SHORT COMMUNICATIONS

ORNITOLOGIA NEOTROPICAL 20: 623–627, 2009 © The Neotropical Ornithological Society

NEST ASSOCIATES AND COLONY TREES OF THE RED- RUMPED CACIQUE (CACICUS HAEMORRHOUS, ICTERIDAE)

Marco Aurélio Pizo1

Universidade do Vale do Rio dos Sinos (UNISINOS), Centro de Ciências da Saúde, 93022-000 São Leopoldo, RS, Brazil. E-mail: [email protected] 1Current address: Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista. Av. 24-A, no. 1515, 13506-900, Rio Claro-SP, Brasil.

Aves e árvores associadas às colônias do Guaxe (Cacicus haemorrhous, Icteridae).

Key words: Cacicus haemorrhous, Pachyramphus, Red-rumped Cacique, Atlantic forest, Brazil, protec- tive nest association.

INTRODUCTION Coloniality is another well-known anti- predator strategy adopted by (Lack Nest predation is one of the most important 1968). However, coloniality has its drawbacks causes of nesting failure in birds (Martin because it is not equally effective against all 1995, Duca & Marini 2008). To protect their potential predators, and the aggregation of nests against predators, birds adopt an many individuals and nests in a restricted area impressive array of strategies. For example, may attract the attention of predators (Wit- protective nesting associations or the exploi- tenberg & Hunt 1985). As a consequence, it is tation of nest defense behavior of another not uncommon for colonial birds to adopt aggressive species are widespread among additional protective strategies, such as the birds. In a recent review, Quinn & Ueta selection of safe sites to establish their colo- (2008) identified 92 protected associate spe- nies. Colonial nesting (Icteridae) of cies in nine avian orders all over the world, the neotropical forests are good examples. but suspected that many more associations Their colonies may congregate dozens of remain to be discovered, especially in the nests and usually attract a variety of predators, tropics. birds are among the most from snakes to birds and monkeys (Robinson common ‘protected’ species, while Charadrii- 1985, Duca & Marini 2004). In the Peruvian formes and Falconiformes, together with sev- Amazon, colonies of Yellow-rumped eral wasp species, belong to the most Caciques (Cacicus cela) placed in lake islands or common ‘protective’ species (Quinn & Ueta near wasp nests are relatively safe from preda- 2008). tors (Robinson 1985). Similarly, at Parque

623 PIZO

Estadual do Rio Doce, aproximately 800 km METHODS north of the study site, Duca & Marini (2008) found that colonies of Red-rumped Caciques I searched for colonies of Red-rumped (Cacicus haemorrhous) established in swamp Caciques from 1993 to 2000 during regular areas presented higher nest survival than visits made to Parque Estadual Intervales colonies in forest or in lake margins. (PEI), more specifically to the Carmo Here I report on the nesting associations Research Station located at 700 m a.s.l.. PEI is involving Crested and Chestnut-crowned a 490 km2 reserve that forms, with adjacent Becards (Pachyramphus validus and P. castaneus, reserves, one of the largest blocks of well pre- respectively) and colonies of Red-rumped served Atlantic forest in southeastern Brazil. Caciques in an Atlantic forest reserve in Extensive areas of old-growth forest (sensu southeastern Brazil. Surprisingly, a nesting Clark 1996) surround the study site. The veg- association in which both protected and pro- etation is composed of Atlantic rain forest tective species are is not common (sensu Morellato & Haddad 2000), with trees in nature. Only four out of 64 studies sur- reaching up to 30 m, and patches of second veyed by Quinn & Ueta (2008) reported such growth vegetation near human settlements a combination. I also explore the possibility and along the margins of dirt roads. A dry- that Red-rumped Caciques select a particular cold season occurs from April to August tree species to establish their colonies. The (winter), and a wet-hot season from Septem- protection offered by such trees against pred- ber to March. The annual mean temperature ators and the possible existence of learned is c. 17ºC (range 4–38°C), the annual precipi- traditions (i.e., culture sensu Laland & Janik tation is 1600 mm per year. 2006) in the selection of nesting sites by Red- Colonies were monitored from September rumped Caciques are discussed. to January, which corresponds to the period Red-rumped Cacique is a colonial nesting during which they were active (Pizo pers. occurring in forested habitats of the observ.). At each colony we recorded the tree Amazon and in the Atlantic Forest in south- species, tree height (visually estimated) and eastern Brazil, northern Argentina, and east- diameter at breast height (DBH), the number ern Paraguay (Jaramillo & Burke 1999). Three of active cacique nests, and the presence of races are recognized: haemorrhous in the Gui- nest associates. I visually estimated the dis- anas, northern Brazil, southeastern Vene- tance from the nests of associate species to zuela, and eastern Colombia, pachyramphus in the nearest active cacique nest. the Amazon basin of Brazil and along its southern tributaries, and affinis in southeast- RESULTS ern Brazil, northern Argentina, and eastern Paraguay (Jaramillo & Burke 1999). Colonies I found seven cacique colonies, six of which of Red-rumped Caciques are established in were established in Piptadenia gonoacantha the same trees year after year. At each breed- (Leguminosae, Mimosoideae) trees ranging ing season, new pouch-like nests are con- from 8 to 17 m height (12.5–67.8 cm DBH). structed, while old nests gradually decay. The other tree species, with only three Colonies may be located close to wasp nests, cacique nests, could not be identified. and they may also form mixed colonies with Each colony had from two to 21 active other icterids, such as Yellow-rumped cacique nests. All but two of the colonies had Cacique and (Psarocolius spp.) associated nests of either Crested or Chest- (Feekes 1981, Jaramillo & Burke 1999). nut-crowned Becards; two of them had both

