NORTH-WESTERN JOURNAL OF ZOOLOGY 11 (2): 372-374 ©NwjZ, Oradea, Romania, 2015 Article No.: 147601 http://biozoojournals.ro/nwjz/index.html

Handling and intake of plastic debris by Wood at an urban site in South-eastern : possible causes and consequences

Ivan SAZIMA1,* and Giulia B. D’ANGELO2

1. Museu de Zoologia, Universidade Estadual de Campinas, 13083-970 Campinas, São Paulo, Brazil. 2. Instituto de Biologia, Universidade Estadual de Campinas, 13083-970 Campinas, São Paulo, Brazil. *Corresponding author, I. Sazima, E-mail: [email protected]

Received: 20. September 2014 / Accepted: 12. December 2014 / Available online: 01. November 2015 / Printed: December 2015

Anthropogenic inedible debris increases in the picked pieces of plastic cable were individually identified food chain of seabirds, marine turtles, and by differences on neck feathering and bill colour. cetaceans and becomes a worldwide problem (e.g. Sequenced photographs allowed the timing of the behavioural events for two of these individuals. Denuncio et al. 2011, Avery-Gomm et al. 2013, Throughout the observations, we used the “ad libitum” Schluyter et al. 2013, Donnelly-Greenan et al. 2014, sampling (Altmann 1974), which is adequate to record Provencher et al. 2015), but this material is rarely rare events. reported entering the food chain of inland wildlife (Peris 2003, Booth 2011, Henry et al. 2011). Storks Among small groups of Wood Storks that varied of the genus are opportunistic visual from 2 to 8 migrant individuals comprised of up to hunters that prey mostly on fish, frogs, snakes, 2 adults and 6 juveniles, we recorded the small mammals, and a variety of insects (Elliott behaviour of 4 juveniles (subadults sensu Coulton 1992). However, this opportunism may be et al. 1999) handling, attempting to swallow or deleterious, since the White (C. ciconia) that swallowing, and regurgitating pieces of pliable forage around rubbish dumps in Europe plastic cable of 60-70 cm long (Fig. 1). 1 reportedly ingests rubber bands and plastic debris picked up, attempted to swallow and regurgitate, (Peris 2003, Ciach & Kruszyk 2010, Henry et al. and finally swallowed a piece of cable about 60 cm 2011). On the other hand, storks of the genus long in the morning of 05 April 2014. 2 and 3 are tactile hunters that catch fishes displayed the same behaviour toward a cable of (including eels), frogs, snakes, insects and about 70 cm long (on one occasion these two birds crustaceans (González 1997, Coulter et al. 1999). disputed the same piece), in the morning of 18 Wood storks (M. americana) are not known to eat April 2014. On 11 May 2014, at noon, bird 4 took at dumps, possibly because of their foraging style, and tried to swallow a piece of cable of about 60 but their foraging habitat is not free from cm long. As usual, the birds waded through the anthropogenic debris (Corbo et al. 2013). Here we muddy water with the bill partially submersed describe and discuss how Wood Storks handle, try and picked a cable piece partly covered with a to swallow or swallow, and regurgitate pieces of film of aquatic microorganisms (Fig. 1a). They pliable plastic cable at an urban site in South- then grabbed the cable and tried to ingest it with eastern Brazil. upward movement of the head (Fig. 1b). However, most pieces were too long to be accommodated in Our observations were done during natural history the crop and hanged loose; the birds were unable studies of waterbirds at the urban park “Parque Ecológico to swallow it entirely (Fig. 1c). They tried to Prof. Hermógenes de Freitas Leitão Filho”, Campinas, São regurgitate the cable with vigorous lateral shaking Paulo, South-eastern Brazil. This recreational park is composed of a large pond (about 0.1 km2) surrounded by of the head accompanied by widely opening the trees and shrubs. The Wood Storks foraged near the left bill (Fig. 1d). These handling, swallowing, and bank of the pond (22° 48’ 44” S, 47° 04’ 14”W, 587 m.a.s.l.), regurgitating behaviours were performed up to mostly in muddy waters. In April and May 2014, during about 30 times in sequence. For bird 1, the cable the austral autumn, we recorded four stork individuals was probably stuck in its crop, but finally and the ways they handle plastic pieces. These birds were managed to swallow it entirely after about 20 min. observed for a total of 5 h 5 min, with bare eye and Bird 2 struggled for 11 min before releasing the through a 70-300 telephoto lens mounted on a camera from a distance of 3-12 m. The bank vegetation minimised piece. On the same day (11 May), bird 3 tried to the observer’s possible disturbance to the birds. Birds that steal the piece from bird 2 (Fig. 1e) but gave up Wood Storks and plastic debris 373

