Analytical with a 25-mm-mesh net over it. Approximately 0.1 ml Chemistry Laboratory at the University of Georgia, of blood was obtained with a syringe and needle from USA. An isotope-ratio mass spectrometer coupled to the brachial or tarsal vein of each bird, which were an elemental analyzer was used for the SIA of carbon subsequently released. Blood samples were placed in and nitrogen. Values are provided in delta notation (d), plastic vials, and frozen until SIA, as described below. expressed in %,byEq.1 from Bond and Hobson Diet composition was investigated by analyzing (2012), as follows: shorebird droppings. Samples were obtained from ÂÃÀÁ d13Cord15N & R =R 1 1 November 2014 to January 2015, after invertebrate ðÞ¼ sample standard À ð Þ sampling, using visual monitoring (with the aid of where R = 13C/12Cor15N/14N. The international 10 9 50 binoculars) of monospecific flocks foraging standard for carbon was Vienna Pee Dee Belemnite during the day in the study area. This procedure ensured and for nitrogen was atmospheric air. Internal labora- that both fecal samples collected were from the correct tory standards were bovine (7.51 ± 0.10% for d15N species and that macroinvertebrate sampling represented and - 21.25 ± 0.07% for d13C) and poplar potential prey for birds. Only fresh droppings, i.e., still (- 2.4 ± 0.21% for d15N and - 27.45 ± 0.04% wet and with an intact shape, were collected, placed for d13C). Standards were run for every 12 unknown individually in plastic vials with 70% ethanol solution, samples. The precision calculated from repeated and examined under a stereomicroscope. measures of internal standards was ± 0.1% for both Prey remains from droppings were identified using d15N and d13C. a reference collection of invertebrates collected in the study area, and with identification guides, as described Data analysis in the section on macroinvertebrate sampling. Undi- gested structures (e.g., coleopteran elytra and mollusk To characterize the invertebrate community of the shells) were inspected, and prey items were identified study area and assess their relative availability, to the lowest possible taxonomic level. invertebrates were identified to the lowest possible taxonomic level. For the analysis of bird diets, Stable isotope analysis invertebrates were kept at higher taxonomic levels (family or order), due to high fragmentation of main For SIA, samples of whole blood from shorebirds and items. In order to convert prey into biomass, measured potential prey were used. Isotopic values of 123 Aquat Ecol (2018) 52:281–296 285

Table 1 Isotopic values of the three potential food items used in Bayesian isotopic mixing models and blood of shorebirds sampled on 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 as mg of AFDM, mean body mass of invertebrate dietary overlap (Schoener 1968). The average propor- species collected in environment from the major tion of numerical frequency and the consumed groups present in feces were used and prepared as biomass of each prey were used for calculation both detailed above. Bst and Dxy (Lourenc¸o et al. 2016). To calculate mean The relative abundance of food items in the values and confidence intervals for both Bst and Dxy, shorebird diets was compared with one-way ANOVA. we first utilized 1000 bootstraps (with replacement), Niche width was calculated using Levin’s measure (B; resampling from biomass values in samples. Levins’s Krebs 1999) as in Eq. 2: index calculated for the proportion of every sample 1 was generated and then standardized. From the pool of B ¼ P ð2Þ calculated index, standard deviation and confidence p2 j intervals were calculated. Bootstrap for Schoener where pj is the proportion of prey category j in the diet, index was obtained in spaa package (Zhang 2016). based on all fecal samples. Results were standardized The mean values were the mean of 1000 estimates, and using the method proposed by Hurlbert (1978) for confidence intervals were estimated as the 0.025 and easier comparison with other studies, as in Eq. 3: 0.975 quantiles of the distribution of index. The shorebirds’ prey consumption relative to the ðÞB À 1 biomass of the prey in the environment was deter- Bst ¼ ð3Þ ðÞn À 1 mined based on Manly index (Krebs 1999): X where Bst is the standardized Levin’s measure and a ¼ ðÞri=pi 1= ðÞri=pi ; i ¼ 1; 2; ...; m ð5Þ varies between 0 and 1, and n is the number of prey types found in all shorebird fecal samples. To evaluate where ri = proportion of prey i consumed; pi = pro- trophic niche overlap, the Schoener index (D; portion of prey i in the environment; and m = number Schoener 1968) was used, as in Eq. 4: of prey items in the environment. When a [ (1/m), 1 then prey species i is preferred by the consumer. D ¼ 1 À ðRjp À p jÞ ð4Þ xy 2 xi yi Conversely, if a \ (1/m), prey species i is avoided. To determine biomass proportion of food ingested, data where Dxy = Schoener index; pxi = proportion of from the different methods of invertebrate sampling resource i by the total of resources used by species x; were grouped. pyi = proportion of resource i by the total of resources Feeding strategies of shorebirds were analyzed used by species y. This index ranges from 0 (no using the graphical method of Costello (1990), overlap) to 1 (complete overlap), and values [ 0.6 are modified by Amundsen et al. (1996). In this method, generally considered as biologically significant information about the feeding ecology of species is 123 286 Aquat Ecol (2018) 52:281–296 obtained through the relationship between prey-speci- Crustacea (N% = 13.7), Oligochaeta (N% = 10.1)

