© 2004 British Ornithologists’ Union

Ibis

(2004),

146

, 351–354

Blackwell Publishing, Ltd.Oxford, UKIBIIbis0019-1019British Ornithologists' Union, 2004? 2004146?Short communication

Cooperative breeding in the Rufous-fronted Thornbird

M. Rodrigues & L.A. Carrara

Short communication

Co-operative breeding in the Rufous-fronted Thornbird

Phacellodomus rufifrons

: a Neotropical ovenbird

MARCOS RODRIGUES

*

& LUCAS AGUIAR CARRARA

Laboratório de Ornitologia, Departamento de Zoologia, ICB, Universidade Federal de Minas Gerais, CP 486,

31270-901, Belo Horizonte, MG, Brazil

Co-operative breeding is a social system in which morethan a pair of individuals help with a breeding attemptat a single nest or brood. Assistance consists of territorydefence, egg incubation and nestling feeding (Brown 1987).This social system has been reported for 308 bird speciesacross 27 families, accounting for 3.2% of all 9672 describedspecies (Arnold & Owens 1998). Usually, the aid-givers aremature offspring with some relationship to the breeders(Brown 1987, Emlen 1991).

Two main hypotheses have been put forward to explainwhy mature offspring delay dispersal and stay in their natalterritory where they will experience a reduced fitness gain.First, the ecological constraints hypothesis states that alack of available breeding territories prevents dispersalof mature offspring (Brown 1974, Emlen 1982). By contrast,the life history hypothesis explains the expression ofco-operative breeding only for some taxonomic lineagesin which low adult mortality and low reproductive and dis-persal rates are found (Arnold & Owens 1998). Althoughthe clumped taxonomic distribution of co-operative breedersis robust, it has been pointed out that information is lack-ing for many avian taxa (Cockburn 1998). Most, if notall, of the studied taxa have been either African andAustralian species or temperate species (mostly Nearctic)(Ford

et al

. 1988, Stacey & Koening 1990, DuPlessis

et al

.1995, Cockburn 1996, see review in Hatchwell & Komdeur2000). It is noteworthy that the gap mainly concernsthe endemic Suboscines of South America, a group thatcontains more than 20% of all passerine birds (Sibley &Monroe 1990).

This paper describes the co-operative breeding behav-iour of the Rufous-fronted Thornbird

Phacellodomusrufifrons

, a Neotropical endemic Suboscine passerine in thefamily Furnariidae. Skutch (1969) studied this species inVenezuela, but did not describe it as a co-operative breeder

(Skutch 1985). Here we report the first study of a colour-ringed population of the Rufous-fronted Thornbird, anddemonstrate that it is a co-operative breeder in which help-ers are engaged in territorial defence and nestling feeding.

METHODS

Study area

Fieldwork was carried out from September 1999 to April2001 at the ‘Parque Nacional da Serra do Cipó’, munici-pality of Jaboticatubas, at the central region of Minas Geraisstate, south-eastern Brazil. The study plot (19

°

12

′−

19

°

35

′

S, 43

°

27

′−

43

°

38

′

W) comprised about 100 ha withinthe Park along the upper Rio Cipó valley. The vegetationconsists of a riverine gallery forest, surrounded by

cerrado

,an open scrub savannah-like vegetation that grows in dry-soilareas (see Eiten 1972 for details).

Rainfall is highly seasonal, with a dry period from Aprilto September, and a wet period from October to March(Rodrigues

et al

. 2000). Mean annual precipitation isaround 1500 mm, falling primarily between Decemberand March. Mean annual temperature is relatively con-stant throughout the year varying between 17 and 18.5

°

C(Antunes 1986).

The species

The Rufous-fronted Thornbird inhabits thorny scrublandof South America, forming a disjunct distribution andthree recognized geographical races (Sibley & Monroe1990). It lives in groups ranging from two to ten individu-als, occupying permanent territories throughout the year(Carrara & Rodrigues 2001). It builds one of the largestnests of any Neotropical ovenbird. The nest can reach 2 mlong and 0.4 m wide, always hung from the extremities ofthe fine branches of isolated trees (Skutch 1969, Thomas1983). The nest is made of sticks and there are usuallytwo or three independent chambers, each with a uniqueentrance. Frequently, new chambers are added to the nest(Carrara & Rodrigues 2001). Other nests can often befound in the same or in a nearby tree (Sick 1993, Carrara& Rodrigues 2001). In the study area, the breeding seasonstarts by mid-September, second broods are rare and nestpredation is very rare (Carrara & Rodrigues 2001).

