the breeding biology of the biscutate swift … · – the breeding biology of the biscutate swift...

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ORNITOLOGIA NEOTROPICAL 13: 61–84, 2002© The Neotropical Ornithological Society

THE BREEDING BIOLOGY OF THE BISCUTATE SWIFT (STREPTOPROCNE BISCUTATA) IN SOUTHERN BRAZIL

Mauro Pichorim

Curso de Pós–Graduação em Zoologia, Univ. Federal do Paraná, Cx. P. 19020, Curitiba, PR, Brazil, 81531-990. E-mail: [email protected].

Resumo. – A biologia reprodutiva do Andorinhão-de-coleira-falha (Streptoprocne biscutata) nosul do Brasil. – A biologia reprodutiva do Andorinhão-de-coleira-falha (Streptoprocne biscutata) foi estudadaem uma gruta situada no Estado do Paraná, sul do Brasil. O trabalho de campo consistiu no monitora-mento dos ninhos, ovos, e filhotes a cada 2 dias durante o período reprodutivo e na marcação das avesadultas com anilhas e marcadores fosforescentes. A construção dos ninhos inicia em outubro, sendo acoleta do material nidular feita com o bico. Os sítios de nidificação são substratos rochosos horizontais ouligeiramente inclinados em paredes verticais ou fendas. O material nidular é composto principalmente porlíquenes, briófitas, pteridófitas, angiospermas e terra. Vistos de cima os ninhos podem ser circular, elip-sóide, ou semicircular. A postura ocorre no começo de novembro, sendo o tamanho da postura de 1–4ovos. O ritmo de ovoposição e o comportamento associado revelam a existência de um padrão de posturae de competição por ninhos. Os ovos são brancos com formas sub-elíptica alongada ou sub-elíptica. Aincubação durou 24 dias em média e em pelo menos um ninho foi realizada pelo casal. A substituição doindivíduo que incuba foi realizada por um comportamento padrão. O período como ninhego é de 33 diasaproximadamente e após deixarem os ninhos eles ficam dentro da gruta por mais 10 dias. Ao nascer osfilhotes são nus e cegos. A primeira plumagem consiste de penugens cinzas a qual alcança o completodesenvolvimento ao 13° dia. Com a idade de 34 dias o filhote tem a plumagem definitiva completa. Oestudo do crescimento mostrou que as medidas lineares foram a asa e a cauda. Por fim, a reprodução doAndorinhão-de-coleira-falha mostrou-se semelhante ao padrão já descrito na literatura para outras espéciesdo gênero, mas aparentemente possui períodos mais curtos de incubação e de permanência no ninho.

Abstract. – The breeding biology of the Biscutate Swift (Streptoprocne biscutata) was studied in a cavelocated in the Paraná State, southern Brazil. Besides monitoring of the nests, eggs, and nestlings every 2days, the field works involved banding of adult birds with metallic bands and phosphorescent markers.Nest building begins in October; the nest material is collected with the bill. Nest sites are horizontal orslightly inclined rocky substrata on otherwise vertical walls or crevices. Nest materials are mainly lichens,bryophytes, pteridophytes, angiosperms, and soil. Nests are circular, ellipsoid, or semicircular in shape.Laying takes place at the beginning of November, with a clutch sizes of 1–4 eggs. The laying rhythm andthe behavior associated with it revealed the existence of a laying pattern and competition for nests. Thewhite eggs are long subelliptical or subelliptical in shapes. Incubation lasted 24 days on the average and, inat least one nest, was shared by both parents. The exchange of the incubating bird was accompanied by astandardized behavior. The nestling period was about 33 days and, after leaving the nests, the fledglingsstay in the cave for about 10 days. At hatching, the nestlings are naked and blind. The first feather coatconsists of gray semiplumes and reaches its full development on the 13th day. At the age of 34 days, thenestlings have their full definitive teleoptile plumage. The study of chick growth showed that the linearmeasurements were the wing and tail. Finally, the reproduction pattern of Biscutate Swift is similar to thatalready described in the literature for other species of the genus, but apparently with shorter periods ofincubation and permanence in the nest. Accepted 1 May 2001.

Key words: Biscutate Swift, Streptoprocne biscutata, Apodidae, Aves, breeding biology, Paraná State, Brazil.