fic abundance (Pi) and frequency of occurrence (Fi), as and Hirudinea (N% = 7.4). Eqs. 6 and 7: A total of 112 droppings were collected from the three selected shorebird species: the resident southern %P ¼ ðÞÂRS =RS 100 ð6Þ i i ti lapwing Vanellus chilensis (n = 27), migratory Amer- where Si = number of samples with only prey i; ican golden-plover Pluvialis dominica (n = 30) and Sti = total of samples with prey i. buff-breasted sandpiper (n = 55). Through undigested structures, a total of 539 invertebrates of 14 taxa, then %F ¼ ðÞÂN =N 100 ð7Þ i i grouped in family or order, were identified in fecal where Ni = number of individuals with prey i in samples (Table 3). Coleoptera was the most abundant samples; N = total number of samples. taxon in the feces of all shorebird species. In addition The d15N and d13C values were used to estimate the to Coleoptera, Formicidae composed 33.5% of items contribution of each food item in the shorebird diets. present in the feces of southern and lepi- Bayesian isotopic mixing models were generated in R dopteran larvae (caterpillar) were the second most software, using the simmr package (Parnell and Inger abundant item in the American golden-plover 2016). Consumer-diet discrimination values used in (N% = 25.4) and buff-breasted sandpiper (22.7%) the models were 2.9 ± 0.16% and 1.3 ± 0.07%, for diets. Seeds were present in samples from all shorebird d15N and d13C, respectively, based on the discrimina- species (Table 3). The abundance of items in the feces tion factors for dunlin Calidris alpina in a controlled did not differ significantly among the species experiment (Ogden et al. 2004). (F = 0.0093, df =2,p = 0.99). To determine the isotopic niches of shorebirds, The highest trophic niche breadth was found for Stable Isotope Bayesian Ellipses in R (SIBER; Jack- buff-breasted sandpiper (Bst = 0.397 and 0.235 con- son et al. 2011) were used. Standard ellipse areas sidering numerical frequency and biomass, respec- adjusted for small sample sizes (SEAc) were used as a tively). The lowest trophic niche breadth was found for 15 13 measure of isotopic niche in d N and d C space. The the resident southern lapwing (Bst = 0.212) consider- overlap area between paired SEAc’s and the respec- ing numerical frequency data. However, using bio- tive percentage of overlap area was calculated man- mass data, American golden-plover had the lowest ually for each pair of species (Jackson et al. 2011). trophic niche breath (Bst = 0.172, Table 4). Dietary similarities ranged from 41 to 79%, and highest overlap was found between buff-breasted sandpiper

Results and American golden-plover (Dxy = 0.79 and Dxy- = 0.78 using frequency and biomass data, respec- A total of 5875 individuals from 29 taxa were tively; Table 4). Based on Manly index values, all identified in the field collections of macroinvertebrates shorebird species consumed some prey items in higher (Table 2). The taxonomic groups of Formicidae, proportions over others. All species fed on coleopter- Diptera and Arachnida together comprised 91.3% of ans in a higher proportion than the proportion of this the invertebrates present in the pitfall traps. These taxon in the environment. Caterpillars (Lepidoptera) three taxa were also the most frequent in pitfalls had values of a [ 1/m for American golden-plover (frequency of occurrence - FO% = 76.7, 67.8 and and buff-breasted sandpiper. For all shorebird species, 55.6, respectively). In kick-net samples, Mollusca mollusks were consumed in lower proportions than its Planorbidae and Hydrobidae were the most frequent abundance in the environment (Table 5). and abundant groups (FO% = 85.2 and 44.4, and The graphical method (Amundsen et al. 1996) N% = 27.7 and 64.6, respectively). Coleoptera and indicated a generalist diet for southern lapwing, Diptera were also frequent in kick-net samples, American golden-plover and buff-breasted sandpiper, present in 63% and 51.8% of samples, respectively. with most food items placed in the lower left quadrant In sediment samples, Mollusca Planorbidae and of the diagrams (Fig. 2). Coleoptera was located in the Hydrobidae were again the most abundant groups upper right of the graphs for all species, indicating that (N% = 39.1 and 22.6, respectively), followed by shorebird species consumed this taxon in higher proportions. 123 Aquat Ecol (2018) 52:281–296 287