624 SHORT COMMUNICATIONS at the same time. The two colonies with no extent, Great Kiskadees are common birds at nest associated were the smallest ones, with the study site (Vielliard & Silva 2001) but were only two and three active cacique nests. The not observed nesting in association with largest of the colonies was monitored during cacique colonies. On the other hand, Crested four years; in all of them the colony had nests and Chestnut-crowned Becards occur at Rio of at least one of the associate species. The Doce (Augusto Alves, pers. com. 2008) but becards differed in the location of their nests were not recorded nesting at cacique colonies within the crown of the colony tree, but main- (Duca & Marini 2004). tained an apparently safe distance from the Although attracting a variety of nest pred- nearest active cacique nest. Nests of Crested ators, cacique species adopt a series of anti- Becards were more at the centre of the crown, predator behaviors that are apparently effec- 5.4 ± 2.8 m (range 2–10 m, n = 5) from the tive in driving nesting predators away from nearest cacique nest, while Chestnut-crowned their colonies (Feekes 1981, Robinson 1985). Becards placed their nests at the extremities Therefore, cacique colonies may constitute a of the crown, 6.0 ± 2.2 m (range 4–10 m, n = relatively safe nesting site for other nesting 5) from the cacique nest. The greatest dis- birds, which makes me believe that the tances from cacique nests were recorded for becards acted primarily as protected species nests placed in trees situated by the side of the while caciques were the protective species. colony tree (one record for each of the associ- Such a distinction may not be so straight- ated species). In total I found five nests of forward, however, because tyrant flycatchers each becard species associated with cacique are known to act as protective species for a colonies, and only two nests of each species variety of species (Skutch 1997). Duca & away from such colonies. Marini (2004), for instance, observed a White- I did not observe any agonistic interac- throated Kingbird attacking a hawk in a tions involving caciques and the nest associ- cacique colony, thus defending its own nest, ates, but extensive observations were not and indirectly the cacique nests. Protective made. In one colony with nests of the two nest associations, however, are not always becard species, however, I saw Crested beneficial, but may involve costs for both pro- Becards robbing nest material from the nest tected and protective species. The most of Chestnut-crowned Becards. common cost for protected species is preda- tion upon adults and eggs by the protective DISCUSSION species (Quinn & Ueta 2008). I did not observe the caciques harassing the becards, Protective nesting associations have already but my observations on the birds’ behavior been recorded for tyrant flycatchers, more were not extensive. The only cost I observed commonly involving wasp nests, but associa- involved the two protected species in the tions with cacique species as reported here form of piracy of nesting material, a kind of have also been observed elsewhere. Five out cost not mentioned by Quinn & Ueta (2008) of seven cacique colonies at Rio Doce had in their review. associated nests of tyrant-flycatchers (Great Regarding the selection of colony trees, Kiskadee Pitangus sulphuratus, White-throated the observations available indicate great Kingbird Tyrannus albogularis, Streaked Fly- geographical variability. At the Manaus region, catcher Myiodynastes maculatus, and Piratic Fly- C. h. pachyramphus choose Peltogyne trees catcher Legatus leucophaius; Duca & Marini (Leguminosae, Faboideae) to establish their 2004). Streaked Flycatcher and, to a lesser colonies, supposedly because the slender,