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PICHORIM

INTRODUCTION

The Apodidae are widely distributed withspecies on almost all continents (Collins1985). The family is mainly tropical and con-sists of about 92 species, of which about 23occur in South America (Chantler & Dries-sens 1995).

Elements of the reproductive biology ofthe Apodidae, such as nest types, breedingplaces and clutch size have been used as char-acters for generic and subfamily levels (Lack1956, Orr 1963, Brooke 1970, Marín & Stiles1992, Collins 2000). Extensive studies of theirbreeding biology have been conducted forAsian, European and North American species(Koskimies 1950, Lack & Lack 1951, Fischer1958). In South America, in spite of the largenumber of species including some endemicones, there are only few published studies(Sick 1947, 1948a, 1948b, 1948c, 1950, 1958,1959; Haverschmidt 1958, Collins 1968a,1968b), all dealing with small species.

The Biscutate Swift (Streptoprocne biscutata)occurs in eastern Brazil from the state ofPiauí south to Rio Grande do Sul, extendingto northeastern Argentina in the province ofMissiones (Meyer de Schauensee 1982, Nores& Yzurieta 1985, Chantler & Driessens 1995,Sick 1997). Published data on the biology ofthe species are limited to sparse comments onthe few known colonies. There is a colony ofabout 80,000 birds in the region of Seridó inthe state of Rio Grande do Norte (Sick 1997).This species inhabits also the Serra do Ibiti-poca in the southern part of Minas GeraisState (Andrade et al. 1985, Andrade & Freitas1987) where notes on the breeding biology ofthe species were taken for the first time(Andrade et al. 1985).

In southern Brazil, the studies are veryscarce and limited. In northeastern of RioGrande do Sul, in the region of the Aparadosda Serra National Park, the observation ofmixed flocks of Biscutate Swift and White-

collared Swift (Streptoprocne zonaris) was noted(Belton 1994). In Santa Catarina, the specieswas recorded in the Mun. of Urubici andnearby regions (Sick & Bege 1984, Rosário1996). For Paraná State, there was only onerecord of the species in the Mun. of Castro,dated 1907 (Pinto 1938). However, since1992, the species has been recorded in severalplaces (Pichorim & M. R. Bornschein unpubl.data), and the colony that is described in thisstudy was discovered. Based on the recentdiscovery of the Biscutate Swift in Paraná,this study was carried out with the objectiveof describing for the first time the breedingbiology of the species.

STUDY AREA AND METHODS

The study was carried out between 1994 and1996 at Anhangava Hill, in the Serra daBaitaca. It is situated in the Mun. of QuatroBarras, State of Paraná, Brazil (25°22’S,48°58’W). This region is part of the Serra doMar, which consists of a large series of hillsalong the Brazilian coast. At the top ofAnhangava, at 1420 m a.s.l., occur ecologicalrefuges and dense ombrophilous high-altitudeforest (following the classification ofFundação Instituto Brasileiro de Geografia eEstatística–IBGE 1992). At the base of thehill, the dense ombrophilous montane forestoccurs between ombrophilous forest withAraucaria angustifolia. Above 1000 m, the areaincludes exposed granite rocks, which prevailin the local landscape at altitudes above 1200m.

The overnight roosting and breeding sitestudied here was a cave of granite formed by acrevice of 120 m in length in the northernmountain face, at 1250 m a.s.l. Its width andheight are highly variable (0.5–4.5 m and 4–15m respectively), and so is the luminosity, theinnermost portion being completely dark.The floor consists of chaotically piled rockyblocks with a deep guano accumulation that

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BREEING BIOLOGY OF STREPTOPROCNE BISCUTATA

decreases in amount toward the innermostportion of the cave. Popularly, this cave iscalled the “caverna das andorinhas” (swal-lows’ cave).

Biscutate Swifts inhabit this site duringthe whole year. However, the population sizeis not constant, having a maximum of about260 individuals in spring (September–December) and a minimum of 150 in winter(June–August).

The regional weather type is cfb of theKöppen classification system, characterizedby a warm and rainy summer and a cold win-ter with casual dry periods (Maack 1981). Theregion has a high rainfall index (about 2000mm per month), a high relative humidity (theannual average is 90%), and is very cloudy(Roderjan 1994).