Table 2 Relative (%) and Taxa Pitfall (90) Kick-net (27) Corer (27) absolute abundances (N) and frequency of NN% FO FO% NN% FO FO% NN% FO FO% occurrence (FO) of composition of the Arachnida 134 7.5 61 67.8 8 0.22 5 18.5 5 1.3 2 7.4 macroinvertebrate Coleoptera 35 2 25 27.8 45 1.25 17 63 8 2.1 5 18.5 community sampled with Crysomelidae 1 0.1 1 1.1 0 0 0 0 0 0 0 0 pitfalls, kick-net and corer samples collected on Curculionidae 2 0.1 2 2.2 0 0 0 0 0 0 0 0 Torotama Island, Lagoa dos Dryopidae 0 0 0 0 0 0 0 0 2 0.5 2 7.4 Patos Estuary, southern Dytiscidae 6 0.3 5 5.5 22 0.6 8 29.6 0 0 0 0 Brazil, in summer Elmidae 14 0.8 10 11.1 0 0 0 0 1 0.3 1 3.7 2014–2015 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

Between December 2014 and February 2015, 21 Fig. 3). The mixing model in simmr indicated that shorebirds were captured: southern lapwing (n = 5), southern lapwing utilized all potential sources in American golden-plover (n = 6) and buff-breasted similar proportions. However, both migratory species sandpiper (n = 10). Nitrogen isotopic values of blood utilized food sources in different proportions. Both ranged from d15N = 8.9 ± 1.2% (mean ± 1 SD) for had a combination of ants and lepidopterans as the southern lapwing to d15N = 10.1 ± 1.2% for Amer- main food sources, but differed in relation to other ican golden-plover. Carbon isotope values ranged sources. While coleopterans were important to buff- from d13C=- 20.25 ± 1.6% (n = 10) for buff- breasted sandpiper, mollusks were important to Amer- breasted sandpiper to d13C=- 18.3 ± 1.7% ican golden-plover (Fig. 4). (n = 6) for American golden-plover (Table 1;

123 288 123

Table 3 Absolute and relative (%) abundance (N), frequency of occurrence (FO) and biomass (B) of food items in fecal samples of shorebirds on Torotama Island, Lagoa dos Patos Estuary, southern Brazil, between December 2014 and February 2015 Taxa Southern lapwing (n = 27) American golden-plover (n = 30) Buff-breasted sandpiper (n = 55) FO NB FO NB FO NB FO FO% NN% BB% FO FO% NN% BB% FO FO% NN% BB%

Gastropoda 5 18.5 6 2.7 3.7 26 7 23.3 7 5.3 5.40 31.0 10 18.2 10 4.4 13.70 39.3 Gastropoda NI 5 18.5 6 2.7 3.7 26 7 23.3 6 5.3 4.44 26.5 9 16.4 9 4 6.66 19.2 Hydrobidae 0 0 0 0 0 0 0 0 1 0 0.76 4.5 1 1.8 1 0.4 7 20.2 Arachnida 4 14.8 4 1.8 0.2 1.4 5 16.7 5 4.4 0.25 1.5 6 11 6 2.7 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 8 29.6 63 28.5 4.25 29.8 9 30 10 8.8 0.67 4.0 20 36.4 26 11.6 1.75 5.0 Dytiscidae 9 33.3 15 6.8 1.01 7.1 3 10 3 2.6 0.20 1.2 19 34.5 28 12.4 1.88 5.4 Curculionidae 2 7.4 2 0.9 0.14 1 1 3.3 1 0.9 0.07 0.4 7 12.7 7 3.1 0.50 1.5 Cerambycidae 2 7.4 2 0.9 0.14 1 3 10 3 2.6 0.22 1.3 5 9.1 5 2.2 0.36 1 Elmidae 1 3.7 16 7.2 1.15 8.1 0 0 0 0 0 0 0 0 0 0 0 0 Lepidoptera 3 11.1 3 1.4 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 6 22.2 6 2.7 0.26 5.3 6 20 6 5.3 0 0.3 7 12.7 7 3.9 0.13 0.4 Diptera NI 6 22.2 4 1.8 0.17 1.2 6 20 6 5.3 0.04 0.3 5 9.1 5 3.1 0.04 0.1 Muscidae 0 0 0 0 0 0 0 0 0 0 0 0 1 1.8 1 0.4 0.04 0.1 Chironomidae 2 7.4 2 0.9 0.09 0.6 0 0 0 0 0 0 1 1.8 1 0.4 0.04 0.1 Formicidae 8 30 74 33.5 0.49 3.5 5 16.7 7 6.1 0.05 0.3 14 25.4 22 9.8 0.15 0.4 Odonata 2 7.4 2 0.9 0.03 0.2 0 0 0 0 0 0 2 3.6 2 0.9 0.03 0.1 52:281–296 (2018) Ecol Aquat Hebridae 1 3.7 1 0.5 0.01 0.1 0 0 0 0 0 0 0 0 0 0 0 0 Trichoptera 0 0 0 0 0 0 0 0 0 0 0 0 1 1.8 1 0.4 0.01 0 Bold values are higher taxonomic levels Aquat Ecol (2018) 52:281–296 289

