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ORNITOLOGIA NEOTROPICAL 22: 453–457, 2011 © The Neotropical Ornithological Society

KLEPTOPARASITISM BY THE CHIMANGO (MILVAGO CHIMANGO) ON THE AMERICAN OYSTERCATCHER (HAEMATOPUS PALLIATUS) AT MAR CHIQUITA LAGOON, ARGENTINA

Germán O. García1,2 & Laura M. Biondi1,2

1Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Av. Rivadavia 1917, C1033AAJ Buenos Aires, Argentina. 2Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Funes 3250, B7602AYJ Mar del Plata, Argentina. E-mail: [email protected]

Cleptoparasitismo de Chimango (Milvago chimango) sobre el Ostrero Común (Haematopus palliatus) en la laguna de Mar Chiquita, Argentina.

Key words: Milvago chimango, Haematopus palliatus, Kleptoparasitism, foraging strategy, Mar Chiquita Lagoon, Argentina.

INTRODUCTION In Mar Chiquita Lagoon (Argentina), American Oystercatchers (Haematopus pallia- Kleptoparasitism is defined as the stealing by tus) forage on sand-lime beaches where they one of food that has been caught by feed mainly clams and crabs (Bachmann & another (Furness 1987). This behavior is an Martínez 1999). In this area, oystercatchers important strategy to obtain limited or are frequently kleptoparasitized by Brown- unavailable resources and it has been adopted hooded Gull Chroicocephalus maculipennis and by a variety of (Giraldeau & Caraco Grey-headed Gull Chroicocephalus cirrocephalus, 2000). In , the likelihood of developing among others (Khatchikian et al. 2002). The this behavior appears to be associated with Caracara Chimango, Milvago chimango, is a certain attributes of the taxa, such as the generalist and opportunistic raptor that inclusion of vertebrate prey in the diet, the feeds on a wide range of vertebrate and inver- use of open feeding habitats (Brockmann & tebrate prey, also showing scavenger habits Barnard 1979), and the possession of a rela- (Biondi et al. 2005). The Caracara Chimango tively large brain (i.e., high cognitive abilities, shares the foraging area with the American Morrand-Ferron et al. 2007). oystercatchers and is quite abundant in the

453 GARCÍA & BIONDI area; it can be frequently seen patrolling the (i.e., clams, total length TL) was estimated in shoreline searching for crabs, fishing discards, relation to the oystercatcher’s bill length as food scraps and garbage among other items “very small” (TL ≤ 15 mm), “small” (15 mm (Biondi et al. 2005). Here we report the < TL ≤ 30 mm), “medium” (30 mm < TL ≤ repeated observation of Caracara Chimangos 45 mm), “large” (45 mm ≤ TL ≤ 60 mm), and kleptoparasitizing American Oystercatchers, “very large” (60 mm < TL ≤ 75 mm). describing this association qualitatively and quantitatively. RESULTS

STUDY AREA AND METHODS A total of 29 kleptoparasitic attacks on oyster- catchers was observed. There was a difference Observations were made between March and in the frequency of the stealing-attempts September 2007 in Mar Chiquita Lagoon made on clams (N = 26) and those involving (Buenos Aires Province, Argentina, 37°46’S, crabs (N = 4). Sixty-five percent of the klep- 57°27’W). This lagoon consists of a body of toparasitic events were successful, all of them tidal brackish water of 46 km2, with mud flats performed on hosts feeding on clams (N = bordered by Spartina densiflora grassland and 17). The size of the clams attempted to steal inhabited by a large number of intertidal were “medium” (31.82%) and “large” crabs. Intertidal benthic communities at this (68.18%) sized. The size of stolen clams was lagoon and in other southwestern Atlantic larger than those registered during the failed estuaries have very low macroinfaunal diver- attempts (successful: “medium” = 3 events, sity, being the Stout Razor clams Tagelus ple- “large” = 16 events; failed: “medium” = 4 beius the dominant species (Gutiérrez et al. events, “large” = 2 events). 2000). Among the epibenthic organisms, the The most frequently observed kleptopara- dominant species are the Burrowing crab Neo- sites : host ratio was 1:1 (N = 20), although a helice granulata and the Mud crab Cyrtograpsus maximum of three Caracara Chimangos asso- angulatus (Spivak et al. 1994). ciated to a single host was observed in three Information on kleptoparasitism per- cases. In all observed attacks, kleptoparasitism formed by the Caracara Chimango on Ameri- was performed by only one raptor. The Cara- can Oystercatchers, was obtained during ad- cara Chimango stole food from oystercatch- libitum observations conducted throughout ers by using two kleptoparasitic tactics, daylight hours (09:00–18:00 h local time) over defined as running (from a nearby position) 17 days. Observations were made with the and flying. There was a difference in the use help of binoculars (8x) and telescope (12– of both stealing-tactics, being the flying one 60x). During samplings, both the occurrence the most frequently performed (95%). of kleptoparasitic interactions and its out- When the kleptoparasite attacked, hosts come were recorded. An attack was consid- left the prey with no apparent defense tactics ered successful when the kleptoparasite took displayed (31.03%, N = 9), or adopted two the prey from the host. For each attack we strategies to avoid the stealing of food: facing also recorded size and type of prey. To reduce the parasite with agonistic vocalizations and biases in the determination and characteriza- peckings (34.48%, N = 10), or running away tion of prey, the same observer made all with the prey in the bill (34.48%, N = 10). observations. Two prey were kleptoparasit- Under both defense tactic scenarios, Caracara ized: Tagelus plebeius and Cyrtograpsus angulatus. Chimangos succeed in stealing prey from oys- The size of the main prey kleptoparasitized tercatchers in 40% of the attacks.