Field procedures

The birds were captured by mist-net and each was ringedwith a metal ring provided by the Brazilian EnvironmentAgency (CEMAVE-IBAMA) and with a unique combina-tion of colour plastic rings.

The nests were monitored weekly; stages of breedingwere deduced from the bird’s behaviour because it was notpossible to inspect nest chambers (see details in Carrara &Rodrigues 2001).

*Corresponding author.Email: ornito@mono.icb.ufmg.br

352

M. Rodrigues & L.A. Carrara

© 2004 British Ornithologists’ Union,

Ibis

,

146

, 351–354

We measured the role of each individual group memberfor nine territorial groups during (1) territorial defenceand (2) food delivery to the nestling.

Territory size was measured by plotting on a map thesong-posts used by the birds. The maximum polygonmethod was used to determine the size of the territory(Rodrigues 1996). These measures were taken throughoutthe breeding season for the years 1999/2000 and 2000/01.The number of points used to draw the territory polygonsranged from eight to 15.

We measured territorial defence by playing back theirterritorial song for 5 min near the nest tree. We recordedthe bird response behaviour and the number of birds thatapproached and replied to the playback song.

Parental care was measured during the nestling periodfor the breeding season of 2000/01. From behind camou-flaged hides built 10 m from the nests, we observed ringedbirds delivering food. Each nest was observed for a dif-ferent period of time throughout the nestling period asfollows: nest A 240 min, B 90 min, C 79 min, D 1050 minand E 300 min; we also recorded the identity of the visitingbird and time of the visit.

Because this species is sexually monomorphic, we couldnot sex the birds and we assumed that two members ofthe group that delivered the most food were the dominantpair. Reproductive success was measured as (1) thenumber of fledglings that survived up to the first weekafter leaving the nest, and (2) the number of fledglings thatsurvived up to 1 month after they left the nest.

RESULTS

Six out of nine groups bred in the season 2000/01 andfive of these groups had more than two members. Allthe groups with more than one pair showed co-operativebreeding, i.e. at least three members of the group engagedeither in territory defence or in nestling feeding.

The average territory size for the 1999/2000 season was2.81 ha (sd =

±

1.30) for ten territories. There was norelationship between group size and territory size duringthis season (

r

9

= 0.53,

P

= 0.12). The following season wasmarked by the disappearance of two territories and theenlargement of the remaining ones, so that the averageterritory size for the 2000/01 season was 4.05 ha (sd =

±

2.50)and again there was no relationship between group sizeand territory area (

r

7

= 0.01,

P

= 0.85).Territory holders responded in 90% of the playback

stimuli (

n

= 48), approaching the speaker and singing theircharacteristic duet. More than two individuals respondedin 81% of the trials in the groups with supposed helpers.A response with all the members of the groups wasrecorded in 30% of the trials (

n

= 32). Groups holding justtwo members responded to all except one trial (

n

= 12).The two birds always shared the response.

We observed sharing of food delivered to the nestlingamong at least three individuals for all the groups holding

more than two members (Fig. 1). In general, two membersof the group were responsible for most of the feeding.Helpers made approximately 20% of the visits to deliverfood to the nestlings.

Groups with helpers produced 1.8 fledglings (sd =

±

1.8),whereas groups without helpers produced 0.5 (sd =

±

1.0);however, as yet, our sample size is too small to testwhether this difference is statistically significant.

The fledglings fly poorly during the first 10 days afterleaving the nest, during which time they were still fed bythe adults, and were usually seen calling from exposedbranches. Only 45% of the young survived beyond theirfirst month. Nine fledglings were produced in the groupswith helpers, but only four (44%) survived beyond thefirst month. Two fledglings were produced in the groupwithout helpers and one (50%) survived beyond thefirst month.

DISCUSSION

The Rufous-fronted Thornbird population studied hereshowed a high frequency of co-operative breeding inwhich more than a pair helped in territory maintenanceand feeding the nestlings. Considering just the groups thatbred, the frequency of co-operative breeding is very high(83%). This puts the Rufous-fronted Thornbird among the23 species with the highest rates of co-operative breeding(Arnold & Owens 1998). The present paper is the firstunequivocal report of co-operative breeding with helpersat the nest for the Furnariidae (Skutch 1985, Brown 1987,Sick 1993, Arnold & Owens 1998). Skutch (1969) did notobserve helpers at the nest in his Venezuelan study popu-lation, although he found other members of the grouphelping in nest building. However, because Skutch didnot colour-ring the birds, his observations were limited,as indeed he himself stated (Skutch 1969, p. 36).