Table 4 Estimates of standardized Levin’s (Bst) niche breadth biomass (B) from prey found in droppings of shorebirds and Schoener’s (Dxy) niche overlap based on 1000 bootstrap sampled on Torotama Island, southern Brazil, in summer samples of the proportion of both estimated frequency (F) and 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

Southern lapwing had 78% probability of consum- SEAc, to 89.3%, between buff-breasted sandpiper SEAc ing mollusks in higher proportions than buff-breasted and American golden-plover SEAc (Table 6). sandpiper. In contrast, buff-breasted sandpiper had 75% probability of consuming beetles in higher proportions than southern lapwing. American Discussion golden-plover had 82% probability of consuming more ants/lepidopterans than southern lapwing, while Coleopterans, gastropod mollusks, lepidopteran cater- southern lapwing had 82% probability of consuming pillars and ants were the main food items of the three more beetles. Finally, buff-breasted sandpiper had shorebirds studied, as inferred by both fecal samples 98% probability of consuming more beetles than and SIA in whole blood. Overall, the three shorebirds American golden-plover, while American golden- had generalist feeding habitats, with 42–79% niche plover had 80% probability of consuming more ants/ overlap. Niche partitioning seems to occur mainly on lepidopterans. secondary, but important food items. The highest isotopic niche breath was found for American golden-plover (SEAc = 7.1), while southern Diet of shorebirds inferred by fecal analysis lapwing and buff-breasted sandpiper had similar values (SEAc’s 3.12 and 3.38, respectively; Fig. 5). Overall, the The three species of shorebirds in this study consumed isotopic niche areas overlapped by 35.9% between some prey items in higher proportions over others, and American golden-plover SEAc and southern lapwing preyed on more coleopterans in comparison with the

123 290 Aquat Ecol (2018) 52:281–296

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 (Caballero- Sadi et al. 2007). Although in different proportions, all species consumed seeds. This item is commonly found in the diet of inhabiting flooded grasslands in (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, Fig. 2 Graphical interpretation of food items in the diet of we found similar results and conclusions regarding shorebirds determined by fecal analysis on Torotama Island, the main food items (and calculated indices in the summer 2014–2015. Points represent different taxa found in the diets: Gas = Mollusca (Gastropoda); Col = Coleoptera; current case study) using both frequency and biomass For = Hymenoptera (Formicidae); Lep = Lepidoptera; data, a finding also reported by Lourenc¸o et al. (2016). Odo = Odonata; Dip = Diptera; Sem = Seed; Ara = Arach- Recently, several studies have described members nida; Tri = Trichoptera; Hem = Hemiptera of Charadriiformes consuming biofilm and seagrass (phanerogams, genus Zostera), which would hardly be proportion of this taxon in the environment. found in fecal analyses (Lourenc¸o et al. 2017). These Coleopterans were also the dominant food item in results demonstrate the existence of gaps in our the diet of Nearctic shorebirds during the non-breed- knowledge of the feeding ecology of shorebirds, ing season in Argentina (Isacch et al. 2005) and in the probably due to the limitations of this technique. diet of upland sandpiper Bartramia longicauda stud- These results also make evident the importance of ied in grasslands in Uruguay (Alfaro et al. 2015). using methods that complement conventional diet 123 Aquat Ecol (2018) 52:281–296 291

Fig. 3 Values of d15N and d13C (in %) of potential food items and values in whole blood of shorebirds on Torotama Island. Source values were corrected for a consumer-diet discrimination factor (2.9% for d15N and 1.3% for d13C) analysis, such as SIA (Kuwae et al. 2008, 2012; Robin Based on fecal analysis, assimilation values of com- et al. 2013; Catry et al. 2015; Lourenc¸o et al. 2016) and bined sources in mixing models probably reflect the DNA (Gerwing et al. 2016). ingestion of ants. The fact that mollusks were an important source for Diet of shorebirds inferred by stable isotope southern lapwings and American golden-plovers, analysis although less frequent in fecal analyses, suggests that this source may have been consumed in adjacent Mixing models indicated differences in the assimila- environments such as mudflats, sandy beaches or rice tion of resources by the three species analyzed. For fields. In this case, blood analysis could have detected buff-breasted sandpiper, insects represented by bee- the importance of a source with isotopic values similar tles, lepidopterans and/or ants (as sources were to mollusks used in the model, on a wider geographical pooled) were the main food sources assimilated, scale. corroborating the information obtained with the fecal analyses. For American golden-plovers, sources rep- Trophic and isotopic niches resented by lepidopterans and/or ants were important, corroborating the fecal analysis, in which lepidopter- Fecal and stable isotope analyses indicated niche ans were the second most frequent taxon. The mixing overlap between migratory and resident shorebirds model also indicated mollusks (Planorbidae) as an during the non-breeding season on Torotama Island. important source. The mixing model utilized for However, some resource partitioning, especially for southern lapwing also indicated that this species secondary food sources, was observed. These results assimilated all food sources in similar proportions. suggest that the area provides different resources that

