Trace elements concentrations in Buff-breasted Sandpiper sampled in Lagoa do Peixe National Park, Southern Brazil

Concentração de elementos-traço em maçarico-acanelado amostrados no Parque Nacional da Lagoa do Peixe, Sul do Brasil

J. F. M. Scherer A. L. Scherer E. Barbieri M. V. Petry V. H. Valiati About the authors

Abstract

Cadmium, cobalt, chromium, copper, manganese, nickel, zinc and lead concentrations were detected in feathers of Buff-breasted Sandpipers (Calidris subruficollis) captured during the non-breeding season and analyzed with relationship to body mass. Of these metals tested for, only copper levels (2.28 µg/g) were positively correlated with bird body mass. Zinc levels showed higher concentration (67.97 µg/g) than the other metals, and cadmium levels showed the lowest concentration (0.14 µg/g). Trace element concentrations were below toxicity levels for all tested chemicals and we suggest that this probably reflects that essential elements are maintained there by normal homeostatic mechanism and that no excessive environmental exposure to these elements during migration or on the wintering area is suggested by these results.

Keywords:
Charadriiformes; contaminants; body mass; wintering area; shorebirds

Resumo

As concentrações de cádmio, cobalto, cromo, cobre, manganês, níquel, zinco e chumbo foram detectadas em penas de Maçarico-acanelado (Calidris subruficollis) capturados durante o período de invernada e analisados em relação a massa corporal. Destes metais analisados, somente os níveis de cobre (2,28 µg/g) foram correlacionados positivamente com a massa corporal dos indivíduos. Níveis de zinco apresentaram-se mais altos (67,97 µg/g) que outros metais e os níveis de cádmio apresentaram as menores concentrações (0,14 µg/g). As concentrações dos elementos-traços estão abaixo dos níveis de toxicidade em todos os testes químicos e sugerimos que isto provavelmente ocorre pela manutenção dos elementos essenciais através do mecanismo normal de homeostase e não reflete a exposição destes elementos durante a migração ou nas áreas de invernada.

Palavras-chave:
Charadriiformes; contaminação; massa corporal; área de invernada; aves costeiras

