Notes on the Biology and Song of the Red-Legged Seriema (Cariama Cristata)

JOURNAL OF FIELD ORNITHOLOGY Formerly BIRD-BANDING A Journal o! Ornitholoqical Investiqation

VOL. 57, NO. 4 AUTUMN 1986 PAGES261--353

J. Field Ornithol., 57(4):261-269

NOTES ON THE BIOLOGY AND SONG OF THE RED-LEGGED SERIEMA (CARIAMA CRISTATA)

BY KENT H. REDFORD AND GUSTAV PETERS

Very little, even of an anecdotalnature, has been written on the two living seriemas,the Black-leggedor Burmeister'sSeriema (Chunga burmeisteri),and the Red-legged,or CrestedSeriema (Cariama cristata) (Blake 1977). Yet they are not rare in zoologicalcollections and are fairly common in many areas of South America south of the Amazon. The Red- legged Seriema is found in grasslandsand open scrub of central and eastern Brazil from the state of Ceara west to Mato Grosso State and easternBolivia, and south to Uruguay, Paraguay, and the Argentinian provincesof San Luis, La Pampa, and Entre Rios (Blake 1977, Frieling 1936). Indeed, the Red-leggedSeriema is one of the mostfrequently seen large birds in central Brazil where KHR spent 2 yrs. It is even more frequently heard than seenbecause its loud distinctivesongs carry for several kilometers. This paper reports incidental field observationsmade on Red-legged Seriemasand presentsan analysisof the vocalizationsof severalcaptive and wild Red-leggedSeriemas. This information is combinedwith the limited publisheddata for the two speciesof seriemasto constructhy- pothesesabout the behavior of a little known species,and to propose further researchto test these hypotheses.

METHODS Data were collectedduring a 1981-1982 studyof giant anteaters.Red- leggedSeriemas were observedas the opportunityarose and notestaken on behavior, singing, and nests.The principal study area was Emas National Park, a 131,868 hectarepark on the border of Goias and Mato Grosso do Sul States in southwesternBrazil (18ø45'S and 52ø45'W). Emas Park is in the cerrado ecosystem,a xeromorphic, semideciduous savannacomposed of severaldistinct subunits(Eiten 1972). The most commonsubunit in Emas is grassland,followed by cerrado or semi- arboreal scrublandand by cerradaoor tall cerradocharacterized by a greaterdensity of tall trees.Termite moundsform an important part of the landscapewhere the vegetationis open and are particularly common in areasadjacent to the park where cattlegraze (Redford 1984). Approximately 1500 mm of rain falls during the September-May wet

261 262] K. H. Redfordand G. Peters j. FieldOrnithol. Autumn 1986

season(Anonymous 1981). Virtually no rain falls and the temperature can exceed55 ø during the day during the rest of the year. Fire is an importantelement in the cerradoecosystem; uncontrolled fires setoutside the park enter and burn virtually the whole park every severalyears (Redford 1985). Three calling sequencesof one unsexedindividual of a pair kept at the National Zoo in Washington D.C. were recordedon 51 August 1982. The recordingswere madeon Ampex 652 tape with a Uher tape recorder (Florida State Museum Master Tape No. 673). One calling sequence recordedby W. Belton in central Brazil (Cornell University Library of Natural Sounds,Cat. No. 20029) was also analyzed.We do not know to what extentthe recordingscontain the full lengthof the callingseries. Sonographicanalyses were done in variousfrequency ranges between 20 and8000 Hz. Soundspectrograms were produced on a Kay Sonagraph Model 7029A, Kay Digital SonagraphModel 7800 and Voiceprint Mod- el 4691A. All spectrogramswere producedusing wide band settingsand flat shaping.Frequency and temporal parameterswere measuredin the sonagramswith overlay grids. No direct measurementsof call intensity were made. Intensity data presentedin this paper representloudness of the calls as perceivedby the observer.