Figure 1. Foraging behavior of juvenile Wood Storks (M. americana) toward plastic debris. Bird 2 mandibulates and tries to swallow a large piece of plastic cable 70 cm long (a, b). Bird 1 tries to swallow and regurgitate a different piece of plastic cable 60 cm long for about 20 min, before swallowing it entirely (d). Bird 3 strives to steal a 70 cm plastic cable from bird 2 (e, f).

after 2 min. The two birds alternately pulled the cable in a dispute that included wing beating (Fig. 1f). Bird 2 managed to retain the cable and walked away, the other bird followed it until the first bird dropped the piece in the water. Afterwards, bird 3 searched for the cable and repeated the sequence of mandibulating, ingesting and regurgitating, until it dropped the object after 27 min. Birds 2, 3, and 4 resumed foraging after dropping the cable, and successfully caught small fish up to 10 cm or other unidentified prey. Bird 3 found the piece of cable again in the same morning, but dropped it after about 30 sec of handling. Bird 1, which swallowed the piece, did not forage afterwards. Wood Storks are tactile foragers and their diet includes eels and aquatic snakes (González 1997, Coulter et al. 1999, Corbo et al. 2013), therefore it seems plausible that the observed juveniles mistook the pieces of plastic cables for elongated prey. Juveniles of the visually foraging (C. ciconia) had a higher proportion of plastic debris than adults in their gizzard (Peris 2003), which indicates that young storks have lesser ability than adults to discriminate natural food from indigestible objects. In the case of the Wood Storks, besides the shape and/or mechanical similarity to an eel or a snake, we suggest that

these attempts may be partly due to the film of aquatic microorganisms on the object, which may increase the sensation of palatability to the birds (Mason & Clark 2000, Birkhead 2012). The handling of pieces of plastic cables and the attempts to swallow and regurgitate them may be regarded as a waste of time and energy for the Wood Storks. The possibility that this was a type of object play behaviour is unlikely, since these

birds generally play with smaller objects such as sticks and dry carcasses, without swallowing them (IS pers. obs.). Moreover, cable handling, swallowing and regurgitating do not match several criteria that characterise a play behaviour: being exaggerated or awkward; sequentially variable; mixing behavior patterns from several contexts, lacking the final consummatory act; and having no obvious immediate function (Burghardt