1 Introduction

Habitats selected by shorebirds along their migration routes are diverse and vary in quality with relation to species eating requirements, availability and productivity of food resources, and foraging tactics), as well as risk of predation while on the site (Lunardi et al., 2012Lunardi, V.O., Macedo, R.H., Granadeiro, J.P. and PalmeIrim, J.M., 2012. Migratory flows and foraging habitat selection by shorebirds along the northeastern coast of Brazil: the case of Baía de Todos os Santos. Estuarine, Coastal and Shelf Science, vol. 96, pp. 179-187. http://dx.doi.org/10.1016/j.ecss.2011.11.001.
http://dx.doi.org/10.1016/j.ecss.2011.11...
). During the migration, birds are more susceptible to contamination, given that they are exposed to different environments along the flyway (Hargreaves et al., 2010Hargreaves, A.L., Whiteside, D.P. and Gilchrist, G., 2010. Concentrations of 17 elements, including mercury, and their relationship to fitness measures in arctic shorebirds and their eggs. The Science of the Total Environment, vol. 408, no. 16, pp. 3153-3161. http://dx.doi.org/10.1016/j.scitotenv.2010.03.027. PMid:20434755.
http://dx.doi.org/10.1016/j.scitotenv.20...
; Torres-Dowdall et al., 2010Torres-Dowdall, J., Farmer, A.H., Abril, M., Bucher, E.H. and Ridley, I., 2010. Trace elements have limited utility for studying migratory connectivity in shorebirds that winter in Argentina. The Condor, vol. 112, no. 3, pp. 490-498. http://dx.doi.org/10.1525/cond.2010.090166.
http://dx.doi.org/10.1525/cond.2010.0901...
). They can be contaminated through direct contact with heavy metals (Warnock and Takekawa, 1996Warnock, S.E.G. and Takekawa, J.Y., 1996. Wintering site fidelity and movement patterns of western sandpipers . (Calidris mauri) in the San Francisco Bay estuaryThe Ibis, vol. 138, no. 2, pp. 160-167. http://dx.doi.org/10.1111/j.1474-919X.1996.tb04323.x.
http://dx.doi.org/10.1111/j.1474-919X.19...
; Lanctot et al., 2002Lanctot, R.B., Blanco, D.E., Dias, R.A., Isacch, J.P., Gill, V.A., Almeida, J.B., Delhey, K., Petracci, P.F., Bencke, G.A. and Balbueno, R.A., 2002. Conservation status of the Buff-Breasted Sandpiper: historic and contemporary distribution and abundance in South America. The Wilson Bulletin, vol. 114, no. 1, pp. 44-72. http://dx.doi.org/10.1676/0043-5643(2002)114[0044:CSOTBB]2.0.CO;2.
http://dx.doi.org/10.1676/0043-5643(2002...
), or by the consumption of contaminated prey (Burger et al., 2001Burger, J., Shukla, T., Dixon, C., Shukla, S., McMahon, M.J., Ramos, R. and Gochfeld, M., 2001. Metals in feathers of sooty tern, white tern, gray-backed tern, and brown noddy from islands in the North Pacific. Environmental Monitoring and Assessment, vol. 71, no. 1, pp. 71-89. http://dx.doi.org/10.1023/A:1011695829296. PMid:11589497.
http://dx.doi.org/10.1023/A:101169582929...
; Kim and Koo, 2008Kim, J. and Koo, T.H., 2008. Heavy metal concentrations in feathers of Korean shorebirds. Archives of Environmental Contamination and Toxicology, vol. 55, no. 1, pp. 122-128. http://dx.doi.org/10.1007/s00244-007-9089-y. PMid:18080082.
http://dx.doi.org/10.1007/s00244-007-908...
). High level contamination by trace metal elements may negatively affect the reproduction and the general health of some birds (Dauwe et al., 2004Dauwe, T., Janssens, E., Kempenaers, B. and Eens, M., 2004. The effect of heavy metal exposure on egg size, eggshell thickness and the number of spermatozoa in blue tit Parus caeruleus eggs. Environmental Pollution, vol. 129, no. 1, pp. 125-129. http://dx.doi.org/10.1016/j.envpol.2003.09.028. PMid:14749076.
http://dx.doi.org/10.1016/j.envpol.2003....
), as well as may cause death of individuals (Bull et al., 1983Bull, K.R., Every, W.J., Freestone, P., Hall, J.R., Osborn, D., Cooke, A.S. and Stowe, T., 1983. Alkyl lead pollution and bird mortalities on the Mersey Estuari, UK, 1979-1981. Environmental Pollution, vol. 31, no. 4, pp. 239-259. http://dx.doi.org/10.1016/0143-1471(83)90062-4.
http://dx.doi.org/10.1016/0143-1471(83)9...
). In this way, anthropogenic factors, such as chemicals and pollutants, can contribute to causing continental level declines of migrant shorebird populations (Zöckler et al., 2003Zöckler, C., Delany, S. and Hagemeijer, W., 2003. Wader populations are declining – how will we elucidate the reasons? Wader Study Group Bulletin, vol. 100, pp. 202-211.).