625 PIZO

FIG. 1. A section of a branch of Piptadenia gonoacantha showing the conspicuous blade-like crests with tiny spines growing lengthwise along the branch. smooth trunk of such trees deter predators perched on Piptadenia branches with (Oniki & Willis 1983). Based on 30 nest trees no apparent annoyance. No observation is of C. h. haemorrhous surveyed in Suriname, available regarding the use of Piptadenia trees Feekes (1981) found that birds are not selec- by snakes, another potential predator of tive in relation to the nesting trees. Similar cacique colonies. Therefore, the protection (if result was found for the Rio Doce population any) offered by Piptadenia trees against poten- where the seven colonies of C. h. affinis tial nest predators of cacique colonies is still monitored were established in six different unclear. tree species (Duca & Marini 2004). At PEI, The geographical variability noted above however, I believe that birds actively choose in the selection of a particular tree species for Piptadenia trees to establish their colonies. the establishment of colonies, both among Although the abundance of Piptadenia in and within cacique subspecies, offers an relation to other tree species is unavailable for opportunity to investigate the role played by the study area, I do not think that this is an culture as a driver of such selection. Even especially common tree. For instance, Nasci- though the selection of colony trees may be mento (1994) found no Piptadenia in ten governed by ecological (e.g., the putative 7.5x11.25 m plots set 8 km from the study protection against predators) or genetic driv- site. Piptadenia have small spines bore in blade- ers (possibly leading to differences among like crests that grow lengthwise along the subspecies), this did not preclude the occur- young trunk and branches (Fig. 1). This fea- rence of learned traditions determining not ture might act to prevent the access of poten- only the selection of colony trees itself, but tial nest predators to cacique nests, but I have also the tree features selected (Laland & Janik seen capuchin monkeys walking along and 2006).

626 SHORT COMMUNICATIONS

ACKNOWLEDGMENTS Laland, K. N., & V. M. Janik. 2006. The cul- tures debate. Trends Ecol. Evol. 21: 542–547. I thank the staff of Parque Estadual Intervales Martin, T. E. 1995. Avian life history evolution in for logistical support, and Wenilton for draw- relation to nest sites, nest predation, and food. ing so accurately the Piptadenia figure. Steven Ecol. Monogr. 65: 101–127. M. McGehee and an anonymous reviewer Morellato L. P. C., & C. F. B. Haddad. 2000. Intro- made useful comments on the manuscript. duction: the Brazilian Atlantic forest. Biotro- pica 32: 786–792. During the study I was supported by Nascimento, F. H. F. 1994. A sucessão secundária Fundação de Amparo à Pesquisa do Estado inicial na Mata Atlântica sobre a Serra de de São Paulo (FAPESP), and I am presently Paranapiacaba, Ribeirão Grande, SP. M.Sc. the- supported by a grant from the Brazilian sis, Universidade de São Paulo, São Paulo, Bra- Research Council (CNPq). zil. Oniki, Y., & E. O.Willis. 1983. Breeding records of REFERENCES birds from Manaus, Brazil: V. Icteridae to Frin- gillidae. Rev. Bras. Biol. 43: 55–64. Clark, D. B. 1996. Abolishing virginity. J. Trop. Quinn, J. L., & M. Ueta. 2008. Protective nesting Ecol. 12: 735–739. associations in birds. Ibis 150: 146–167. Duca, C., & M. Â. Marini. 2004. Aspectos da nidifi- Robinson, S. K. 1985. Coloniality in the Yelow- cação de Cacicus haemorrhous (Passeriformes, rumped Cacique as a defense against nest pred- Icterinae) no sudeste do Brasil. Ararajuba 12: ators. Auk 102: 506–519. 25–32. Skutch, A. F. 1997. The life of the flycatcher. Univ. Duca, C., & M. Â. Marini. 2008. Breeding success of Oklahoma Press, Norman, Oklahoma. of Cacicus haemorrhous (Linnaeus) (Aves: Ic- Vielliard, J. M. E., & W. R. Silva. 2001. Avifauna. teridae) in different environments in an Atlantic Pp. 125–145 in Leonel, C. (ed.). Intervales. forest reserve in southeast Brazil. Rev. Bras. Fundação para a Conservação e a Produção Zool. 25: 165–171. Florestal do Estado de São Paulo, São Paulo, Feekes, F. 1981. Biology and colonial organization Brazil. of two sympatric Caciques, Cacicus c. cela and Wittenberg, J. F., & G. L. Hunt. 1985. The adaptive Cacicus h. haemorrhous (Icteridae, Aves) in Suri- significance of coloniality in birds. Pp. 1–78 in name. Ardea 69: 83–107. Farner, D. S., J. R. King, & K. C. Parkes (eds.). Jaramillo, A., & P. Burke. 1999. New world black- Avian Biology, Volume 8. Academic Press, San birds. Princeton Univ. Press, Princeton, New Diego, California. Jersey. Lack, D. 1968. Ecological adaptations for breeding Accepted 5 August 2009. in birds. Methuen & Co., London, UK.

627