374 I. Sazima & G.B. D’Angelo

1998, Sazima 2008). The fact that one of the storks Avery-Gomm, S., Provencher, J.F., Morgan, K.H., Bertram, D.F. (2013): Plastic ingestion in marine-associated bird species from found the cable again during its foraging, and the eastern North Pacific. Marine Pollution Bulletin 72: 257-259. dropped it shortly after handling, may indicate Birkhead, T. (2012): Bird sense. Bloomsbury, New York. that it learned that this was an inedible object. The Booth, G.C. (2011): Trashing wildlife. Virginia Wildlife 72: 23-26. Burghardt, G. (1998): The evolutionary origins of play revisited: ingestion of inedible objects may lead to asphyxia lessons from turtles. pp. 1-26. In: Bekoff, M., Byers, J.A. (eds.): or crop or gizzard occlusion, as recorded for White play: evolutionary, comparative, and ecological Storks that feed on rubber bands (Henry et al. perspectives. Cambridge University Press, Cambridge. Ciach, M., Kruszyk, R. (2010): Foraging of White Storks Ciconia 2011). ciconia on rubbish dumps on non-breeding brounds. Waterbirds White Storks occur at rubbish dumps, but this 33: 101-104. behaviour was unrecorded on Wood Storks, Corbo, M., Macarrão, A., D’Angelo, G.B., Almeida, C.H., Silva, W.R., Sazima, I. (2013): Aves do campus da Unicamp e therefore the possibility of the latter to handle arredores. Avis Brasilis, Vinhedo. inedible anthropogenic objects as prey may be less Coulter, M.C., Rodgers, J.A., Ogden, J.C., Depkin, F.C. (1999): frequent than the previous species. Additionally, Wood Stork (Mycteria americana). In: Poole, A. (ed.): The Birds of Online. Cornell Laboratory of Ornithology, the differences in foraging behaviour between the Ithaca , two species, i.e. visual vs. tactile (Elliott 1992, accessed at 2014.08. 28. Coulter et al. 1999), may minimise the intake of Denuncio, P., Bastida, R., Dassis, M., Giardino, G., Gerpe, M., Rodríguez, D. (2011): Plastic ingestion in Franciscana dolphins, inedible objects by Wood Storks. Although our Pontoporia blainvillei (Gervais and d’Orbigny, 1844), from observation was restricted to one site, there is a Argentina. Marine Pollution Bulletin 62: 1836-1841. possibility that the same condition occur in other Donnelly-Greenan, E.L., Harvey, J.T., Nevins, H.M., Hester, M.M., Walker, W.A. (2014): Prey and plastic ingestion of Pacific areas. Field observations on this topic would Northern Fulmars (Fulmarus glacialis rogersii) from Monterey clarify our suggestions. Bay, California. Marine Pollution Bulletin 85: 214-224. Our report on the handling and intake of Elliot, A. (1992): Family Ciconiidae (Storks). pp. 436-465. In: Hoyo, J., Elliot, A., Sargatal, J. (eds.), Handbook of the birds of the plastic cables by Wood Storks is the first record on world. Volume 1. Ostrich to ducks. Lynx Edicions, Barcelona. the impact of such an inedible anthropogenic Gonzáles, J.A. (1997): Seasonal variation in the foraging ecology of object on birds in Brazil. It further illustrates the the Wood Stork in the southern llanos of Venezuela. The Condor 99: 671-680. detrimental effect that rubbish may have on the Henry, P-Y., Wey, G., Balança, G. (2011): Rubber-band ingestion by lives of aquatic inland birds, such as entanglement a rubbish dump dweller, the White Stork (Ciconia ciconia). of wings or bill, and ingestion of inedible objects Waterbirds 34: 504-508. Mason, J.R., Clark, L. (2000): The chemical senses in birds. pp. 39- (Peris 2003, Henry et al. 2011, Ryan 2013, Corbo et 56. In: Whittow, G.C. (ed.), Sturkie's avian physiology. al. 2013). Rubbish dumps and anthropogenic Academic Press, New York. materials (edible or not) in urbanised or natural Milchev, B., Georgiev, V. (2014): Extinction of the globally endangered Egyptian Neophron percnopterus breeding in habitats are a worldwide problem that affect the SE Bulgaria. North-western Journal of Zoology 10: 266-272. food chain and other aspects of the lives of inland Novaes, W.G., Cintra, R. (2013): Factors influencing the selection of wildlife (e.g. Prakash et al. 2003, Peirce & Van communal roost sites by the Coragyps atratus (Aves: Cathartidae) in an urban area in Central Amazon. Daele 2006, Ciach & Kruszyk 2010, Booth 2011, Zoologia 30: 607-614. Novaes & Cintra 2013, Milchev & Georgiev 2014). Peirce, K.N., Van Daele, J. (2006): Use of a garbage dump by brown bears in Dillingham, Alaska. Ursus 17: 165-177. Peris, J. (2003): Feeding in urban refuse dumps: ingestion of plastic objects by the White Stork (Ciconia ciconia). Ardeola 50: 81-84. Prakash, V., Pain, D.J., Cunningham, A.A., Donald, P.F., Prakash, Acknowledgements. We thank Marlies Sazima and N., Verma, A., Gargi, R., Sivakumar, S., Rahmani, A.R. (2003): Micael E. Nagai for their constant support; César Cestari Catastrophic collapse of Indian White-backed Gyps bengalensis and Micael E. Nagai for reading the first draft; two and Long-billed Gyps indicus vulture populations. Biological anonymous reviewers and the Subject Editor (Attila D. Conservation 109: 381-390. Sándor) for critical comments and valuable suggestions Provencher, J.F., Bond, A.L., Mallory, M.L. (2015): Marine birds and that greatly improved the manuscript; Martin Pareja for plastic debris in Canada: a national synthesis and a way forward. Environmental Reviews 23: 1-13. improving our English; the CNPq for earlier financial Ryan, P. (2013): Toxic waste: oceans of plastic threaten seabirds. support to IS, and the CAPES for earlier postgraduate African Birdlife: 52-56. grant to GBD. Sazima, I. (2008): Playful birds: cormorants and herons play with objects and practice their skills. Biota Neotropica 8: 259-264. Schuyler, Q., Hardesty, B.D., Wilcox, C., Townsend, K. (2013): Global analysis of anthropogenic debris ingestion by sea turtles. Conservation Biology 28:129-139. References

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