Buff-breasted Sandpiper (Calidris subruficollis), (Vieillot, 1819) has continued a population decline which began with commercial hunting in the last century, and has continued that decline in the present century due to habitat loss and to contamination from spilled oil, gas and other toxic agents (Lanctot et al., 2010Lanctot, R.B., Aldabe, J., Almeida, J.B., Blanco, D., Isacch, J.P., Jorgensen, J., Norland, S., Rocca, P. and Strum, K.M., 2010. Conservation plan for the buff-breasted sandpiper (Tryngites subruficollis). Anchorage, Alaska: Fish and Wildlife Service; Manomet, Massachusetts: Manomet Center for Conservation Sciences. 114 p. Version 1.1. U. S ; Andres et al., 2012Andres, B.A., Smith, P.A., Morrison, R.I.G., Gratto-Trevor, C.L., Brown, S.C. and Friis, C.A., 2012. Population estimates of North American Shorebirds, 2012. Wader Study Group Bulletin, vol. 119, no. 3, pp. 178-194.; Cosewic, 2012COMMITTEE ON THE STATUS OF ENDANGERED WILDLIFE IN CANADA – COSEWIC, 2012. COSEWIC assessment and status report on the Buff-breasted sandpiper Tryngites subruficollis in Canada. Ottawa: COSEWIC. 44 p.; Lounsberry et al., 2013Lounsberry, Z.T., Almeida, J.B., Grace, T., Lanctot, R.B., Liebezeit, J., Sandercock, B.K., Strum, K.M., Zack, S. and Wisely, S.M., 2013. Range-wide conservation genetics of Burr-breasted Sandpipers (Tryngites subruficollis). The Auk, vol. 130, no. 3, pp. 429-439. http://dx.doi.org/10.1525/auk.2013.12206.
http://dx.doi.org/10.1525/auk.2013.12206...
) leading to the species being currently classified as "Near Threatened Status" (Birdlife International, 2014BIRDLIFE INTERNATIONAL, 2014 [viewed 01 January 2014] Species factsheet: Tryngites subruficollis. BirdLife International [online]. Available from: http://www.birdlife.org/datazone/species/factsheet/22693447.
http://www.birdlife.org/datazone/species...
). The species migrate from their breeding grounds in Alaska and Canada to winter in the pampas of South America (Lanctot et al., 2002Lanctot, R.B., Blanco, D.E., Dias, R.A., Isacch, J.P., Gill, V.A., Almeida, J.B., Delhey, K., Petracci, P.F., Bencke, G.A. and Balbueno, R.A., 2002. Conservation status of the Buff-Breasted Sandpiper: historic and contemporary distribution and abundance in South America. The Wilson Bulletin, vol. 114, no. 1, pp. 44-72. http://dx.doi.org/10.1676/0043-5643(2002)114[0044:CSOTBB]2.0.CO;2.
http://dx.doi.org/10.1676/0043-5643(2002...
; Norling et al., 2012Norling, W., Jeske, C.W., THIGPEN, T.F. and CHADWICK, P.C., 2012. Estimating shorebird population during spring stopover in rice fields of the Louisiana and Texas Gulf Coastal Plain. Waterbirds, vol. 35, no. 3, pp. 361-370. http://dx.doi.org/10.1675/063.035.0301.
http://dx.doi.org/10.1675/063.035.0301...
), at places such as Lagoa do Peixe National Park (LPNP) and surrounding sites (Resende and Leeuwenberg, 1987Resende, S.L. and Leeuwenberg, F., 1987. Ecological studies of Lagoa do Peixe. Washington: World Wildlife Foundation–WWF. 52 p. Unpublished Report 4.; Scherer and Petry, 2012Scherer, AL. and Petry, MV., 2012. Seasonal variation in shorebird abundance in the State of Rio Grande do Sul, Southern Brazil. The Wilson Journal of Ornithology, vol. 124, no. 1, pp. 40-50. http://dx.doi.org/10.1676/11-034.1.
http://dx.doi.org/10.1676/11-034.1...
; Harrison et al., 2013Harrison, N.M., Whitehouse, M.J. and Madureira, A.S.P., 2013. Observations of the under-described avifauna of the Mostardas Peninsula, Rio Grande do Sul, Brazil. Check list, vol. 9, no. 2, pp. 391-399. http://dx.doi.org/10.15560/9.2.391.
http://dx.doi.org/10.15560/9.2.391...
). The LPNP is an important reserve because protects one of South America’s most outstanding refuges for long-distance migrants (WHSRN, 2014WESTERN HEMISPHERE SHOREBIRD RESERVE NETWORK – WHSRN, 2014 [viewed 06 July 2014]. Lagoa do Peixe - about us. WHSRN [online]. Available from: http://www.whsrn.org/site-profile/lagoa-do-peixe.
http://www.whsrn.org/site-profile/lagoa-...
). One of the main reasons that high concentrations of shorebirds use the lagoon is presumably the availability of food resources and sites for replacement, where individuals can gain weight to complete the migration process between hemispheres.

Feathers are useful for measuring levels of trace elements in birds without causing harm to the individual (Furness and Greenwood, 1993Furness, R.W. and Greenwood, J.J.D., 1993. Birds as monitors of environmental change. London: Chapman and Hall. 356 p.). This makes it possible to use them for studies correlating trace elements with individual body mass (Burger et al., 1993Burger, J., Seyboldt, S., Morganstein, N. and Clark, K., 1993. Heavy metals and selenium in feathers of three shorebird species from Delaware bay. Environmental Monitoring and Assessment, vol. 28, no. 2, pp. 189-198. http://dx.doi.org/10.1007/BF00547037. PMid:24221132.
http://dx.doi.org/10.1007/BF00547037...
; Lucia et al., 2012Lucia, M., Bocher, P., Cosson, R.P., Churlaud, C. and Bustamante, P., 2012. Evidence of species-specific detoxification processes for trace elements in shorebirds. Ecotoxicology, vol. 21, no. 8, pp. 2349-2362. http://dx.doi.org/10.1007/s10646-012-0991-3. PMid:23001427.
http://dx.doi.org/10.1007/s10646-012-099...
). The goal of this study was to determine trace element levels of six metals in Buff-breasted Sandpiper and attempt to correlate them with birds body mass.

