ORNITOLOGIA NEOTROPICAL 14: 397–403, 2003 © The Neotropical Ornithological Society

THE BLACK-GOGGLED TANAGER (TRICHOTHRAUPIS MELANOPS): AN OCCASIONAL KLEPTOPARASITE IN MIXED- FLOCKS AND ANT SWARMS OF SOUTHEASTERN

Marcos Maldonado-Coelho1,2 & Renata Durães1

Departamento de Biologia Geral, ICB, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, 31270-110, Belo Horizonte, Minas Gerais, Brazil.

Resumo. – O Tiê-de-topete (Trichothraupis melanops): um cleptoparasita ocasional em bandos-mis- tos de aves e correições de formigas no Sudeste do Brasil. – Cleptoparasitismo é raramente reportado para Passeriformes. Acredita-se que associações intra- e interespecíficas são situações ecológicas que podem favorecer a ocorrência de tal comportamento. Nos neotrópicos, associações de aves em bandos mistos e em torno de correições de formigas são comuns, mas mesmo durante estas associações cleptoparasitismo parece ser raro. O Tiê-de-topete (Trichothraupis melanops) é uma espécie freqüentemente registrada nestes dois sistemas sociais no Sudeste do Brasil, onde foi observada tentando roubar artrópo- des diretamente do bico de outras nove espécies de aves em 15 ocasiões, incluindo um ataque intraespecí- fico. O vôo ágil e o comportamento de forrageio tipo “sallier” apresentado nos bandos-mistos e correições são provavelmente algumas das características que permitem ao Tiê-de-topete roubar presas mesmo de espécies maiores, apesar do fato de que cleptoparasitismo é um comportamento de for- rageio infreqüente para esta espécie. Algumas das possíveis causas tanto para a ocorrência quanto para a aparente raridade de cleptoparasitismo em associações interespecíficas de aves nas florestas neotropicais são discutidas. Abstract. – Kleptoparasitism rarely has been reported among . One of the ecological situations in which this behavior is believed to be favored is during intra- and interspecific associations. In the Neo- tropics, assemblies of in mixed-species flocks and attending army-ant raids are common, but even in these associations kleptoparasitism seems to be uncommon. The Black-goggled Tanager (Trichothraupis me- lanops) is a species commonly recorded in mixed-species flocks and attending army-ant raids in southeast- ern Brazil. We observed this species attempting to steal arthropod prey from the bill of nine bird species on 15 occasions, during three years of study, including an intraspecific attack. The flight agility and sallying foraging behavior of the Black-goggled Tanager are probably some of the features that contribute to its ability to steal prey of even larger birds. We discuss some possible causes for both occurrence and apparent rarity of kleptoparasitic behavior in interspecific bird associations in Neotropical forests. Accepted 5 February 2003. Key words: Kleptoparasitism, Black-goggled Tanager, Trichothraupis melanops, Atlantic forest, Brazil, Mixed-species bird flocks, Ant swarms. ______1Current address: Department of Biology and International Center for Tropical Ecology, University of Mis- souri-St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121-4499, USA. 2Corresponding author’s e-mail: [email protected]