RESULTS Biology.--Red-leggedSeriemas were commonlyseen in and adjacent to the park, particularlyin areasthat had beenrecently burned or grazed where there appearedto be a greater number of invertebratesfor which the birds were apparentlysearching. Seriemas were usuallysingle (n = 25) or in pairs (n = 20), thoughgroups of three (n = 4) and four (n = 1) were occasionallyseen. Within a group, seriemaswere usuallyclose to each other. When one individual in a group or pair was frightened and ran, it was often followed by the other members. Seriemaswere reluctant to fly and could be chasedin a car at speedsup to 25 km/h beforetaking off. Their flightswere short, usually consistingof a burst of rapid flapping followedby a long glide. Seriemasare strong,agile runnersand can easilyoutdistance a human over unevenground. Seriemas nest in low trees. Six nests were found between 1 and 5 m in trees growing in open grasslandor cerrado. Three nests found in Septemberand October containedclutches of 2 eggs(pers. obs., Mat- thews, pets. comm., Ridgely, pets. comm.). One nest was observedby Matthews from a blind over a period of severalweeks. Two eggswere hatchedin a nest2.5-5 m off the groundand the chickswere fed by both parents.The adult birds broughtsnakes or worm lizards to the nest.The adult birds always approachedthe nest on foot and jumped up into it (Matthews, pers. comm.). Some time between 10 and 14 d after hatchingthe parents fed the young in the nest and then jumped down to the ground and vocalized quietly until 1 of the chicksleft the nest. The 5 birds stayednear the nestwith the parentscalling continually for 15 min beforewalking away. Vol.57, No. 4 Biologyand Song of the Red-legged Seriema [263

Within 5 min of the parents' departure, the secondchick jumped from the nest and movedoff towards its parents (Matthews, pers. comm.). On only two occasionsdid we observebehavior other than singingand foraging.The first was a copulationin September.The male approached the female, hoppedonto her back and remainedin copulafor 12 s before dismounting.The other behavior was an aggressiveencounter between 2 seriemasthat repeatedlyjumped at one another, feet first, flapping their wings for balance. This behavior continued for about a minute beforethe birds, detectingthe observer,fled. Song.--Although seriema singingwas heard from before dawn until well after dark, the majority of songswere heard in early-mid morning. The songis composedof three parts, not all of which are always sung together.For example, somebirds sangonly the introductorypart of the songand then resumedforaging. Usually, however,several complete songs were sung in a row, the averagelength of 11 singingbouts being 70.5 s (range = 32-95). In suchcases it was impossibleto countthe numberof individual songsbecause more than one bird in a group was singing. When one member of a pair began to sing the other member often began to sing as well. In such casesit appeared as if the secondbird often beganits songjust as the songof the first bird was finishing.Since songswere often repeatedmany times within a bout, this out-of-phase placement of songsresulted in a continuoussong. In one instance3 membersof a group sang at the same time. A seriemaoften respondedto the songof anotherbird by singing;this was true both within and between pairs. When a songwas heard, the seriemastopped, listened for severalseconds, and then either resumedits activity or sang. Before singing,virtually all birds jumped onto a Cor- nitermescumulans termite mound,a fence,or a low tree (Fig. 1). Singing was performedin a very characteristicway: the introductoryparts of the songwere sungwith the neck held straightwhile the loudestportions of the songwere sung with the neck bent and the back of the head nearly touchingthe back of the bird (seephotographs in Schneider1957). Seri- ema songsare very loud and can carry severalkilometers. Thus, up to 4 individualsor groupscould often be heard singingsimultaneously. The vocalizationsrecorded and analyzed for adult seriemasare long, intense, and structurally complex sequencesof tonal notes, i.e., songs (Pettingill 1970, Thorpe 1964). The 4 songsof the 2 individualsanalyzed show a rather uniform structure.The songswere clearly organizedinto 3 phrases(terminology cf. Jellis 1977), each of which had a distinct compositionand progressivechange of certainstructural parameters (Fig. 2 and Table 1). The general structureof thesesongs agrees with those describedby Schneider(1957). The first phrase (A) (Fig. 2) was a series of short notes with the intercall intervalsbecoming shorter as the phrase proceeded.In the second phrase(B), notesof the samestructural type as in A were grouped into short sub-phrases(in pairs, triplets, or more elements),the interval between two successivesub-phrases being longer than any interval be- 264] K. H. Redfordand G. Peters j. FieldOrnithol. Autumn 1986