2 Material and Methods

Shorebird catches were conducted in pasturelands in the Lagoa do Peixe National Park (LPNP) (31° 15’ 19" S, 050° 58’ 19" W) in spring 2011. In the field, Buff-breasted Sandpipers were weighed; a blood sample collected, and one primary and a few breast feathers were collected from each bird and stored in sealed plastic bags. We analyzed cadmium, cobalt, chromium, copper, manganese, nickel, zinc, and lead according methods used by Barbieri et al. (2010)Barbieri, E., Passos, E.A., Filippini, A., Santos, I.S. and Garcia, C.A.B., 2010. Assessment of trace metal concentration in feathers of seabird (Larus dominicanus) sampled in the Florianópolis, SC, Brazilian coast. Environmental Monitoring and Assessment, vol. 169, no. 1-4, pp. 631-638. http://dx.doi.org/10.1007/s10661-009-1202-4. PMid:19856122.
http://dx.doi.org/10.1007/s10661-009-120...
. All element concentrations (µg/g) in feathers were expressed as dry weight basis. Genomic DNA was extracted from red blood cells using the standard phenol/chloroform and proteinase K extraction followed by ethanol precipitation (Sambrook et al., 2001Sambrook, K.J., Russel, D.W. and Sambrook, J., 2001. Molecular cloning: a laboratory manual. New York: CSHL. 2100 p.). Thereafter, the gene CHD1 (chromo-helicase-DNA-binding 1) was amplified by polymerase chain reaction (PCR), using primers P2 and P8 (Griffiths et al., 1998Griffiths, R., Double, M.C., Orr, K. and Dawson, R.J.G., 1998. A DNA test to sex most birds. Molecular Ecology, vol. 7, no. 8, pp. 1071-1075. http://dx.doi.org/10.1046/j.1365-294x.1998.00389.x. PMid:9711866.
http://dx.doi.org/10.1046/j.1365-294x.19...
) to identify sex of each bird. A Pearson correlation test was performed to analyse element correlations with weight. The significance level was set at p < 0.05 for analyse.

3 Results

We analyzed feathers of 29 Buff-breasted Sandpiper, being 7 males, 17 females and, 5 undetermined. Concentration levels of trace elements tested for in feathers were below toxicity levels for all individuals and average values are presented in Table 1. Nickel and chromium concentrations were below the detection level for all samples. Pearson correlation tests showed that copper was positively correlated with Buff-breasted Sandpiper body mass (r = 0.375, p = 0.045).

Table 1
Values of trace elements concentrations (mean ± SD, µg/g) in feathers of Buff-breasted Sandpiper (n = 29) and other bird species.

4 Discussion

All trace element levels found in this study were below the toxic range reported in the literature (Vermeer and Castilla, 1991Vermeer, K. and Castilla, J.C., 1991. High cadmium residues observed during a pilot study in shorebirds and their prey downstream from the El Salvador Copper Mine, Chile. Bulletin of Environmental Contamination and Toxicology, vol. 46, no. 2, pp. 242-248. http://dx.doi.org/10.1007/BF01691944. PMid:2018870.
http://dx.doi.org/10.1007/BF01691944...
; Puls, 1994Puls, R., 1994. Mineral levels in animal health: diagnostic data. British Columbia: Sherpa International. 356 p.; Burger et al., 2001Burger, J., Shukla, T., Dixon, C., Shukla, S., McMahon, M.J., Ramos, R. and Gochfeld, M., 2001. Metals in feathers of sooty tern, white tern, gray-backed tern, and brown noddy from islands in the North Pacific. Environmental Monitoring and Assessment, vol. 71, no. 1, pp. 71-89. http://dx.doi.org/10.1023/A:1011695829296. PMid:11589497.
http://dx.doi.org/10.1023/A:101169582929...
; Barbieri et al., 2007Barbieri, E., Garcia, C.A.B., Passos, E.A., Aragão, K.A.S. and Kennedy, A.S., 2007. Heavy metal concentration in tissues of Puffinus gravis sampled on the Brazilian coast. Revista Brasileira de Ornitologia, vol. 15, no. 28, pp. 69-72.; Kim and Oh, 2013Kim, J. and Oh, J.M., 2013. Assessment of trace metals in four bird species from Korea. Environmental Monitoring and Assessment, vol. 185, no. 8, pp. 6847-6854. http://dx.doi.org/10.1007/s10661-013-3069-7. PMid:23430066.
http://dx.doi.org/10.1007/s10661-013-306...
). Essential elements are present in all living organisms and necessary for regulation of body functions and are usually maintained by homeostasis mechanisms, which act in the removal of excess and maintenance of normal bodily concentrations (Kim and Oh, 2013Kim, J. and Oh, J.M., 2013. Assessment of trace metals in four bird species from Korea. Environmental Monitoring and Assessment, vol. 185, no. 8, pp. 6847-6854. http://dx.doi.org/10.1007/s10661-013-3069-7. PMid:23430066.
http://dx.doi.org/10.1007/s10661-013-306...
). Therefore, low levels of these components result from a good intrinsic regulatory system, and it is suggested that this process can regulate chromium, cobalt, copper, manganese, nickel, and zinc. Significant copper levels correlation with body mass may reflect that these shorebirds, when compared with other birds, may use more energy by keeping higher metabolic rates (Colwell, 2010ColwelL, M.A., 2010. Shorebird ecology, conservation and management. London: University of California Press. 328 p.) and ingest higher prey mass. Thus, copper level being correlated with body mass may have arisen from bioaccumulation via species-specific metabolism and it is thought to be unlikely reflect pollution or higher natural background level of copper in their habitats (Kim et al., 1996Kim, E.Y., Ichihashi, H., Saeki, K., Atrashkevich, G., Tanabe, S. and Tatsukawa, R., 1996. Metal accumulation in tissues of seabirds from Chaun, northeast Siberia, Russia. Environmental Pollution, vol. 92, no. 3, pp. 247-252. http://dx.doi.org/10.1016/0269-7491(96)00007-3. PMid:15091375.
http://dx.doi.org/10.1016/0269-7491(96)0...
).