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INTRODUCTION toparasitic behavior by Black-goggled Tana- gers while in mixed-species flocks and The stealing of food, or kleptoparasitism, has following ant swarms. We test Brockmann & been recorded for a number of bird species, Barnard’s (1979) hypothesis that kleptopara- and is particularly common among Falconi- sitism should be more frequent in situations formes and Charadriiformes (reviewed in of food shortage by comparing the frequency Brockmann & Barnard 1979). In contrast, of this behavior between the dry and rainy although most bird species are in the order seasons. Additionally, since body size has Passeriformes, the incidence of this behavior been shown to mediate social dominance in seems to be infrequent and sporadic among foraging behavior among birds following passerines (but see Kellner & Cooper 1998, army-ant raids (Willis & Oniki 1978) and in Etterson & Howery 2001, Llambías et al. mixed-species flocks (Alatalo 1981, Alatalo et 2001). An ecological context that may favor al. 1986, Pierpont 1986, Alatalo & Moreno kleptoparasitism is the occurrence of intra- or 1987), we examine whether kleptoparasitic interspecific associations, because of the con- behavior of the Black-goggled Tanager is centration of potential hosts in such associa- influenced by host body size. Finally, we dis- tions (Brockmann & Barnard 1979). cuss some potential ecological causes for the Kleptoparasitism has been recorded in mixed- apparent rarity of this behavior in mixed-spe- species flocks in Africa and Asia (Greig-Smith cies flocks in Neotropical forests. Detailed 1978, Herremans & Herremans-Tonnoeyr descriptions of mixed-species flocks in our 1997, Hino 1998, King & Rappole 2001, in study area are published elsewhere (Mal- press), but is apparently rare among Neotro- donado-Coelho & Marini 2000, Maldonado- pical species, including those that take part in Coelho & Marini in press). mixed-species flocks or follow ant swarms, two of the most common social systems in METHODS this region (but see Munn 1986, Jullien & Thi- ollay 1998). We conducted this study during rainy (Octo- One of the bird species that most fre- ber to January) and dry (May to August) sea- quently forages in mixed-species flocks and sons from December 1996 to August 1999 in follows ant swarms in southeastern Brazilian Atlantic forest fragments at Viçosa (20º50’S, forests is the Black-goggled Tanager (Tricho- 42º56’W, 650 m a.s.l.) and Belo Horizonte thraupis melanops) (Willis 1986, Willis & Oniki (19º50’S, 43º50’W, 1100 m a.s.l.) Mun., Minas 1992, Rodrigues et al. 1994, Maldonado- Gerais State, southeastern Brazil. The forag- Coelho & Marini 2000). At some localities in ing behavior of the Black-goggled Tanager Minas Gerais State, the Black-goggled Tana- was recorded in these areas, where flocks (N ger has a nuclear role in mixed-species flocks, = 493) and ant swarms (N = 6, Labidus sp.) helping to maintain flock cohesion through were located and followed along roads and frequent vocalizations and conspicuous trails in the forest interiors and borders (see movements (Maldonado-Coelho 2000, Mal- details in Maldonado-Coelho 2000, Mal- donado-Coelho & Marini 2000). In addition, donado-Coelho & Marini 2000). We spent a this species is a flock sentinel, giving alarm total of 734 and 609 h following these two calls at the approach of potential predators types of associations during the rainy and dry such as hawk-sized birds and human observ- seasons, respectively. Once a flock was ers (Maldonado-Coelho pers. observ.). located, it was followed up to one hour or Here we provide the first reports of klep- until lost from sight. Observations at ant

398 KLEPTOPARASITISM IN BLACK-GOGGLED TANAGER

TABLE 1. Records of kleptoparasitism by the Black-goggled Tanager (Trichothraupis melanops) in mixed-spe- cies bird flocks (ms) and ant swarms (as) during rainy and dry seasons in Atlantic forest of Brazil.

Host species Number of Number of Type of Season Mean body mass successful uncessessful social (g) ± SD (N) attempts attempts system Rufous-browed Peppershrike (Cycla- 3 – ms dry 28.3 ± 3.4 (5)1 rhis gujanensis) Variable Antshrike (Thamnophilus cae- 2 1 ms rainy 20.9 ± 3.2 (46)1 rulescens) Red-eyed Vireo (Vireo olivaceus) 2 – ms dry 14.3 ± 1.1 (3)1 White-collared Foliage-gleaner (Ana- 1 1 ms rainy 37.8 ± 2.8 (5)2 bazenops fuscus) Sepia-capped Flycatcher (Leptopogon 1 – ms dry 11.6 ± 0.8 (13)1 amaurocephalus) Black-goggled Tanager (Trichothraupis 1 – ms rainy 22.3 ± 4.2 (22)1 melanops) White-shouldered Fire-eye (Pyriglena 1 – as dry 26.1 ± 1.9 (15)1 leucoptera) Red-crowned Ant-Tanager (Habia 1 – as dry 34.6 ± 2.0 (15)2 rubica) Rufous ( line- 1 – as dry 20.6 ± 3.5 (85)1 ata) Total number of observations 13 2