In order to identify individual birds dur-ing the reproductive period, an attempt wasmade to band the largest possible number ofindividuals in the colony during fourteen3-day visits from March 1994 to December1995. The birds were captured with a circularnet similar to a butterfly net, but with a sup-porting ring of 2 m in diameter. The ring wasmade of flexible fiber glass rods (as used intents for camping) and supported by a 4 mlong tubular aluminum handle.

The basic procedure to capture adultbirds consisted of awaiting their departurefrom the cave in the morning, near the fre-quently used exit. When the birds started toleave the cave, the net was quickly raised intothe flock, capturing between 5 and 15 indi-viduals each time. This procedure wasrepeated only three times in one day in ordernot to stress the birds excessively.

Metallic numbered bands of size “ J ”(inner diameter of 4.5 mm) were used. Thebands were supplied by CEMAVE/IBAMA(Centro de Pesquisas para Conservação dasAves Silvestres/Instituto Brasileiro do MeioAmbiente e dos Recursos Naturais Ren-ováveis).

Reproduction took place from Octoberto the middle of January in each of the threestudy years. At the beginning of this period,during each one of the study years, one visitper week was made to the cave with the pur-pose of finding the first signs of breedingactivities. During these visits, a systematic andmeticulous search for nests was made, cover-ing about 70% of the whole internal area ofthe cave. When the first signs of nest buildingwere detected, the frequency of visits wasincreased to two days per week.

The study of parental care were made onone pair of birds by a special marking devel-oped for observation under aphotic condi-tion. Plasticized disks of fine cardboard, 15mm in diameter, were painted on both sideswith phosphorescent ink. A black letter (“A”and “B”) was printed on each of them. Twoof these disks were used, with the same letter,for each one of the mates that made up thepair. The disks were glued on the coverts ofboth wings with instantaneous glue (“superbonder”) while care was taken to not let it getin contact with the skin. These birds could beidentified from a distance when they arrivedat the nest, since the phosphorescent ink con-tinued to irradiate the light that had beenabsorbed outside the cave for about 10 min,thus making the letter code visible. Throughthis method, it was possible to quantify thetimes of incubation for each adult bird.

A tent made of black cloth was used tohide the observer’s presence inside the cave.The incubation activities of the marked pairwere observed during six days. The observa-tions in each day have started between 06:00and 10:00 h and finished between 15:00 and19:00 h (Eastern Standard Time). Thesebegan in the second day after marking the“B” individual.

The measurements taken for each nestwere: the largest and smallest external width,the width of the nest cup, the external heightand the depth of the nest cup in relation to

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PICHORIM

the highest border. To calculate the averagefor the measurement for all nests, only thehighest value obtained in each reproductiveseason was used, because variations occurredin the nest dimensions during the breedingseason. The eggs were marked by a pencil,weighed and measured (width and length)during the visit in which each one was foundfor the first time (0 to 2 days after havingbeen laid). The nestlings received plasticbands that were replaced by metallic oneswhen the birds were at a minimum age of 14–16 days. The following measurements weretaken on each visit to the nest after hatching:mass, wing (flattened), tail, tarsus andexposed culmen. In addition, the develop-ment of the plumage and behavior were alsodescribed. The eggs shape description followsBaicich & Harrison (1997).

The measurements of the nestlings andeggs and the dimensions of the nests weretaken with calipers to 0.05 mm and a metallicrule to 0.5 mm. The masses, including thoseof the adult birds, were obtained with pesolaspring balances (50 g, 100 g and 300 g). Spele-ology equipment like carabiners, harness,tapes and electric head lanterns were used forthe activities conducted inside the cave. Toreach the nests, 25 steel pitons 15 cm inlength and 12 mm in diameter were placed

close to them. Nylon ropes (12 mm thick)were fixed to them. The ropes were not sus-pended in the air but lay flat against the rockwalls, so that they did not interfere with birdflights inside the cave. These ropes facilitateda fast and safe access to the nests and did notappear to interfere in the reproductive activi-ties of the birds.

RESULTS AND DISCUSSION

Nests. From August to October 1994, 21 nestswere found, all having been built in areas thatpossessed an accumulation of nest material ofthe former breeding season. This implies thatthese places had already been used previously.In the next year, 21 nests were found, ofwhich 19 were built in the same places used inthe previous year. In 1996, 16 nest werefound and their construction was again in thesame areas used in the previous years. Thus,during these three years, 25 preferential placesfor nest construction were observed, whichyielded 58 completed nests. These preferredareas are herein considered as “nest site” (Fig.1).