FIGURE1. Carlamacristata in typical singingposition on top of a termite mound. tween noteswithin them. The third phrase(C) was the moststructurally complexin the seriema'ssong. It consistedof bi-partite sub-phraseswith 10 or more notes;the first sectionof the sub-phraseshaving fewer elements than the second.Phrase C was further divided into two parts becausethe entire songrose to a climax in phrase C. In phraseA call duration was relativelyuniform at about 0.15-0.16 s. Intervals between the notes decreasedin duration almost continually from a maximum of about 10 s at the beginningof the songto a minimum of about 1 s at the end of the phrase. The pitch of the notesremained nearly constant,the fundamentalhaving its maximum frequencyat 1.2- 1.3 kHz. The duration of the notes in phrase B stayed relatively uniform at between 0.15-0.16 s. In sub-phraseswith 3 or more notesthe duration of the intervalsbetween notes usually becameprogressively shorter from a maximum of about 1 s to a minimum of about 0.2 s. The pitch of the notesin phraseB stayedabout the sameas in phraseA, the fundamental reachingits highestfrequency at about 1.3-1.4 kHz. Notesin phrasesA and B had a frequency range from about 0.4 to above 8 kHz with the main energy in the range betweenapproximately 0.8-2.6 kHz. Phrase C was structurally more complexthan phrasesA and B not only becauseof structural changesin the notes composingit but also becauseof changesin various other structural parameters.The gradual Vol.57, No. 4 Biologyand Song of the Red-legged Seriema [265

phrase A B sub-phrase caU: BI elemenl phrase C sub -phrase C• C2 section C•a I C• C2a I C2b

FIGURE 2. General structural schemeof Cariama cristatasong. The bottom graph is a continuation of the top graph.

structural changesfrom one note to the next within a sub-phraserep- resented a continuum of intermediate forms of the basic note structure. Like phrase B, phrase C consistedof sub-phraseswhich themselves were divided into two sections(Fig. 2), each with unique structural characteristics,an internal changein certain structural parametersand a progressivestructural change from sub-phraseto sub-phrase(see Table 1). The interval betweentwo successivesub-phrases was always longer than any interval betweentwo successivecalls within thesesub-phrases. The number of notesin the a and b sections(Table 1) of a sub-phrase in phrase C increasedprogressively until about the climax of the song and from then on stayedrelatively constant.In the beginningof the song, a-sectionshad 4 or 5 notes and in the climax may have had up to 6, b-sectionsat the start of the song also had 4 or 5 notes,but may have had up to 10 or more by the climax. The frequencyrange of the notesin phraseC was about0.4 to above 8 kHz with the main componentsbelow 4 kHz. In all notesof sections a and b the fundamental had the highest energy. In the a-sectionsthe first and/or secondharmonic also had relatively high energy, further harmonicsbeing only faintly represented.In the initial notesof the b-sectionsthe first harmonicwas the mostpronounced after the fundamental. In the final notesthe secondharmonic had a higher energythan the first. In the first note of the b-sectionsin the beginningof phraseC the second harmonichad more energythan the first; in later sub-phrasesthis relationship was reversed.

DISCUSSION The scantpublished information on the Red-leggedSeriema can be combinedwith the data gathered in Emas Park and the fragmentary information available on the Black-leggedSeriema, Chunga burmeisteri, to generatefive hypotheseson variousaspects of cariamidbiology. Feeding.--In Emas Park Red-leggedSeriemas were commonlyseen foraging in areas with cattle dung. As might be expectedfrom this, 266] K. H. Redfordand G. Peters J. Field Ornithol. Autumn 1986

TABL• 1. Structural characteristicsof songin Cariamacristata (refer to Fig. 2).