1Data from the authors, gathered mostly in the study areas. 2Data provided by R. Ribon (pers. com.). swarms varied from a few minutes to one prey from six bird species while associated hour. In general, a pair of Black-goggled Tan- with mixed-species flocks, and from three dif- agers was present in each flock and at each ant ferent bird species while following ant swarms swarm. We considered a kleptoparasitic (Table 1). Fifteen kleptoparasitism attempts, attempt to be whenever an individual Black- including an intra-specific attack, were goggled Tanager attacked another bird of the observed, of which 86.7% (N = 13) were suc- same or other species that was carrying an cessful. The number of kleptoparasitic events insect in the bill. The attempt was considered did not differ statistically between dry (N = 9) successful when the prey was seen in the bill and rainy (N = 6) seasons (χ2 = 0.067, df = 1, of the Black-goggled Tanager after its attack. P > 0.05; Yates’ correction for continuity). Even though birds were not banded, observa- The number of kleptoparasitic attempts was tions were recorded in different days and at not affected by host size, once that the num- several forest fragments (N = 7), so we ber of species smaller or larger than the Black- assumed that each kleptoparasitic attempt was goggled Tanager was similar (Table 1). Thus, carried out by distinct individuals. kleptoparasitism does not seem to be influ- enced by size dominance in this species. RESULTS The Black-goggled Tanager’s usual forag- ing behavior consists of scanning down and Black-goggled Tanagers were seen stealing up towards moderately distant foliage while

399 MALDONADO-COELHO & DURÃES perched on horizontal twigs. Foraging maneu- cies are the wide visual field provided by its vers are predominantly sallies (> 90%, N = flycatcher-like behavior and its central posi- 266; Maldonado-Coelho unpubl.) of one to tion in mixed-species flocks and ant swarms. several meters to capture arthropods in the air In ant swarms, its central position can be or from the upper and lower leaf surfaces. related to the absence of dominant bird spe- Kleptoparasitic attempts were all similar: the cies in this foraging system in southeastern Black-goggled Tanager watched other flock Brazil, which allows nonprofessional species or ant swarm members carefully, and stole the (e.g., Black-goggled Tanager) to move food directly from their bills. The theft was towards the center of this association (Willis always on the wing, and occurred immediately & Oniki 1978). Perching behavior on sites after host birds caught an arthropod from a that allow monitoring flockmates seems to substrate (air, leaves, twigs, or ground). We favor kleptoparasitism in at least one another did not observe any reaction of host individu- species (the Greater Racket-tailed Drongo; als to the attacks. King & Rappole in press). Lastly, although some studies show that arthropod biomass in DISCUSSION Atlantic forest is largely reduced during the dry season in comparison to the rainy season Ecological conditions that could favor the (e.g., Davis 1945, Develey & Peres 2000), the evolution of kleptoparasitism in birds include similar frequency of kleptoparasitic attempts the following: (1) large concentration of during the dry and the rainy seasons does not hosts, (2) large quantities of food, (3) high- seem to support Brockmann & Barnard’s quality food items, (4) predictable food sup- (1979) hypothesis that this behavior should ply, (5) visible food, and (6) food shortage be more frequent during periods of food (Brockmann & Barnard 1979). Of these, con- shortage (condition 6). This differs from Her- ditions 1, 3, 5, and 6 could possibly help to remans & Herremans-Tonnoyer’s (1997) explain the occurrence of kleptoparasitic observation that kleptoparasitism among behavior in the Black-goggled Tanager. In Fork-tailed Drongos (Dicrurus adsimilis) is relation to the first condition (large concen- more frequent in southern Africa during the tration of hosts), several individuals regularly coolest and driest periods, than during the forage together in mixed-species flocks and wet and hot summer months. However, the ant swarms, providing ecological opportuni- number of observations in the present study ties for food stealing. Even though we do not is small for such a comparison and needs to have information to test the third condition be interpreted carefully. (high-quality food items), it is possible that An important feature that possibly allows the Black-goggled Tanager only engages in Black-goggled Tanagers to steal food even kleptoparasitism when the prey captured by from larger bodied birds is their flight agility, the host is large enough to compensate the a characteristic that might be considered a effort of an attack. Although it was not possi- pre-adaptation for kleptoparasitic behavior ble to identify all prey items stolen, circum- (see Brockmann & Barnard 1979). Indeed, stantial evidence supporting this idea is that sallying behavior, characteristic of the Black- two were a large lepidoptera larvae and a goggled Tanager, seems to be a common cicada. Large prey items are also likely to be strategy among kleptoparasite species in more visible (condition 5). In addition, other mixed-species flocks, both in Neotropical characteristics that would increase prey visi- (Munn 1986, Jullien & Thiollay 1998) and bility and favor kleptoparasitism by this spe- Paleotropical (Herremans & Herremans-Ton-