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DISCUSSION the likelihood of engaging in kleptoparasitic behaviors using the aerial tactic. Several studies have shown that the American A significant number of precedents have Oystercatcher is kleptoparasitized by seabirds described and analyzed the hosts’ behavior and shorebirds (Martinez & Bachmann 1997, to avoid or reduce the theft of food by Tuckwell & Nol 1997, Khatchikian et al. 2002, kleptoparasitism. These types of behaviors Hand et al. 2010). However, this is the may include the flight with prey, aggression to first study that provides a quali-quantitative kleptoparasites (Amat & Aguilera 1989), and des-cription of the kleptoparasitic interaction even reduced handling time (Hockey & Steele bet-ween American Oystercatchers and a 1990, García et al. 2008). The two observed raptor. avoidance tactics (running away and agonistic Many bird species act as scavengers on behaviors) indicate that kleptoparasitism the scraps, feces or parasites of other animals affected the feeding behavior of oystercatch- (see Brockmann & Barnard 1979). Such ers and likely their foraging performance. behavior may occasionally result in birds actu- Previous studies have associated the body ally stealing from the host while handling size differences between host and kleptopara- prey (Cowan 1968). The Caracara Chimango site with the occurrence of kleptoparasitism has frequently been observed consuming the (see Brockmann & Barnard 1979). Larger flesh remains of the clams left by oystercatch- kleptoparasites might be at an advantage in ers, together with the aggressiveness and contexts where they can use threats or actual maneuverability skills characterizing a physical aggression on hosts, but not neces- medium-sized raptor are probably determi- sarily in cases where the kleptoparasite attack nant factors leading to the development of the host before it can detect or react to that kleptoparasitic interactions with American attack (Giraldeau & Caraco 2000). Other Oystercatchers. studies have found that the residual brain size During the field observations we found a of kleptoparasites is associated positively with higher occurrence of kleptoparasitism on the occurrence of kleptoparasitism in bird large clams, indicating a possible preference taxa (Morand-Ferron et al. 2007). Despite the of this prey size by kleptoparasites. Consider- fact that the Caracara Chimango (~ 300 g) is ing that kleptoparasites prefer to steal large or smaller than its host (~ 600 g), this size differ- conspicuous prey (García et al. 2010), it is very ence did not prevent the parasite from achiev- likely that both conspicuousness and ex- ing a high kleptoparasitic success (65%). This tended handling times of larger clams favored claim is consistent with data proceeding from the development of such behavior. recent studies which allow classifying the Car- The distribution of tactics used by klepto- acara Chimango as a species with a remark- parasites during the observations showed a able ecological plasticity and a relatively high greater use of the flying tactic compared to residual brain size (Biondi et al. 2005, 2008). the running one. The predominance of the The social learning ability of the Caracara Chi- aerial tactic could be the result of prevailing mango, which has recently been demonstrated wind conditions during the observations, experimentally (Biondi et al. 2010), might facilitating movement and increasing maneu- speed the transmission of a feeding strategy verability to kleptoparasites. In addition, the (i.e., kleptoparasitism) throughout the Cara- fact that the Caracara Chimango usually cara Chimango individuals, increasing its patrols the area through low flights, looking effects on the local populations of oyster- for any feeding opportunity, might increase catchers.