123 292 Aquat Ecol (2018) 52:281–296

Fig. 4 Output of Bayesian stable 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 Aquat Ecol (2018) 52:281–296 293

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 Fig. 5 Isotopic niche of shorebirds in delta space (d,in %), between shorebirds (Novcic 2016). In this case, buff- based on standard ellipse areas adjusted for small sample sizes breasted sandpiper would present high fidelity to the (SEAc) using Stable Isotope Bayesian Ellipses in R (SIBER) feeding area, which can be corroborated by the similarity in the results found through the analysis of can be used by a suite of species. Birds in the same area feces and blood. In addition, this species had the but using different microhabitats can have differences lowest variability in d13C values, used to distinguish in diet and isotopic signatures in tissues. In some the origins of food resources (Fig. 5; Fry 2006). cases, the use of different microhabitats can be Finally, for the analysis of trophic niches, food items observed even in the same shorebird species, through were classified to family or order levels. We therefore sexual segregation (Catry et al. 2012). cannot rule out the possibility that segregation might Similar to our findings, Holmes and Pitelka (1968) have been detected in the dietary analysis if prey had found high trophic niche overlap between Calidris been identified to genus or species level, which would species in a breeding area in Alaska. Davis and Smith require a genetic-based approach for fecal analysis. (2001) found high trophic niche overlap in four Based on these results, we concluded that the shorebirds with similar body sizes during the non- resident and both Nearctic migrant shorebirds had breeding season, and Kober and Bairlein (2009) also generalist habits during the non-breeding period at our found strong diet overlap in a study with shorebirds in study site and shared the main food sources. However, the Amazon River delta. However, shorebird commu- some degree in resource partitioning was evident, nities in staging and wintering areas in Europe and especially in secondary food sources. This strategy Africa had little overlap between isotopic niches seems to be advantageous for migratory shorebirds, as (Catry et al. 2015; Lourenc¸o et al. 2016; Schwemmer they feed in several regions during their annual cycle et al. 2016). and must adapt to the consumption of different prey, in We found similar isotopic niche overlap between contrasting environments, and often share resources species (35–89%), in comparison with 41–79% over- with other species (Skagen and Oman 1996; Davis and lap found through fecal analyses. However, fecal Smith 1998; Alfaro et al. 2015). analysis and isotopic mixture models presented some Notwithstanding, the dietary overlap could poten- differences. One possible explanation could be the tially be reduced if certain variables not considered in timescale of the methods used: while feces reflect the this study were to be analyzed, such as the prey sizes most recent diet (h), blood has a turnover time of and the time of day used for foraging. It is well known approximately 2 weeks in shorebirds (Ogden et al. that some shorebird species may feed on the same

Table 6 Standard ellipse areas for small sample sizes (SEAc), overlap area (%2) and proportion (%) of overlap between shorebird species 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