400 KLEPTOPARASITISM IN BLACK-GOGGLED TANAGER noyer 1997, Hino 1998) regions. Similarly, forests could be that many flocking and ant- Munn (1986) suggested that the fast flight of swarm following individuals conceal them- Bluish-slate Antshrike (Thamnomanes schistogy- selves while handling prey, which makes them nus) allows it to steal arthropods flushed or less visible to potential parasitic species. In actually captured by other birds in Amazonian addition, Paulson (1985) highlights the impor- mixed-species flocks. Willis (1986) and Willis tance of visibility of parasites for kleptopara- & Oniki (1992) suggested that Black-goggled sitism. He suggests that this behavior is less Tanager’s flight agility allows it to attack larger common in woodlands when compared to bird species, e.g., White-shouldered Fire-eye more open habitats, although he also (Pyriglena leucoptera), when following army-ant acknowledges that this may be due to human swarms in southern Brazil. observers overlooking such behaviors due to As pointed out above, the aggregation of the reduced visibility in these habitats. The several individuals in mixed-species flocks and fact that most kleptoparasitism records in at ant swarms might provide an ecological mixed-species flocks have been done in dry opportunity favoring the occurrence of klep- forests and more open habitats is consistent toparasitism (Brockman & Barnard 1979). with this hypothesis (Greig-Smith 1978, Her- This behavior has been documented in remans & Herremans-Tonnoeyr 1997, Hino mixed-species flocks in African wooded 1998, King & Rappole 2001). It would be grasslands, in Madagascar’s dry forests, and in interesting to objectively test whether klepto- Asian dipterocarp forests, where parasitism is more common in mixed-species birds of the Dicrurus were seen several bird flocks in dry and more open habitats times stealing prey from other flock species than in humid and more closed forests, or if (Greig-Smith 1978, Herremans & Herre- this apparent trend is only an artifact of sur- mans-Tonnoeyr 1997, Hino 1998, King & vey due to the differences in visibility between Rappole 2001, in press). On the other hand, these habitats. although mixed-flocks and ant-swarms are It should be stressed that kleptoparasitism two of the most common types of social sys- seems to be an uncommon behavior for the tems in Neotropical forests (Willis & Oniki Black-goggled Tanager, because the frequency 1978, 1992; Powell 1985), kleptoparasitism of thefts is small in relation to the total num- seems surprisingly rare in this region. The ber of foraging maneuvers (5.6%, N = 266; only records we are aware of besides our Maldonado-Coelho unpubl. data). It would be study are provided by Munn (1986) and Jul- worthy to compare the frequency of klepto- lien & Thiollay (1998), who report that parasitism observed for the Black-goggled nuclear species of Amazonian canopy and Tanager with those recorded for other flock- understory mixed-species flocks (Lanius spp. ing species across different regions, but unfor- and Thamnomanes spp.) steal prey flushed by tunately this is not possible due to the lack of other flock species by giving false alarm calls detailed and quantitative information in these to deceive and distract them. Nevertheless, studies. However, kleptoparasitism by Black- the Black-goggled Tanager’s strategy of steal- goggled Tanagers is exceptional in that none ing food directly from the bill of other birds of the other species (approx. 90) recorded in seems to be uncommon among these species flocks and ant swarms in the study areas were (see also Herremans & Herremans-Tonnoyer recorded engaging in this behavior despite 1997). more than 1300 observation hours. It would One of the potential causes of the appar- be interesting to assess whether individual ent rarity of kleptoparasitism in Neotropical Black-goggled Tanagers across populations