Levels of non-essential elements such as cadmium and lead were found in individuals. According to Scherer et al. (unpublished data), cadmium levels found in sediment of LPNP were about 0.02 µg/g. Therefore we cannot say with certainty where this exposure occurred, but what we can say, is that in our study, the individuals all evidenced low cadmium concentrations and that their exposure does not reflect levels of bioaccumulation during wintering in the park, suggesting that the levels found in individuals are not sufficient to cause damage to them. According to Burger et al. (2001)Burger, J., Shukla, T., Dixon, C., Shukla, S., McMahon, M.J., Ramos, R. and Gochfeld, M., 2001. Metals in feathers of sooty tern, white tern, gray-backed tern, and brown noddy from islands in the North Pacific. Environmental Monitoring and Assessment, vol. 71, no. 1, pp. 71-89. http://dx.doi.org/10.1023/A:1011695829296. PMid:11589497.
http://dx.doi.org/10.1023/A:101169582929...
, for terns, the toxicity levels must be above 2 µg/g before sublethal effects are noted, and the individuals in our study showed concentrations far below this (0.15 µg/g). Another hand, according to Clark and Scheuhammer (2003)Clark, A.J. and Scheuhammer, A.M., 2003. Lead poisoning in upland-foraging birds of prey in Canada. Ecotoxicology, vol. 12, no. 1-4, pp. 23-30. http://dx.doi.org/10.1023/A:1022576510445. PMid:12739854.
http://dx.doi.org/10.1023/A:102257651044...
, lead concentrations between 2.0 and 10.0 µg/g are associated with exposure to lead pollution. Although low lead concentrations were found in our study (2.18 µg/g), this level is indicative of exposure of these individuals to this metal, but without toxicological risk, and thus it could be considered as the background level (Kim and Oh, 2013Kim, J. and Oh, J.M., 2013. Assessment of trace metals in four bird species from Korea. Environmental Monitoring and Assessment, vol. 185, no. 8, pp. 6847-6854. http://dx.doi.org/10.1007/s10661-013-3069-7. PMid:23430066.
http://dx.doi.org/10.1007/s10661-013-306...
). Our study is the first to evaluate trace elements in Buff-breasted Sandpiper in LPNP and contributes valuable information because we showed that metallic trace element levels found in the birds captured in park are below the range of considered toxic, and do not show excessive bioaccumulation, thus retaining normal traces element levels. Further studies in regularly used shorebird wintering areas will be important to determine the degree of heavy metal contamination on a timescale, as well as whether some of these sites might interfere in birds’ health and population stability. Performing studies like this can serve as an important tool for monitoring wintering areas, serving as a conservation tool for both habitats and for species that use them.