123 294 Aquat Ecol (2018) 52:281–296 prey, but of different sizes (Lifjeld 1984). However, 44683-2. CEMAVE/ICMBio provided metal bands. Finally, we even feeding on similar prey, when analyzing resource are grateful to Dr. Juan Pablo Isacch and Dr. Fabiana Schneck, and three anonymous reviewers, for their critical review of a use in a larger timescale with stable isotopes, assim- previous version of this paper, and Dr. Silvina Botta for insights ilation of different food sources was evident, mainly into SIBER analysis. L. Bugoni is a research fellow from the by both migratory species. Besides some dietary Brazilian CNPq (Proc. No. 310550/2015-7). 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 References (Davis and Smith 2001). This study provided new information on the feeding Alfaro M, Sandercock BK, Liguori L, Arim M (2015) The diet of upland sandpipers (Bartramia longicauda) in managed ecology of one resident and two migratory species of farmland in their Neotropical non-breeding grounds. shorebirds during the non-breeding season on an Ornitol Neotrop 26:337–347 estuarine island in southern Brazil. There is still Amundsen PA, Gabler HM, Staldvik FJ (1996) A new approach limited information on the feeding ecology of Nearctic to graphical analysis of feeding strategy from stomach contents data—modification of the Costello (1990) migrants during the non-breeding season in South method. J Fish Biol 48:607–614 American grasslands (Kober and Bairlein 2009; Anderson JT, Davis CA (2013) Wetland techniques. Springer, Martı´nez-Curci et al. 2015), and no trophic study has New York been conducted in southern Brazilian grasslands. In Asmus ML (1998) A Planı´cie Costeira e a Lagoa dos Patos. In: Seeliger U, Odebrecht C, Castello JP (eds) Os ecossistemas addition, the current study was based on the use of costeiro e marinho do extremo sul do Brasil. Ecoscientia, complementary dietary approaches: diets were Rio Grande, pp 7–12 inferred both from fecal analysis and from SIA of Barrett RT, Camphuysen K, Anker-Nilssen T et al (2007) Diet blood carbon and nitrogen effectively assimilated studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691 from food sources. SIA, although widely used in Bearhop S, Adams CE, Waldron S et al (2004) Determining ecological studies of different groups, includ- trophic niche width: a novel approach using stable isotope ing shorebirds (e.g., Catry et al. 2012, 2015; Schwem- analysis. J Anim Ecol 73:1007–1012 mer et al. 2016), has not previously been used to assess Belton W (1994) Aves do Rio Grande do Sul: distribuic¸a˜oe biologia. Unisinos, Sa˜o Leopoldo the feeding ecology of shorebirds in South America. Beltzer AH (1991) Aspects of the foraging ecology of the SIA proved to be an important tool for trophic ecology Tringa flavipes, Calidris fuscicollis and Charadrius studies of shorebirds, particularly when combined collaris (Aves: Scolopacidae; ) in Del Cristal with conventional analyses (Bocher et al. 2014). By Pond (Santa Fe´, Argentine). Stud Neotrop Fauna Environ 26:65–73 analyzing blood samples, we also obtained informa- Bencke GA, Maurı´cio GN, Develey PF, Goerck JM (eds) (2006) tion on the diet at different timescales, supporting and A´ reas importantes para a conservac¸a˜o das aves no Brasil. complementing the information obtained from fecal Parte I - estados do domı´nio da Mata Atlaˆntica. SAVE analyses. Brasil, Sa˜o Paulo Bocher P, Robin F, Kojadinovic J et al (2014) Trophic resource In addition to the ecological approach, these results partitioning within a shorebird community feeding on are important for the conservation of shorebirds in the intertidal mudflat habitats. J Sea Res 92:115–124 Western Hemisphere flyways. Cattle grazing provides Bond AL, Hobson KA (2012) Reporting stable-isotope ratios in a permanently short-grass feeding area, essential for ecology: recommended terminology, guidelines and best practices. Waterbirds 35:324–331 some species. The heterogeneity of this area creates Brandimarte AL, Shimizu GY, Anaya M, Kuhlmann ML (2004) distinct microhabitats and supports a high diversity of Amostragem de invertebrados bentoˆnicos. In: Bicudo macroinvertebrates, allowing resource partitioning by CEM, Bicudo DC (eds) Amostragem em limnologia. Rima, their consumers. Sa˜o Carlos, pp 213–230 Brooks WS (1967) Organisms consumed by various migrating shorebirds. Auk 84:128–130 Acknowledgements The authors are grateful to their Bugoni L, McGill RAR, Furness RW (2010) The importance of colleagues for support in field and laboratory work. We thank pelagic longline fishery discards for a seabird community Dr. Daiane Carrasco Chaves who helped to identify ants. We are determined through stable isotope analysis. J Exp Mar Bio also grateful to Sandro and Jorge for allowing the collection of Ecol 391:190–200 samples on their properties on Torotama Island. The Instituto Caballero-Sadi D, Rocca P, Achaval F, Clara M (2007) Dieta del Chico Mendes de Conservac¸a˜o da Biodiversidade (ICMBio) tero Vanellus chilensis y abundancia de presas en el allowed the study to be carried out through License SISBIO No. Aeropuerto Internacional de Carrasco, Canelones, 123 Aquat Ecol (2018) 52:281–296 295