The nest sites were characterized by a hor-izontal or slightly tilted rocky substratumlocated inside the cave at a height of 3–8 m.These places were quite inaccessible and con-

FIG. 1. Schematic drawing of the studied cave with the nest sites. The letters A, B and C indicate the threeentrances used by the birds. Adapted from drawing made by Darci P. Zakrzewski.

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sisted mainly of plateaus in vertical walls orcrevices. A brief description of each nest siteis given in Table 1. There were no perennialwatercourses near any of the nest sites. Thisdiffers of what has earlier been reported forWhite-collared Swift, a species that seems toprefer humid areas (Marín & Stiles 1992, Sick1997). However, some nests were located

very close to temporary water streams thatappeared only during intense rains, and whichflooded all nest material and sprinkled theeggs and nestlings. After the breeding season,at such places, the remaining nest materialswere totally removed by the action of thewater along the year. In spite of this, in thenext breeding season, the nests were rebuilt

TABLE 1. Characteristics of the nest sites of Biscutate Swifts at the Anhangava Hill, southern Brazil.

Sites Type1 Measurements2 Nest distance Usage3

from the exit (m) 1994 1995 1996S1S2S3S4S5S6S7S8S9S10S11S12S13S14S15S16S17S18S19S20S22S23S24S25

AAAACAABBBCCCCCCCCCCCCBD

58 cm/1000 cm2 40 cm/1200 cm2

20 cm/390 cm2

27 cm/1500 cm2

25 cm/1.3 m40 cm/1400 cm2

15 cm/720 cm2

650 cm2

*650 cm2

17 cm/4 m50 cm/7 m20 cm/4 m

27 cm/90 cm20 cm/20 cm9 cm/70 cm28 cm/1.4 m

*****

450 cm2

12 cm/18 cm

8.5242423

23.41.78.57.419.415.425

39.417.722131315

15.42.94.54.54.521.71.4

++++++++-++++++++++-??++

++++-+++++-+++-+++++++++

+-+--+++-+--++--++++++-+

1The nest sites were classified in four types: A = stone arrested in vertical crevice, B = plateau in verticalwall, C = interior of vertical crevice, and D: interior of horizontal crevice.

2The measures were obtained at the spot used for the nest construction. Asterisks indicate nest sites wheremeasuring was impossible. A sequence of presentation of the values was adopted for each site type, as fol-lows: type A - width of the crevice in the used place and approximate area of the upper side of the stonewhere the nest was situated, type B - approximate area of the plateau, and types C and D - width of thecrevice in the used place and depth until the nest.

3The sites were considered in use when any sign of nest construction was detected, even if laying had notyet begun.

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PICHORIM

at the same specific site.The use of the same sites for reproduc-

tion in successive years entailed only in arelining of the old nests, and not in a totalreconstruction of them, except in cases whereall old material had been washed away. Thenew nest material was added first in the wornborders of the old nest cup. This was clearlyvisible as the old material always was dry andcompacted, contrasting with the greenish anddamp fresh material. In the nests on inclinedsurfaces, the birds initially compensated byadding more new nest material to the lowestborder, and built the remainder of the nestlater. Starting at these points of repair, all oldnest material was progressively covered by alayer of fresh material. The renovating of thefirst nests began at the beginning of October(2 October 1995 was the earliest verifieddate). However, some nests began to berenewed only at the end of that month (29October 1994). The addition of material isnot limited to the pre laying period; the adultscontinue to renew the nests at a seeminglylower intensity during incubation and in theinitial phase of development of the nestlings.This behavior causes alterations in the nest

dimensions during each single breeding sea-son (Table 2).

Many species similarly utilize nests fromthe former reproductive season, or recon-struct them on the exact same site, e.g.,White-collared Swift, White-naped Swift(Streptoprocne semicollaris), White-chinned Swift(Cypseloides cryptus), Chestnut-collared Swift(Streptoprocne rutila), Spot-fronted Swift (Cypse-loides cherriei), Gray-rumped Swift (Chaeturacinereiventris), Chimney Swift (Chaetura pelagica)and Ashy-tailed Swift (Chaetura andrei) (Dexter1952, Sick 1959, Snow 1962, Collins 1968b,Whitacre 1989, Marín & Stiles 1992). Afterstudying the breeding of Biscutate Swift inthe southern part of Minas Gerais State,Andrade et al. (1985) commented that thesame individuals come back to the same cavesin each reproductive period. However, it isnot clear if the old nests were used again ornot. The fidelity to nest sites seems to berelated to the reproductive success that a cer-tain place offers. In this study, it was observedthat where eggs or nestlings were depredatedthe nest sites were not utilized again in thefollowing year (see “Eggs”).