Acknowledgements

We thank CEMAVE staff and, ICMBio Lagoa do Peixe National Park staff for helping in the fieldwork. The research was supported by CNPq, CAPES, FAPERGS and, UNISINOS. We appreciate the improvements in English usage made by Phil Whitford through the Association of Field Ornithologists' program of editorial assistance. All individuals were banded with a steel ring under CEMAVE permission nº 3221/2010. Blood samples were taken under ICMBio permission nº 23159/2010.

References

  • Andres, B.A., Smith, P.A., Morrison, R.I.G., Gratto-Trevor, C.L., Brown, S.C. and Friis, C.A., 2012. Population estimates of North American Shorebirds, 2012. Wader Study Group Bulletin, vol. 119, no. 3, pp. 178-194.
  • Barbieri, E., Passos, E.A., Filippini, A., Santos, I.S. and Garcia, C.A.B., 2010. Assessment of trace metal concentration in feathers of seabird (Larus dominicanus) sampled in the Florianópolis, SC, Brazilian coast. Environmental Monitoring and Assessment, vol. 169, no. 1-4, pp. 631-638. http://dx.doi.org/10.1007/s10661-009-1202-4. PMid:19856122.
    » http://dx.doi.org/10.1007/s10661-009-1202-4
  • Barbieri, E., Garcia, C.A.B., Passos, E.A., Aragão, K.A.S. and Kennedy, A.S., 2007. Heavy metal concentration in tissues of Puffinus gravis sampled on the Brazilian coast. Revista Brasileira de Ornitologia, vol. 15, no. 28, pp. 69-72.
  • BIRDLIFE INTERNATIONAL, 2014 [viewed 01 January 2014] Species factsheet: Tryngites subruficollis. BirdLife International [online]. Available from: http://www.birdlife.org/datazone/species/factsheet/22693447.
    » http://www.birdlife.org/datazone/species/factsheet/22693447
  • Bull, K.R., Every, W.J., Freestone, P., Hall, J.R., Osborn, D., Cooke, A.S. and Stowe, T., 1983. Alkyl lead pollution and bird mortalities on the Mersey Estuari, UK, 1979-1981. Environmental Pollution, vol. 31, no. 4, pp. 239-259. http://dx.doi.org/10.1016/0143-1471(83)90062-4.
    » http://dx.doi.org/10.1016/0143-1471(83)90062-4
  • Burger, J., Gochfeld, M., Sullivan, K., Irons, D. and McKnight, A., 2008. Arsenic, cadmium, chromium, lead, manganese, mercury, and selenium in feathers of Black-legged Kittiwake (Rissa tridactyla) and Black Oystercatcher (Haematopus bachmani) from Prince William Sound, Alaska. The Science of the Total Environment, vol. 398, no. 1-3, pp. 20-25. http://dx.doi.org/10.1016/j.scitotenv.2008.02.051. PMid:18440597.
    » http://dx.doi.org/10.1016/j.scitotenv.2008.02.051
  • Burger, J., Shukla, T., Dixon, C., Shukla, S., McMahon, M.J., Ramos, R. and Gochfeld, M., 2001. Metals in feathers of sooty tern, white tern, gray-backed tern, and brown noddy from islands in the North Pacific. Environmental Monitoring and Assessment, vol. 71, no. 1, pp. 71-89. http://dx.doi.org/10.1023/A:1011695829296. PMid:11589497.
    » http://dx.doi.org/10.1023/A:1011695829296
  • Burger, J., Seyboldt, S., Morganstein, N. and Clark, K., 1993. Heavy metals and selenium in feathers of three shorebird species from Delaware bay. Environmental Monitoring and Assessment, vol. 28, no. 2, pp. 189-198. http://dx.doi.org/10.1007/BF00547037. PMid:24221132.
    » http://dx.doi.org/10.1007/BF00547037
  • Clark, A.J. and Scheuhammer, A.M., 2003. Lead poisoning in upland-foraging birds of prey in Canada. Ecotoxicology, vol. 12, no. 1-4, pp. 23-30. http://dx.doi.org/10.1023/A:1022576510445. PMid:12739854.
    » http://dx.doi.org/10.1023/A:1022576510445
  • ColwelL, M.A., 2010. Shorebird ecology, conservation and management. London: University of California Press. 328 p.
  • COMMITTEE ON THE STATUS OF ENDANGERED WILDLIFE IN CANADA – COSEWIC, 2012. COSEWIC assessment and status report on the Buff-breasted sandpiper Tryngites subruficollis in Canada. Ottawa: COSEWIC. 44 p.