401 MALDONADO-COELHO & DURÃES along their geographic range engage in klep- data. Am. Nat. 127: 819–834. toparasitism, and whether this behavior Alatalo, R. V., & J. Moreno. 1987. Body size, inter- occurs with the same low frequency observed specific interactions, and use of foraging sites in the two studied populations, in order to in tits (Paridae). Ecology 68: 1773–1777. evaluate if this is a stereotypical behavior for Brockmann, H. J., & C. J. Barnard. 1979. Klepto- parasitism in birds. Anim. Behav. 27: 487–514. this species (sensu Sherry 1990). Since the fre- Davis, D. E. 1945. The annual cycle of plants, mos- quency of stealing maneuvers by Black-gog- quitoes, birds, and mammals in two Brazilian gled Tanagers is small, the only apparent cost forests. Ecol. Monogr. 15: 243–295. to other species in associating with them in Develey, P. F., & C. A. Peres. 2000. Resource sea- mixed-species flocks is the occasional loss of sonality and the structure of mixed species bird prey. Conversely, these species likely benefit flocks in coastal Atlantic forest in southeastern from their sentinel behavior (Maldonado- Brazil. J. Trop. Ecol. 16: 33–53. Coelho & Marini 2000). Etterson, M. A., & M. Howery. 2001. Kleptopara- sitism of soil-foraging passerines by Logger- head Shrikes. J. Field Ornithol. 72: 458–461. ACKNOWLEDGMENTS Greig-Smith, P. W. 1978. The formation, structure and function of mixed-species insectivorous M. M. C. was supported by a Researcher bird flocks in west African savanna wodland. Grant from World Wildlife Fund (WWF) and Ibis 120: 284–297. by a scholarship provided by Conselho Herremans, M., & D. Herremans-Tonnoeyr. 1997. Nacional de Desenvolvimento Científico e Social foraging of the forktailed drongo Dicru- Tecnológico (CNPq). R. D. was supported by rus adsimilis: beater effect of kleptoparasitism? a scholarship provided by Conselho de Aper- Bird Behav. 12: 41–45. feiçoamento de Pessoal de Ensino Superior Hino, T. 1998. Mutualistic and commensal organi- (CAPES). M. M. C. and R. D. are currently zation of avian mixed-species foraging flocks in a forest of western Madagascar. J. Avian Biol. supported by CNPq and CAPES, respectively. 29: 17–24. The authors are grateful to COPASA-MG at Jullien, M., & J. M. Thiollay. 1998. Multi-species Belo Horizonte and to farm owners at Viçosa territoriality and dynamic of Neotropical forest for their authorization to conduct this study understorey bird flocks. J. Anim. Ecol. 67: 687– in their properties. M. L. Maldonado Coelho 703 revised the English. J. Rappole, M. Â. Marini, Kellner, C. J., & R. J. Cooper. 1998. Two instances M. F. Vasconcelos, M. Rodrigues, J. G. Blake, of kleptoparasitism in passerines. J. Field. Orni- B. Loiselle, C. D. Cadena, I. Jimenez, T. B. thol. 69: 55–57. Ryder, A. Azpiroz, A. Rodrigues and two King, D. I., & J. H. Rappole. 2001. Mixed-species anonymous reviewers improved substantially bird flocks in dipterocarp forest of north-cen- the manuscript with constructive criticisms. tral Burma (Myanmar). Ibis 143: 380–390. King, D. I., & J. H. Rappole in press. Kleptopara- sitism of Laughingthrushes by Greater Racket- REFERENCES tailed Drongos Dicrurus paradisieus in Myanmar (Burma). Forktail 117: 121–124. Alatalo, R. V. 1981. Interspecific competition in tits Llambías, P. E., V. Ferreti, & P. S. Rodrigues. 2001. Parus spp. and the goldcrest Regulus regulus: for- Kleptoparasitism in the Great Kiskadee. Wil- aging shifts in multispecific flocks. Oikos 37: son Bull. 113: 116–117. 335–344. Maldonado-Coelho, M. 2000. Efeitos da fragmen- Alatalo, R. V., L. Gustafsson, & A. Lundberg. 1986. tação florestal em bandos mistos de aves de Interspecific competition and niche changes in Mata Atlântica, no Sudeste de Minas Gerais. tits (Parus spp.): evaluation of nonexperimental M.Sc. thesis, Univ. Federal de Minas Gerais,

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