The collection and transport of nest mate-

TABLE 2. Dimensions (cm) of Biscutate Swift nests at three nest sites in the same reproductive season, atthe Anhangava Hill, southern Brazil.

Sites Date Smallest external diameter

Largest external diameter

Smallest internal diameter

Largest internal diameter

Smallest external height

Largest external height

Depth

S 1S 1S 1S 10S 10S 10S 17S 17S 17

29 October 199416 November 1994

18 January 199529 October 1994

16 November 199418 January 199529 October 1994

16 November 199418 January 1995

1415-1

171717

11.512.511.5

16.517-

222120

19.519.513.5

7.58-

1010107.57.57

89.5-

1011108.59.58.8

11.5-233111

5.57-3

4.54

10.597

33.5-

3.53

2.5332

1The dash means total loss of the nest configuration, the measure being impossible to be obtained.

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rial was consistently observed to be gatheredin the bill and taken from rocky walls or fromthe nearby soil, as already described for theWhite-collared Swift (Whitacre 1989, Marín& Stiles 1992). Medway (1962), proposed forswiftlets (Collocalia) that species that transportnest material with the bill have little capacityof echolocation, since species that really usethis navigation mechanism transport nestmaterial with the feet, leaving the bill free forthe emission of sounds for orientation. If thishypothesis is correct for others swifts, theobserved behavior of Biscutate Swifts with

regard to the mode of nest material transportshould indicate that this species has little orno capacity of echolocation. However, thissubject requires more detailed investigation.

During the nest building period, frag-ments of mosses and lichens are abundant onthe cave floor, particularly below the wallscovered by such plants. Four swifts wereobserved collecting this material, and in onecase a bird pulled pieces of incrusting bryo-phytes from a vertical wall and seeminglychewed them soon afterwards. Perhaps thisrepresents a form of adding some saliva to

TABLE 3. Dimensions (cm) of Biscutate Swift nests found in 1994 and 1995 at the Anhangava Hill, south-ern Brazil1.

Smallest external diameter

Largest external diameter

Smallest internal diameter

Largest internal diameter

Smallest external height

Largest external height

Depth

RangeMeanSD

8.0-18.514.22.88

13-2317.912.39

5-107.891.29

6-108.641.16

0.5-3.51.980.93

2.5-10 5.412.52

1-4.52.790.71

FIG. 2. Drawings of the three basic nest types of Biscutate Swift found between 1994 and 1996 at theAnhangava Hill, southern Brazil. A = semicircular, B = circular, and C = ellipsoid.

1Only the largest measurement in each reproductive season was considered, as alterations did occur duringthe period as a whole. The sample consists of 23 nests.

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PICHORIM

TABLE 4. Nest material found in 23 nests of the Biscutate Swift at the Anhangava Hill, southern Brazil,between 1994 and 1996.

Nest material Number of nests where the item was found1

Lichens fragmentsCoccocarpia sp. (Coccocarpiaceae) Ramalina camptospora (Ramalinaceae)Usnea sp. (Usneaceae) Cladia aggregata (Cladiaceae) Cladonia sp. (Cladoniaceae)Relicina abstrusa (Parmeliaceae)Parmotrema wainii (Parmeliaceae)Rimelia cetrata (Parmeliaceae)Parmotrema delicatulum (Parmeliaceae)Hypotrachyna peruviana (Parmeliaceae) Parmelinopsis sp. (Parmeliaceae) Unidentified Parmeliaceae