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ACKNOWLEDGMENTS on the grapsid crab Cyrtograpsus angulatus: advantages and disadvantages of an unusual We would like to thank María Pía Gómez food resource. Ibis 150: 110–114. Laich for the language editing. Thanks to García, G. O., M. Favero, & A. Vassallo. 2010. Fac- Marco Favero and Richard Johnston for pro- tors affecting kleptoparasitism by gulls in a multi-species seabird colony. Condor 112: 521– vide helpful comments of this manuscript. 529. This research was supported by a grant from Giraldeau, L. A., & T. Caraco. 2000. Social foraging Universidad Nacional de Mar del Plata (Grant theory. Princeton Univ. Press, Princeton, New 15/E238, UNMdP, Argentina) and a doctoral Jersey, USA. scholarship from Consejo Nacional de Inves- Gutiérrez, J., G. Palomo, & O. Iribarne. 2000. Pat- tigaciones Científicas y Técnicas (CONICET, terns of abundance and seasonality of poly- Argentina). chaetes in a SW Atlantic estuarine epibenthic shell assemblage. Bull. Mar. Sci. 67: 165–174. REFERENCES Hand, C. E., P. G. R. Jodice, & F. J. Sanders. 2010. Foraging proficiency during the nonbreeding Amat, J. A., & E. Aguilera. 1989. Some behavioural season in a specialized forager: Are juvenile responses of Little Egret and Black-tailed God- American Oystercatchers (Haematopus palliatus) wit to reduce prey loses from kleptoparasites. ‘bumble-beaks’ compared to adults? Condor Ornis Scand. 20: 234–236. 112: 670–675. Bachmann, S., & M. M. Martinez. 1999. Feeding Hockey, P. A. R., & W. K. Steele. 1990. Intraspe- tactics of the American Oystercatcher (Hae- cific kleptoparasitism and foraging efficiency as matopus palliatus) on Mar Chiquita costal lagoon, constraints on food selection by Kelp Gulls Argentina. Ornitol. Neotrop. 10: 81–84. Larus dominicanus. Pp. 679–706 in Hughes, R. N. Biondi, L. M., M. S. Bó, & M. Favero. 2005. Dieta (ed.). Behavioural mechanisms of food del Chimango (Milvago chimango) durante el peri- selection. Springer-Verlag London, London, odo reproductivo en el sudeste de la provincia UK. de Buenos Aires, Argentina. Ornitol. Neotrop. Khatchikian, C. E. 2000. Cleptoparasitismo de 16: 31–42. Gaviotas (Larus spp.) sobre el Ostrero Pardo Biondi, L. M., M. S. Bó, & A. Vassallo. 2008. (Haematopus palliatus) en la albufera Mar Chi- Experimental assessment of problem solving in quita. Tesis de Licenciatura, Univ. Nacional de Milvago chimango (Aves: ). J. Ethol. Mar del Plata, Mar del Plata, Argentina. 26: 113–118. Khatchikian, C. E., M. Favero, & A. Vassallo. 2002. Biondi, L. M., G. O. García, M. S. Bó, & A. Vas- Kleptoparasitism by Brown-hooded Gull and sallo. 2010. Social learning in the Caracara Grey hooded Gull on the American Oyster- Chimango, Milvago chimango (Aves: Falconi- catchers in Mar Chiquita coastal lagoon, formes): an age comparison. Ethology 116: Argentina. Waterbirds 25: 137–141. 722–735. Martinez, M. M., & S. Bachmann. 1997. Kleptopar- Brockmann, H. J., & C. J. Barnard. 1979. Klepto- asitism of the American Oystercatcher Hae- parasitism in birds. Anim. Behav. 27: 487– matopus palliatus by gulls Larus spp. in the Mar 414. Chiquita Lagoon, Buenos Aires, Argentina. Cowan, P. J. 1968. Feeding relationships between Mar. Ornithol. 25: 68–69. Mullet and Herring Gulls. Brit. Birds 61: 31. Morand-Ferron, J., D. Sol, & L. Lefebvre. 2007. Furness, R. W. 1987. Kleptoparasitism in seabirds. Food-stealing in birds: brain or brawn? Anim. Pp.77–99 in Croxal, J. P. (ed.). Seabirds, feeding Behav. 74: 1725–1734. biology and role in marine ecosystem. Cam- Spivak, E., K. Anger, T. Luppi, C. Bas, & D. bridge Univ. Press, Cambridge, UK. Ismael. 1994. Distribution and habitat prefer- García, G. O., M. Favero, & R. Mariano-Jelicich. ences of two grapsid crab species in Mar Chi- 2008. Red-gartered Coot Fulica armillata feeding quita Lagoon (Province of Buenos Aires,

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