  • Dauwe, T., Janssens, E., Kempenaers, B. and Eens, M., 2004. The effect of heavy metal exposure on egg size, eggshell thickness and the number of spermatozoa in blue tit Parus caeruleus eggs. Environmental Pollution, vol. 129, no. 1, pp. 125-129. http://dx.doi.org/10.1016/j.envpol.2003.09.028. PMid:14749076.
    » http://dx.doi.org/10.1016/j.envpol.2003.09.028
  • Furness, R.W. and Greenwood, J.J.D., 1993. Birds as monitors of environmental change. London: Chapman and Hall. 356 p.
  • Griffiths, R., Double, M.C., Orr, K. and Dawson, R.J.G., 1998. A DNA test to sex most birds. Molecular Ecology, vol. 7, no. 8, pp. 1071-1075. http://dx.doi.org/10.1046/j.1365-294x.1998.00389.x. PMid:9711866.
    » http://dx.doi.org/10.1046/j.1365-294x.1998.00389.x
  • Hargreaves, A.L., Whiteside, D.P. and Gilchrist, G., 2010. Concentrations of 17 elements, including mercury, and their relationship to fitness measures in arctic shorebirds and their eggs. The Science of the Total Environment, vol. 408, no. 16, pp. 3153-3161. http://dx.doi.org/10.1016/j.scitotenv.2010.03.027. PMid:20434755.
    » http://dx.doi.org/10.1016/j.scitotenv.2010.03.027
  • Harrison, N.M., Whitehouse, M.J. and Madureira, A.S.P., 2013. Observations of the under-described avifauna of the Mostardas Peninsula, Rio Grande do Sul, Brazil. Check list, vol. 9, no. 2, pp. 391-399. http://dx.doi.org/10.15560/9.2.391.
    » http://dx.doi.org/10.15560/9.2.391
  • Kim, J. and Oh, J.M., 2013. Assessment of trace metals in four bird species from Korea. Environmental Monitoring and Assessment, vol. 185, no. 8, pp. 6847-6854. http://dx.doi.org/10.1007/s10661-013-3069-7. PMid:23430066.
    » http://dx.doi.org/10.1007/s10661-013-3069-7
  • Kim, J. and Koo, T.H., 2008. Heavy metal concentrations in feathers of Korean shorebirds. Archives of Environmental Contamination and Toxicology, vol. 55, no. 1, pp. 122-128. http://dx.doi.org/10.1007/s00244-007-9089-y. PMid:18080082.
    » http://dx.doi.org/10.1007/s00244-007-9089-y
  • Kim, E.Y., Ichihashi, H., Saeki, K., Atrashkevich, G., Tanabe, S. and Tatsukawa, R., 1996. Metal accumulation in tissues of seabirds from Chaun, northeast Siberia, Russia. Environmental Pollution, vol. 92, no. 3, pp. 247-252. http://dx.doi.org/10.1016/0269-7491(96)00007-3. PMid:15091375.
    » http://dx.doi.org/10.1016/0269-7491(96)00007-3
  • Lanctot, R.B., Aldabe, J., Almeida, J.B., Blanco, D., Isacch, J.P., Jorgensen, J., Norland, S., Rocca, P. and Strum, K.M., 2010. Conservation plan for the buff-breasted sandpiper (Tryngites subruficollis). Anchorage, Alaska: Fish and Wildlife Service; Manomet, Massachusetts: Manomet Center for Conservation Sciences. 114 p. Version 1.1. U. S
  • Lanctot, R.B., Blanco, D.E., Dias, R.A., Isacch, J.P., Gill, V.A., Almeida, J.B., Delhey, K., Petracci, P.F., Bencke, G.A. and Balbueno, R.A., 2002. Conservation status of the Buff-Breasted Sandpiper: historic and contemporary distribution and abundance in South America. The Wilson Bulletin, vol. 114, no. 1, pp. 44-72. http://dx.doi.org/10.1676/0043-5643(2002)114[0044:CSOTBB]2.0.CO;2.
    » http://dx.doi.org/10.1676/0043-5643(2002)114[0044:CSOTBB]2.0.CO;2
  • Lounsberry, Z.T., Almeida, J.B., Grace, T., Lanctot, R.B., Liebezeit, J., Sandercock, B.K., Strum, K.M., Zack, S. and Wisely, S.M., 2013. Range-wide conservation genetics of Burr-breasted Sandpipers (Tryngites subruficollis). The Auk, vol. 130, no. 3, pp. 429-439. http://dx.doi.org/10.1525/auk.2013.12206.
    » http://dx.doi.org/10.1525/auk.2013.12206