Bryophyta fragmentsPlagiochila sp. (Plagiochilaceae) Plagiochila rutilans (Plagiochilaceae)Frullania brasiliensis (Frullaniaceae) Leucoloma sp. (Dicranaceae) Campylopus sp. (Dicranaceae)Campylopus aemulans (Dicranaceae)Herberta sp. (Herbertaceae) Polytrichum juniperinum (Polytrichaceae) Leucobryum crispum (Leucobryaceae) Phyllogonium viride (Phyllogoniaceae)Syrrhopodon prolifer (Calymperaceae)Syrrhopodon prolifer (Calymperaceae)Lejeunea flava (Lejeuneaceae) Omphalanthus filiforme (Lejeuneaceae) Porotrichum longirostre (Neckeraceae) Rhacocarpus sp. (Hedwigiaceae)Schlotheimia tecta (Orthotrichaceae) Macromitrium punctatum (Orthotrichaceae)Schlotheimia rugifolia (Orthotrichaceae)Sematophyllum caespitosum (Sematophyllaceae) Squamidium leucotrichum (Meteoriaceae) Zelometeorium recurvifolium (Meteoriaceae)

Pteridophyta fragmentsRumobra adiantiformis (Dryopteridaceae) leaf fragment Micrograma sp. (Polypodiaceae) fragment or entire leafCampyloneurum sp. (Polypodiaceae) entire plantHymnophyllum polyanthos (Hymenophyllaceae) root and entire leaf Cochlidium punctatum (Grammitidaceae) entire plant

112111231113

81144455612212126111112

55139

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the nest material, once some authors considersuch activity occurs to some extent in allmembers of the family (Sick 1947, Lack 1956,Snow 1962). However, in Cypseloidinae, thesize of salivary glands is greatly reduced andthe production of saliva is lower (Johnston1961). For Biscutate Swifts, nothing has sofar been published on this matter, but insome nests I observed the presence of a vis-cous substance in the moss fragmentsrecently added to nests. However, when thenest is dry it does not reveal the existence ofany agglutinative substance. Perhaps theeffectiveness of the saliva is not as importantfor this species as it is for many others,because its nest is just a simple constructionon a horizontal substratum.

The nests when seen from above werecircular, ellipsoid and semicircular in shape(Fig. 2). These variations seem to be relatedto differences in the available space at thechosen nest site. When the space alongsidewas narrow, the form was ellipsoid; when theavailable space was plentiful, the nest was cir-cular, and in cases where the nests were com-pressed against a vertical wall, they becamesemicircular. In lateral view, the base wasalways wider than the upper part, makingthem shaped like a crater. At uneven placesthe lowest margin of a nest always included alarger accumulation of material than on theopposite side, resulting in different externalheights at opposite sides of the nest. A com-pensation for similar unevenness was already

TABLE 4. Continued.

Nest material Number of nests where the item was found1

LiliopsidaTillandsia sp. (Bromeliaceae) entirely or slightly fragmented plantOrchidaceae, entire or fragmented leafBambusoidae (Poaceae) entire or fragmented leafPoaceae, entire or fragmented leafLiliaceae, leaf

MagnoliophytaTibouchina sp. (Melastomataceae), fragmented leafCroton sp. (Euphorbiaceae), entire or fragmented leafPeperomia sp. (Piperaceae), whole leafRapanea sp. (Myrsinaceae), leafMimosaceae, leaf rachisMyrtaceae, leafBignoniaceae, leafLeaf fragments, little twigs, barks and unidentified roots

ByproductsBiscutate Swift's remiges and rectricesBiscutate Swift's guano (elytra and membranous insect wings)Sand (quartz grains of 0.5-1.5 mm in diameter)Soil (a mixture of earth, small sand particles and guano)

Synthetic materialSynthetic blue thread of 10 cm length

429112

7112191117

7171723

1

1Only the presence and absence was considered and not the used amount.

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PICHORIM

observed in the Waterfall Swift (Hydrochousgigas) (Becking 1971). Inside the nest, an incu-bating chamber always exists which consistsof a circular or ellipsoid depression. In gen-eral, the aspect of the nest of Biscutate Swiftwas similar to that described for the White-collared Swift (Whitacre 1989, Marín & Stiles1992). Table 3 indicates the variation indimensions of 23 monitored nests.

The nests were principally composed of acompact mass of lichens, bryophytes andsmall roots (Table 4). Elytra and membranouswings of insects were also found mixed withthe nest material and were probably derivedfrom the birds’ feces. The presence of fecalremnants in the nests does not mean that thismaterial is an important component for nestconstruction. These insect remains, thoughfrequently encountered, were not abundant.Thus, defecation in the nest during nest con-struction should not be considered indispens-able for the achievement of its final structure.