Recently, much attention has been given to interspecificstudies attempting to provide a comprehensive explana-tion for the evolution of co-operative breeding (Koening

et al

. 1992, Arnold & Owens 1998, 1999). Hatchwelland Komdeur (2000) emphasized that there is a markedgeographical variation in the occurrence of co-operativebreeding. Co-operative breeding is common in the tropicsand remarkably prevalent in Australian birds. This unevendistribution suggests either an environmental or a phylo-genetic effect on the evolution of co-operative breeding.Arnold and Owens (1998) analysed 79 species that ‘defi-nitely’ co-operated in breeding, and found that this behav-iour is not randomly distributed among avian taxa. In thisrespect, the social systems of Neotropical Suboscines arevirtually unknown (see Sick 1993 for an overview of thestate of knowledge of Neotropical birds). For example,the Furnariidae represent more than 20% of all Suboscinebirds, or approximately 231 species (Sibley & Monroe1990). The family includes three well-established lineages:the Furnariinae, the Synallaxinae and the Philydorinae

© 2004 British Ornithologists’ Union,

Ibis

,

146

, 351–354

Cooperative breeding in the Rufous-fronted Thornbird

353

(Sibley & Ahlquist 1990, Zyskowski & Prum 1999).

Pha-cellodomus

is a genus of seven species within the Synallax-inae, all of which share behavioural characteristics such asa large domed nest made of hard dead sticks, song duet andgroup living in open country (Sick 1993, Ridgely & Tudor1994). We suspect that co-operative breeding might befound in other

Phacellodomus

species and other Synallaxinae,such as the Firewood Gatherer

Anumbius anumbi

and, asalready suggested by Whitney

et al

. 1996 the Pink-leggedGraveteiro

Acrobatornis fonsecai

. Two other Philydorinae,

the Rufous Cachulote

Pseudoseisura cristata

and theBrown Cachalote

P. lophotes

, also show behaviouralcharacteristics similar to

Phacellodomus

, and might showco-operative breeding, as suggested by Zimmer andWhittaker (2000). Studies on the breeding biology andsocial behaviour of Suboscines will be important tostrengthen future phylogenetical analysis.

We are indebted to L.P. de Faria, L. Atzeni, H.B. Gomes andD. Sarfar for their essential support in the field. C. Jacobi, J. Bertoluci,

Figure 1. Percentage of food delivered to nestlings by each individual of five (out of six) breeding groups of the Rufous-fronted Thornbirdthat had more than two members. The individual birds are named according to ring colours. Grey bars refer to delivering visits (numberof visits) and white bars refer to food load (percentage of small items). Numbers above bars are the absolute values. ‘Non’ refers to anunringed bird.

354

M. Rodrigues & L.A. Carrara

© 2004 British Ornithologists’ Union,

Ibis

,

146

, 351–354

L. Atzeni, M.A. Pizo and two anonymous referees made construc-tive suggestions and criticism of the manuscript. This work wassupported by ‘Fundação O Boticário de Proteção à Natureza’ andPRPq-UFMG. M.R. is supported by the Brazilian Research Coun-cil (CNPq) and L.A.C. received a student fellowship from CNPq(PIBIC-UFMG). We thank the staff of the Brazilian Environmen-tal Agency (IBAMA and CEMAVE), especially Albino B. Gomes(Director of the ‘Parque Nacional da Serra do Cipó’), for allowingus to work in the Park.

REFERENCES

Antunes, F.Z.

1986. Caracterização climática do estado deMinas Gerais.

Inf

.

Agropec

.

12

: 9–13.

Arnold, K.E. & Owens, I.P.F.

1998. Cooperative breeding inbirds: a comparative test of the life history hypothesis.

Proc

.

R

.

Soc

.

Lond

.

B

265

: 739–745.

Arnold, K.E. & Owens, I.P.F.

1999. Cooperative breeding inbirds: the role of ecology.

Behav

.

Ecol

.

10

: 465–471.

Brown, J.L.

1974. Alternative routes to sociality in jays: with atheory for evolution of altruism and communal breeding.

Am

.

Zool

.

14

: 63–80.

Brown, J.L.

1987.