  • Lucia, M., Bocher, P., Cosson, R.P., Churlaud, C. and Bustamante, P., 2012. Evidence of species-specific detoxification processes for trace elements in shorebirds. Ecotoxicology, vol. 21, no. 8, pp. 2349-2362. http://dx.doi.org/10.1007/s10646-012-0991-3. PMid:23001427.
    » http://dx.doi.org/10.1007/s10646-012-0991-3
  • Lunardi, V.O., Macedo, R.H., Granadeiro, J.P. and PalmeIrim, J.M., 2012. Migratory flows and foraging habitat selection by shorebirds along the northeastern coast of Brazil: the case of Baía de Todos os Santos. Estuarine, Coastal and Shelf Science, vol. 96, pp. 179-187. http://dx.doi.org/10.1016/j.ecss.2011.11.001.
    » http://dx.doi.org/10.1016/j.ecss.2011.11.001
  • Norling, W., Jeske, C.W., THIGPEN, T.F. and CHADWICK, P.C., 2012. Estimating shorebird population during spring stopover in rice fields of the Louisiana and Texas Gulf Coastal Plain. Waterbirds, vol. 35, no. 3, pp. 361-370. http://dx.doi.org/10.1675/063.035.0301.
    » http://dx.doi.org/10.1675/063.035.0301
  • Puls, R., 1994. Mineral levels in animal health: diagnostic data. British Columbia: Sherpa International. 356 p.
  • Resende, S.L. and Leeuwenberg, F., 1987. Ecological studies of Lagoa do Peixe. Washington: World Wildlife Foundation–WWF. 52 p. Unpublished Report 4.
  • Roodbergen, M., Klok, C. and van der Hout, A., 2008. Transfer of heavy metals in the food chain earthworm Black-tailed godwit (Limosa limosa): comparison of a polluted and a reference site in The Netherlands. The Science of the Total Environment, vol. 406, no. 3, pp. 407-412. http://dx.doi.org/10.1016/j.scitotenv.2008.06.051. PMid:18752837.
    » http://dx.doi.org/10.1016/j.scitotenv.2008.06.051
  • Sambrook, K.J., Russel, D.W. and Sambrook, J., 2001. Molecular cloning: a laboratory manual. New York: CSHL. 2100 p.
  • Scherer, AL. and Petry, MV., 2012. Seasonal variation in shorebird abundance in the State of Rio Grande do Sul, Southern Brazil. The Wilson Journal of Ornithology, vol. 124, no. 1, pp. 40-50. http://dx.doi.org/10.1676/11-034.1.
    » http://dx.doi.org/10.1676/11-034.1
  • Torres-Dowdall, J., Farmer, A.H., Abril, M., Bucher, E.H. and Ridley, I., 2010. Trace elements have limited utility for studying migratory connectivity in shorebirds that winter in Argentina. The Condor, vol. 112, no. 3, pp. 490-498. http://dx.doi.org/10.1525/cond.2010.090166.
    » http://dx.doi.org/10.1525/cond.2010.090166
  • Vermeer, K. and Castilla, J.C., 1991. High cadmium residues observed during a pilot study in shorebirds and their prey downstream from the El Salvador Copper Mine, Chile. Bulletin of Environmental Contamination and Toxicology, vol. 46, no. 2, pp. 242-248. http://dx.doi.org/10.1007/BF01691944. PMid:2018870.
    » http://dx.doi.org/10.1007/BF01691944
  • Warnock, S.E.G. and Takekawa, J.Y., 1996. Wintering site fidelity and movement patterns of western sandpipers . (Calidris mauri) in the San Francisco Bay estuaryThe Ibis, vol. 138, no. 2, pp. 160-167. http://dx.doi.org/10.1111/j.1474-919X.1996.tb04323.x.
    » http://dx.doi.org/10.1111/j.1474-919X.1996.tb04323.x
  • WESTERN HEMISPHERE SHOREBIRD RESERVE NETWORK – WHSRN, 2014 [viewed 06 July 2014]. Lagoa do Peixe - about us. WHSRN [online]. Available from: http://www.whsrn.org/site-profile/lagoa-do-peixe.
    » http://www.whsrn.org/site-profile/lagoa-do-peixe
  • Zöckler, C., Delany, S. and Hagemeijer, W., 2003. Wader populations are declining – how will we elucidate the reasons? Wader Study Group Bulletin, vol. 100, pp. 202-211.

Publication Dates

  • Publication in this collection
    10 Nov 2015
  • Date of issue
    Nov 2015

History

  • Received
    19 Feb 2014
  • Accepted
    02 Aug 2014
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br