Soil and sand were also found in the nests,but I never observed a deliberate depositionof these materials. They probably arrivedstuck to the plant material. Besides, the nests

located at specific sites that were totallywashed by the infiltrating water always con-tained little soil and they were composedmainly of plant parts. Thus, only the neststhat maintained their original structurethroughout the year possessed plenty of soil,which was probably brought in attached tovegetative material during successive nest ren-ovations.

The incubation chambers of the nestswere covered with leaves and thin twigs ofangiosperms and feathers of Biscutate Swift(Table 4). These feathers probably did notbelong to the birds that built the nests, as theyconsisted of molted remiges and rectrices,and the molt period occurs after incubation(pers. observ.). They probably representfeathers of previous molt periods, and rem-iges and rectrices from previous molts couldbe found easily inside the nesting cave. Apartfrom the natural materials mentioned above,one nest contained a piece of synthetic bluethread 10 cm in length. This thread probablyoriginated from climbers’ rope material, asthe area is in use for trekking and rock climb-ing activities.

FIG. 3. Typical shapes of Biscutate Swift eggs observed at the Anhangava Hill, southern Brazil.

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Eggs. There was only one clutch laid per nestper reproductive season in each of the studyyears (1994, 1995 and 1996). The eggs of allbirds of the colony were laid synchronously,in a very restricted time, between 1 and 9November. After this period, no additionalegg laying was observed. Thus, the last weekof October and the first week of Novemberwas the most critical period for the reproduc-tive success of the colony.

Fresh eggs had a smooth, opaque andunmarked white shell. Sometimes later duringthe incubation period eggs were found dirtyfrom soil in the nests. The egg shape waslong subelliptical or subelliptical (Fig. 3).They had a length of 33.9–39.7 mm (mean =37.2 mm, SD = 1.5, n = 49), width of 22.3–25.8 mm (mean = 24.2 mm, SD = 0.7, n =49) and a mass of 10–14.3 g (mean = 11.6 g,SD = 0.9, n = 48). The observed eggs werevery similar to those of White-naped Swiftand White-collared Swift in nearly all charac-teristics (Rowley & Orr 1962, De La Penha1982, Marín & Stiles 1992), except for theratio between their mass and the adult birdmass in the breeding season (mean = 119.4 g,SD = 9.0, n = 85), which was equal to 9.7%.This is a slightly lower value than the oneobtained by Marín & Stiles (1992) for White-collared Swift (10.2%). This difference existsin spite of the average mass of the BiscutateSwift eggs being larger than that of White-

collared Swift.The clutch size varied from one to four

eggs, the modal value being two (Table 5). Inthe nests that received up to two eggs, itappeared that one egg was laid per day. Insome cases, nests that contained three or foureggs were observed to receive up to two eggsin a single day. This is probable consequenceof intraspecific brood-parasitism, where asame nest is used by more than a singlefemale. In other swifts (not belonging to thegenus Streptoprocne), collective clutches havebeen described, including some cases wherethe birds also divided the incubation task(Lack & Lack 1951, Dexter 1952, Sick 1959,Snow 1962). In White-collared Swift andWhite-naped Swift only clutch sizes of one ortwo eggs have been reported (Rowley & Orr1962, De La Penha 1982, Marín & Stiles1992); in Biscutate Swift, previous recordswere of two or three eggs (Andrade et al.1985), which was questioned by Marín &Stiles (1992).

The pattern of egg laying in BiscutateSwift demonstrated the existence of a confus-ing and complex behavior. In the beginningof November of each study year, many egg-shells were found on the cave floor. With cer-tainty they were not eggshells of recentlyhatched chicks, as in this period the adultbirds had only started egg laying and incuba-tion. These eggshells were initially consideredas resulting from the predation of recentlylaid eggs. However, not only were smallpieces of eggshells found, but also entireshells, both found at the same place. In somecases, the internal content of the eggs, yolkand albumen, could be seen. This fact indi-cated that these eggs had not been eaten.Nevertheless, the possibility remained thatsome predator had rolled the eggs out of thenest while trying to eat them, or that the eggswere accidentally ejected from the nest by thebreeding adult birds. Doubts remained as thebroken eggs were found below areas used

TABE 5. Biscutate Swift clutch sizes encounteredbetween 1994 and 1996 at the Anhangava Hill,southern Brazil.

Clutch size Amount of clutches found1234

9215*1*

Mean = 1.94 egg/nest, SD = 0.71

*Probably the result of layings by multiple females,see text.

72

PICHORIM

only for roosting and which did not haveappropriate sites to support nests.