Phrase

A B C Structural Sequenceof tonal Sequenceof tonal Sequenceof tonal changesin calls of uniform calls of uniform calls with changes respective duration and pitch duration and pitch, in severalstructural parts of the groupedin parameters,grouped song sub-phrases in sub-phrases Within-phrase Decreasingdura- Decreasingduration Decreasingduration tion of intervals of intervals be- of intervals between between calls tween sub-phrases sections of (increasinginten- (and intervals sub-phrases;pitch- sity of calls) within sub-phras- changewithin sub- es) increasing phrasesfirst number of calls increasing,later de- per sub-phrase creasing;increasing (increasinginten- number of calls per sity of calls) sub-phrase(in the beginning);in the beginningincreas- ing duration of sub- phrases Within sub- Decreasingduration See below phrase of intervals between calls in sub- phraseswith >3 calls; increasing intensityof calls Within sections a-sections:increasing intensity,pitch and duration of calls, decreasingduration of intervals between calls; b-sections: de- creasingintensity, pitch and duration of calls

stomachsof the Red-legged Seriema contain grasshoppers,Atta ants, beetles,larval insects,a few small fruit, and tree gum (Burmeister1938, Miranda-Ribeiro 1938). This speciesalso eats snakes and other reptiles, small birds, and small mammals(Sick 1984). In the wild and in captivity Cariarna grabs small vertebratesin its beak and beats them against the ground before dismemberingthem with its beak and claws (Miranda- Ribeiro 1938, Santos 1979, Sick 1984). The Black-leggedSeriema has similar food habits. In Tucuman, Ar- gentina they were often observedforaging near cattle and horse dung. The gizzardsof 4 individualscontained beetles, locusts, green leaves, and grasswith a few hard seedsand the body of an entire rat or youngcavy. Vol.57, No. 4 Biologyand Song of the Red-legged Seriema [267

Black-leggedSeriemas in captivity greedilyfed on the bodiesof rats and birds.As was the casewith the Red-leggedSeriema, the prey was beaten on the groundbefore being consumed(Boyle 1917). Hypothesis.Seriemas are omnivoresconsuming prey in relationship to its availability. During the nestingseason they catchmore vertebrates to feed to the young. Songtransmission.--The Cariama songhas been describedas a cross between"the serratedbark of a youngdog and the cluckingof turkeys" (Burmeister1938; translationby KHR). This songis heard during the day as well as before dawn and many birds may sing at the sametime (Burmeister1958). Most singingis donein the morning,and usuallythe bird singsfrom an elevatedposition. Chunga'ssong has been described by Boyle (1917): "The call noteswere a seriesof criesand yelpswhich were givenin chorus;that is oneindividual would start his queer,turkey- like yelps,while other birdsjoined in until four or five would be chanting at the same time." Like the Red-leggedSeriema, C. burmeisterihas a loud songthat starts with a sustainedcall, followed by a seriesof calls in quick successionwith progressivelydecreasing pitch. In the end of the songthe short calls are merged. Chunga songsare usually heard in the morning and the eveningand rarely at other times of the day. Hypothesis. Singing from an elevatedposition in the morning serves to reducelosses in soundpropagation (Morton 1975, Marten and Marler 1977, Wiley and Richards 1978). Songattenuation.--Most calls of the Cariama songhave their energy peak in the range between 1 and 2 kHz, which in foresthabitats atten- uates lessthan either lower or higher frequencies(Marten and Marler 1977, Marten et al. 1977). In grasslandhabitat excessattenuation in- creaseswith increasingfrequency (measurements taken 1 ft [50 cm] above the ground; Morton 1975). In nonpasserinegrassland birds in Panama Morton (1975) found an emphasizedfrequency range around 5.1 kHz which is considerablyhigher than the main energy frequenciesin the seriema'ssong. Hypothesis.The main frequencyrange in a seriema'ssong is probably relatively little affectedby excessattenuation. Developmentof youngand of singing.--The nest of Cariamacristata is large and poorly constructed,similar to the nestsof raptors and located within 5 m of the ground. Its clutch is usually 2 or 5 eggswhich are incubatedfor 26-50 d (Burmeister 1958, Miranda-Ribeiro 1958, Santos 1979). In captivity one chick was fed meat, mice, hard-boiledeggs, and cockroachesby its parents and left its nest at 1 mo of age (Seth-Smith 1912). Sick(1984) reportsseriema chicks leaving the nestat 12 d, already with the ability to singportions of the adult songalbeit weakly. According to Heinroth (1924) a 12 day-old captive Cariama called "in the typical manner of the seriema" (translation by GP); probably referring to the species'song. He also reported that the same individual producedthis samevocalization at 1 mo of age in responseto the unisoncalls of cranes. Eisentraut (1935) reported a low-intensitysingle note beggingcall of 268] K. H. Redfordand G. Peters J.Field Ornithol. Autumn 1986 a 2-wk-old C. burmeisteri. The same individual, a short while later, producedthe adult songonly slightlymodified and at a lower intensity. By the age of 2-3 wks, juvenilesof both speciesof seriemaseem able to producethe adult song.The fact that in the wild young leave the nest by 2 wks of age indicatesrapid physicaldevelopment coupled with this rapid acquisitionof the complexadult song. Hypothesis.Young seriemasassist their parents in defendinga terri- tory. This includessinging territorial songs. Territoriality.--Red-leggedSeriemas frequently respondto the songs of conspecifics.Birds will stop and listen to a song, respondingif the songis from another group, or joining if the songis being sung by a group member.The third or fourth bird in a group is almostdefinitely the offspring of a pair and at least 3 and probably 4 birds in several groupshave been heard singingsimultaneously. Boyle (1917) describedone captiveChunga as repeatedlyrunning at a tree and hitting it with both feet. This behavior is similar to that describedearlier in the agonisticinteraction between two Cariama and is expectedwhen singing doesnot serveto separateseriemas. Hypothesis.Seriemas are territorial and their loud songsserve to sep- arate family groups.