Uruguay. Inf Te´cnico No 2 Para el Com Nac Peligro SIBER—Stable Isotope Bayesian ellipses in R. J Anim Aviario 16 pp Ecol 80:595–602 Catry T, Alves JA, Gill JA et al (2012) Sex promotes spatial and Johnson OW (2003) Pacific and American golden-plovers: dietary segregation in a migratory shorebird during the reflections on conservation needs. Study Gr Bull non-breeding season. PLoS ONE 7:e33811 100:10–13 Catry T, Lourenc¸o PM, Lopes RJ et al (2015) Structure and Karnovsky NJ, Hobson KA, Iverson SJ (2012) From lavage to functioning of intertidal food webs along an avian flyway: a lipids: estimating diets of seabirds. Mar Ecol Prog Ser comparative approach using stable isotopes. Funct Ecol 451:263–284 30:468–478 Kober K, Bairlein F (2009) Habitat choice and niche charac- Costello MJ (1990) Predator feeding strategy and prey impor- teristics under poor food conditions. A study on migratory tance: a new graphical analysis. J Fish Biol 36:261–263 Nearctic shorebirds in the intertidal flats of Brazil. Ardea Davis CA, Smith LM (1998) Behavior of migrant shorebirds in 97:31–42 playas of the Southern High Plains, Texas. Condor Krebs CJ (1999) Ecological methodology. Addison Wesley 100:266–276 Educational Publishers, California Davis CA, Smith LM (2001) Foraging strategies and niche Kuwae T, Beninger PG, Decottignies P et al (2008) Biofilm dynamics of coexisting shorebirds at stopover sites in the grazing in a higher vertebrate: the western sandpiper, Southern Great Plains. Auk 118:484–495 Calidris mauri. Ecology 89:599–606 Dias RA, Gianuca D, Gianuca AT et al (2011) Estua´rio da Lagoa Kuwae T, Miyoshi E, Hosokawa S et al (2012) Variable and dos Patos. In: Valente RM, Silva JMC, Straube FC, complex food web structures revealed by exploring miss- Nascimento JLX (eds) Conservac¸a˜o de aves migrato´rias ing trophic links between birds and biofilm. Ecol Lett Nea´rticas no Brasil. Conservation International Brasil, 15:347–356 Bele´m, pp 335–341 Lanctot RB, Blanco DE, Dias RA et al (2002) Conservation Dias RA, Maurı´cio GN, Bugoni L (2017) Birds of the Patos status of the buff-breasted sandpiper: historic and con- Lagoon Estuary and adjacent coastal waters, southern temporary distribution and abundance in South America. Brazil: species assemblages and conservation implications. Wilson Bull 114:44–72 Mar Biol Res 13:108–120 Lifjeld JT (1984) Prey selection in relation to body size and bill Ferreira WLS, Bemvenuti CE, Rosa LC (2005) Effects of the length of five species of waders feeding in the same habitat. shorebirds predation on the estuarine macrofauna of the Ornis Scand 15:217–226 Patos Lagoon, south Brazil. Thalassas 21:77–82 Lourenc¸o PM (2007) Analysing faecal samples of ragworm Fry B (2006) Stable isotope ecology. Springer, New York predators: not just a matter of counting mandibles. Ardea Garcia CAE (1998) Caraterı´sticas hidrogra´ficas. In: Seeliger U, 95:151–155 Odebrecht C, Castello JP (eds) Os ecossistemas costeiro e Lourenc¸o PM, Catry T, Piersma T, Granadeiro JP (2016) marinho do extremo sul do Brasil. Ecoscientia, Rio Grande, Comparative feeding ecology of shorebirds wintering at pp 18–21 Banc d’Arguin, Mauritania. Estuaries Coast 39:855–865 Gerwing TG, Kim J, Hamilton DJ et al (2016) Diet recon- Lourenc¸o PM, Catry T, Lopes RJ et al (2017) Invisible trophic struction using next-generation sequencing increases the links? Quantifying the importance of non-standard food known ecosystem usage by a shorebird. Auk 133:168–177 sources for key intertidal avian predators in the eastern Gillings S, Sutherland WJ (2007) Comparative diurnal and Atlantic. Mar Ecol Prog Ser 563:219–232 nocturnal diet and foraging in Eurasian golden plovers Maltchik L, Stenert C, Spies MR, Siegloch AE (2009) Diversity Pluvialis apricaria and northern lapwings Vanellus and distribution of Ephemeroptera and Trichoptera in vanellus wintering on arable farmland. Ardea 95:243–257 southern Brazil wetlands. J Kansas Entomol Soc Gill-Jr RE, Piersma T, Hufford G et al (2005) Crossing the 82:160–173 ultimate ecological barrier: evidence for an 11000-km-long Marangoni JC, Costa CSB (2009) Diagno´stico ambiental das nonstop flight from Alaska to New Zealand and eastern marismas no estua´rio da Lagoa dos Patos - RS. Atlaˆntica Australia by bar-tailed godwits. Condor 107:1–20 31:85–98 Holmes RT, Pitelka FA (1968) Food overlap among coexisting Martı´nez-Curci NS, Azpiroz AB, Isacch JP, Elı´as R (2015) sandpipers on northern Alaskan tundra. Syst Zool Dietary relationships among Nearctic and Neotropical 17:305–318 migratory shorebirds in a key coastal wetland of South Hurlbert SH (1978) The measurement of niche overlap and America. Emu 115:326–334 some relatives. Ecology 59:67–77 Merritt RW, Cummins KW (eds) (1996) Aquatic insects of Hussey NE, MacNeil MA, McMeans BC et al (2014) Rescaling North America. Kendal/Hunt Publishing Company, the trophic structure of marine food webs. Ecol Lett Dubuque 17:239–250 Montalti D, Arambarri AM, Soave GE et al (2003) Seeds in the Hutchinson GE (1957) Concluding remarks. Cold Spring Harb diet of the white-rumped sandpiper in Argentina. Water- Symp Quant Biol 22:415–427 birds 26:166–168 Isacch JP, Darrieu CA, Martı´nez MM (2005) Food abundance Mugnai R, Nessimian JL, Baptista DF (eds) (2010) Manual de and dietary relationships among migratory shorebirds identificac¸a˜o de macroinvertebrados aqua´ticos do estado using grasslands during the non-breeding season. Water- do . Technical Books, Rio de Janeiro birds 28:238–245 Newsome SD, Del-Rio CM, Bearhop S, Phillips DL (2007) A Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing niche for isotopic ecology. Front Ecol Environ 5:429–436 isotopic niche widths among and within communities: 123 296 Aquat Ecol (2018) 52:281–296