Helping and Communal Breeding in Birds:Ecology and Evolution

. Princeton: Princeton University Press.

Carrara, L.A. & Rodrigues, M.

2001. Breeding biology ofthe Rufous-fronted Thornbird

Phacellodomus rufifrons

, aNeotropical ovenbird.

Int

.

J

.

Ornithol

.

4

: 209–217.

Cockburn, A.

1996. Why do so many Australian birds cooper-ate: social evolution in the Corvidae? In Floyd, R.B., Sheppard,A.W. & De Barro, P.J. (eds)

Frontiers in Population Ecology:

451–472. Melbourne: CSIRO Publishing.

Cockburn, A.

1998. Evolution of helping behaviour in coopera-tively breeding birds.

Annu

.

Rev

.

Ecol

.

Syst

.

29

: 141–177.

DuPlessis, M.A., Siegfried, W.R. & Armstrong, A.J.

1995.Ecological and life history correlates of cooperative breedingin South African birds.

Oecologia

102

: 180–188.

Eiten, G.

1972. The cerrado vegetation of Brazil.

Bot

.

Rev

.

38

:201–341.

Emlen, S.T.

1982. The evolution of helping. I. An ecologicalconstraints model.

Am

.

Natur

.

119

: 29–39.

Emlen, S.T.

1991. Evolution of cooperative breeding in birds andmammals. In Krebs, J.R. & Davies, N.B. (eds)

BehaviouralEcology: an Evolutionary Approach:

301–307. Oxford:Blackwell Science.

Ford, H.A., Bell, H., Nias, R. & Noske, R.

1988. The relation-ship between ecology and the incidence of cooperative

breeding in Australian birds.

Behav

.

Ecol

.

Sociobiol

.

22

:239–249.

Hatchwell, B.J. & Komdeur, J.

2000. Ecological constraints, lifehistory traits and the evolution of cooperative breeding.

Anim

.

Behav

.

59

: 1079–1086.

Koening, W.D., Pitelka, F.A., Carmen, W.J., Mumme, R.L. &Stanback, M.T.

1992. The evolution of delayed dispersal incooperative breeders.

Q

.

Rev

.

Biol

. 67: 111–150.Ridgely, R.S. & Tudor, G. 1994. The Birds of South America:

the Suboscine Passerines. Oxford: Oxford University Press.Rodrigues, M. 1996. Song activity in the Chiffchaff: territorial

defence or mate guarding? Anim. Behav. 51: 709–716.Rodrigues, M., Carrara, L.A. & Faria, L.P. 2000. Avifauna como

ferramenta para o monitoramento de Unidades de Conservação.In Milano, M. (ed.) II Congresso Brasileiro de Unidades deConservação: 356–364. Campo Grande: Rede NacionalPró-Unidades de Conservação.

Sibley, C.G. & Ahlquist, J.E. 1990. Phylogeny and Classifica-tion of Birds. New Haven: Yale University Press.

Sibley, C.G. & Monroe, B.L. 1990. Distribution and Taxonomyof Birds of the World. New Haven & London: Yale UniversityPress.

Sick, H. 1993. Birds in Brazil. Princeton: Princeton University Press.Skutch, A.F. 1969. A study of the Rufous-fronted Thornbird and

associated birds. Wilson Bull. 81: 5–43.Skutch, A.F. 1985. Clutch size, nesting success, and predation

on nests of neotropical birds, reviewed. Ornithol. Monogr. 36:575–594.

Stacey, P.B. & Koening, W.D. 1990. Cooperative Breedingin Birds: Long-Term Studies of Ecology and Behavior.Cambridge: Cambridge University Press.

Thomas, B.T. 1983.The Plain-fronted Thornbird: nest construc-tion, material choice and nest defence behavior. Wilson Bull.95: 106–117.

Whitney, B.M., Pacheco, J.F., Da Fonseca, P.S.M. & Barth, R.H.1996. The nest and nesting ecology of Acrobatornis fonsecai(Furnariidae), with implications for intrafamilial relationships.Wilson Bull. 108: 434–448.

Zimmer, K.J. & Whittaker, A. 2000. The Rufous Cachalote(Furnariidae: Pseudoseisura) is two species. Condor 102:409–422.

Zyskowski, K. & Prum, R.O. 1999. Phylogenetic analysis of thenest architecture of neotropical ovenbirds (Furnariidae). Auk116: 891–911.

Received 15 November 2002; revision accepted 30 July 2003.