ACKNOWLEDGMENTS The recordingsof the callsof a juvenile seriemawere kindly provided by Mr. H. Lutgens.KHR would like to thank the National Geograph- ical Society,Harvard University, the Organization of American States and Friends of the National Zoo for financial support. The work in Emas Park was made possiblethrough permissionof IBDF and the directorHeber Silva de Oliveira. Dr. E. Morton kindly loanedhis equip- ment. GP participatedin this studyduring a stay at the Department of ZoologicalResearch, National ZoologicalPark, which was madepossible througha Smithsoniangrant extendedby Dr. D. G. Kleiman. We would like to thank the followingpeople for criticizingthe manuscript:Drs. J. F. Eisenberg,J. G. Robinson,E. Morton, and N. T. Wheelwright.

LITERATURE CITED

ANONYMOUS.1981. Plano de manejo.Parque Nacional dasEmas. Doct. tec. No. 4 MA/ IBDF and FBCN. Brasilia. BI•^K•, E. R. 1977. Manual of Neotropicalbirds. Vol. 1. Univ. ChicagoPress, Chicago. BOYLe,H.S. 1917. Field noteson the seriema (Chungaburmeisteri). Auk 34:294-296. BUI•MEISTER,H. 1938. Contribuicao para a historia natural da seriama. Rev. Museu Paulista 23:91-152. EISENTR^UT,M. 1935. BiologischeStudien im bolivianischenChaco. VI. Beitrag zur Biologieder Vogelfauna.Mitt. zool. Mus. Berlin 20:367-443. EIT•N, G. 1972. The cerradovegetation of Brazil. Bot. Rev. 38:201-341. FR•I•NG, H. 1936. Cariama cristataL. als Anpassungsforman das Savannenleben.Z. Morph. Okol. Tiere 30:673-730. HE•N•OTH, O. 1924. Die Jugendentwicklungvon Cariamacristata. J. Ornithol. 72:119- 124. J•I•I•S, R. 1977. Bird soundsand their meaning.British BroadcastingCorporation, Lon- don. Vol.57, No. 4 Biologyand Song of the Red-legged Seriema [269