Newsome SD, Yeakel JD, Wheatley PV, Tinker MT (2012) Ralph CP, Nagata SE, Ralph CJ (1985) Analysis of droppings to Tools for quantifying isotopic niche space and dietary describe diets of small birds. J Field Ornithol 56:165–174 variation at the individual and population level. J Mammal Robin F, Piersma T, Meunier F, Bocher P (2013) Expansion into 93:329–341 an herbivorous niche by a customary carnivore: black- Novcic I (2016) Niche dynamics of shorebirds in Delaware Bay: tailed godwits feeding on rhizomes of Zostera at a newly foraging behavior, habitat choice and migration timing. established wintering site. Condor 115:340–347 Acta Oecol 75:68–76 Schoener T (1968) The Anolis lizards of Bimini: resource par- Ogden LJE, Hobson KA, Lank DB (2004) Blood isotopic (d13C titioning in a complex fauna. Ecology 49:704–726 and d15N) turnover and diet-tissue fractionation factors in Schoener T (1974) Resource partitioning in ecological com- captive dunlin (Calidris alpina pacifica). Auk munities. Science 85:27–39 121:170–177 Schwemmer P, Voigt CC, Corman A et al (2016) Body mass Parnell A, Inger R (2016) Stable isotope mixing models in R change and diet switch tracked by stable isotopes indicate with Simmr. https://cran.rproject.org/web/packages/ time spent at a stopover site during autumn migration in simmr/simmr.pdf. Accessed 28 Sep 2018 dunlins Calidris alpina alpina. J Avian Biol 47:806–814 Pe´rez GR (ed) (1998) Guı´a para el estudio de los macroinver- Skagen SK, Knopf FL (1994) Migrating shorebirds and habitat tebrados del Departamento de Antioquia. Editorial Pres- dynamics at a prairie wetland complex. Wilson Bull encia Ltda, Bogota´ 106:91–105 Pe´rez GE, Schondube JE, Del-Rio CM (2008) Iso´topos esta- Skagen SK, Oman HD (1996) Dietary flexibility of shorebirds in bles en ornitologı´a: una introduccio´n breve. Ornitol Neo- the Western Hemisphere. Can Field-Nat 110:419–444 trop 19:95–112 Smith AC, Nol E (2000) Winter foraging behavior and prey Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. selection of the semipalmated plover in coastal Venezuela. Annu Rev Ecol Syst 18:293–320 Wilson Bull 112:467–472 Phillips DL, Inger R, Bearhop S et al (2014) Best practices for Triplehorn CA, Johnson NF (eds) (2011) Estudo dos insetos. use of stable isotope mixing models in food-web studies. Cengage Learning, Sa˜o Paulo Can J Zool 92:823–835 Vooren CM (1998) Aves marinhas e costeiras. In: Seeliger U, Pianka ER (1981) Competition and niche theory. In: May RM Odebrecht C, Castello JP (eds) Os ecossistemas costeiro e (ed) Theoretical ecology principles and applications. marinho do extremo sul do Brasil. Ecoscientia, Rio Grande, Blackwell, Hoboken, pp 167–196 pp 170–176 Piersma T, Wiersma P (1996) Family Charadriidae (plovers). In: Vooren CM, Chiaradia A (1990) Seasonal abundance and del Hoyo J, Elliot A, Sargatal J (eds) Handbook of the birds behavior of coastal birds on Cassino Beach, Brazil. Ornitol of the world (vol. 3): hoatzin to auks. Lynx Edicions, Neotrop 1:9–24 Barcelona, pp 384–442 Zhang J (2016) spaa: SPecies Association Analysis. R package Piersma T, Van-Gils J, Wiersma P (1996) Family Scolopacidae version 0.2.2. https://cran.r-project.org/web/packages/ (sandpipers, snipes and phalaropes). In: del Hoyo J, Elliot spaa/index.html. Accessed 02 Oct 2018 A, Sargatal J (eds) Handbook of the birds of the world (vol. 3): hoatzin to auks. Lynx Edicions, Barcelona, pp 444–526

123