MARTEN,K., ANDP. MARLER. 1977. Soundtransmission and its significancefor animal vocalization.I. Temperate habitats.Behav. Ecol. Sociobiol.2:271-290. , D. (•UINE,AND P. MARLER. 1977. Soundtransmission and its significancefor animal vocalization.II. Tropical foresthabitats. Behav. Ecol. Sociobiol.2:291-302. MIRANDA-RIBEIRO,A. DE. 1938. A seriema. Rev. Museu Paulista 23:39-90. MORTON,E. S. 1975. Ecologicalsources of selectionon avian sounds.Am. Nat. 109: 17-34. PETTINGILL,O.S. 1970. Ornithology. Burgess,Minneapolis. REDFORD,K. H., 1984. The termitaria of Cornitermescumulans (Isoptera, Termitidae) and their role in determininga potentialkeystone species. Biotropica 16:112-119. 1985. Emas National Park and the plight of the Brazilian cerrados.Oryx 19: 218-214. SANTOS,E. 1979. Da Ema ao Beija-flor. Itatiaia, Belo Horizonte. SCHNEIDER,K. g. 1957. Uber gegliederterufweisen bei Tieten. Beitr. Vogelk. 5:168- 183. SETH-SMITH, D. 1912. Proc. Zool. Soc. London 1912:557-558. SICK,H. 1984. OrnitologiaBrasileira. Editora Universidadede Brasilia, Brasilia D.F. THORPE,W.H. 1964. Singing.Pp. 739-750, in A. L. Thompson,ed. A new dictionary of birds. Nelson and Sons, London. WILEY, g. H., AND D. G. RICHARDS.1978. Physicalconstraints on acousticcommuni- cationin the atmosphere:implications for the evolutionof animal vocalizations.Behav. Ecol. Sociobiol. 3:69-94. Centerfor Latin AmericanStudies, Grinter Hall, Universityof Florida, Gainesville,Florida 32611 USA (KHR), and ZoologischesForschungsin- stitutund MuseumAlexander Koenig, D-5300 Bonn 1, Adenauerallee150- 16d,West Germany (GP). Received27 Dec. 1985; accepted27 May 1986.

NOTES AND NEWS

Recipientsof the E. Alexander Bergstrom Memorial ResearchAwards for 1986 are: CRAIG BERMAN, UNIVERSITYOP DEL^W^RE,Tactics of intraspccificbrood parasitism in the House Sparrow Passerdomesticus, $150. C. RAY CHANDLER, BOWLINOGREEN ST^TE UN•VER$•Y¾,Individual variation in foraging behaviorof Black-cappedChickadees Parus atricapillus, $250. JENNIFER CLARKE, W^SHINOTONST^TE UNIVERSITY, White-tailed Ptarmigan in the Sierra Nevada Mountains: a comparativestudy of an introducedpopulation, $200. CHERI L. GRATTO, UNIVERSITYOP NORTH D^KOT^, Endocrinologicalanalysis of sandpipersocial systems, $200. CAROLA HAAS, CORNELLUNIVERSITY, Site fidelity and dispersalof birds in a patchy environment, $150. PAUL HENDRICKS, W^SHINGTONST^TE UNiVERSiTY, Evolution of monogamyin Aleu- tian Rosy Finches Leucostictearctoa griseonucha, $200. GEOFFREY HILL, UNIVeRSiTYOF NEW MEXICO, The reproductiveconsequences of subadult plumage in male Black-headedGrosbeaks, $200. NANCY LEDERER, BOULDER,COLOR^DO, Nesting statusof Golden Eaglesin the northern Front Range of Colorado, $250. PAUL MAYER, UNIWRSIT¾oF MISSOURI-COLUMBIA,Population ecology of the Piping Plover in the Northern Great Plains, $200. MARA McDONALD, S^V^NN^HRIVER ECOLOGYL^B, The evolutionand biologyof Hispaniolan Palm Tanagcrs, genusPhaenicophilus, $200. DAVID MORIMOTO, BOSTONUNIVERSITY, Avian community structure in the pine barrens of southeasternMassachusetts, $100. TERRY PLANTIER, FLORID^ATLANTIC UNIVERSITY, A studyof possibleadvantages of early and later nestingin SootyTerns ($ternafuscata), $200. JORGE SALIVA, RUTGERSUNiVERSiTY, Behavior of SootyTerns nestingunder varying vcgctativccover and vegetationtypes, $200.