In order to clarify this, in 1996 a tulle netwas suspended about 1 m above the floor ofthe nest cave in an area above which no nestswere located. This net would catch any fallingeggs. Eggs falling from nearby nests would bebroken on the rocks below with only piecesof shell possibly reaching the net. Thus, onlyeggs dropped or laid by birds perching on therock surface exactly above the net wouldarrive intact in it.

After five days in position, the net con-tained two intact eggs. They were not dam-aged, in spite of haven fallen about 6 m. It islikely that the majority of eggs found brokenon the floor of the cave in the beginning ofthe oviposition period each year had not pro-ceeded from predation or from accidentalsejections. This seems more likely the conse-quence of a peculiar behavior of this speciesthat can be explained by two hypotheses,described below.

The first interpretation would be thatbrood parasitism or dispute for nests occursin this species. Parasitizing females removethe eggs in a nest to lay their own eggs in it. Ifthis is the case, the presence of the intact eggsobserved in the tulle net can be explained bythe fact that the intruding female had seizedthe eggs in the host nest, carried them to aroosting site and there dropped them. In thiscase, each egg would have been transportedindividually in the bill (it is impossible for abird to carry more than a single egg inside themouth). In another five nests, a kind ofbehavior was observed that can be interpretedalso as either brood-parasitism or as competi-tion for nesting space. In these cases, the eggswere not carried far away from the hosts’nests. At the beginning of the laying period,one egg was found in these nests; the egg wasmarked with a pencil. After two days, duringthe next inspection, these eggs were foundintact but they were outside the nest cup, but

near the nests on the nearby nest ledge. In thenest cup of each nest was a new egg, whichalso received a pencil mark. The expelled eggwas put back in each nest but two days later itwas out of the nest again, and a second newegg was in the nest. In two nests, there was athird egg. The first eggs were put back againand during the next inspections some had dis-appeared while others had not been expelledand were being normally incubated. Theseobservations suggest that the firsts laid eggswere deliberately expelled from the nests, as itis hard to believe that the observed ejectionscould have happened accidentally and repeat-edly. Koskimies (1950) observed the expul-sion of eggs from nests of the Common Swift(Apus apus) and he attributed this behaviormainly to climatic changes, or due to a mecha-nism of the species to control the number ofnestlings to be fed.

This first hypothesis (brood-parasitism ordispute for nest site) would explain the bro-ken eggs found on the cave floor, as well asthose two eggs captured by the tulle net.However, it would mean that on some occa-sions the eggs were transported a large dis-tance from the parasitized nest and in othercases, they were just pushed outside the nestcup. This hypothesis does not explain the rea-sons of occurrence of two different behav-iors, as both lead to the same function. Whyin some occasions would the parasite birdscarry the eggs away to a rocky wall roost siteto release them and, in other occasions, sim-ply expel the eggs outside the parasitizednests? In addition, if the transport of eggs to along distance from the nests was really hap-pening the total eggs that disappeared duringthe laying period should be high. Neverthe-less, this was not the case. The number ofeggs that disappeared was low, as each eggrecently found in a nest received a pencilmark on the day of its discovery, and it wasobserved individually during the followinginspection. Few disappearances of eggs hap-

73


pened after the laying period when severalbroken eggs had been detected on the cavefloor. That is to say, a large number of bro-ken eggs were found in the beginning of thelaying period and the few disappearances ofeggs occurred later, during incubation.

From the observations made in the fivenests mentioned above, it must be concludedthat brood-parasitism and/or competitionfor nests were occurring. This behavior couldresult in apparent clutch sizes of three to foureggs, but at these nests more than one femaleis laying. The only observed clutch size offour eggs occurred under a peculiar circum-stance; three eggs were inside the nest cupand the last one was on the nest material ofthe nest’s side. The frequency of laying inthese nests with enlarged clutches indicatesthat the laying was probably done by morethan one female, since in some situationsthese nests received up to two eggs in oneday. A laying rate of one egg per day was typi-cal of other observed nests.

The second hypothesis that could explainthe recover of eggs in the tulle net and othersfound broken on the cave floor would be thatsome females could be laying directly on thevertical rock walls. As mentioned, brokeneggs were found under areas used only asroosts, and from these places the femaleswould drop their eggs directly on the ground.The situation that would lead to this behav-ioral pattern is unclear. An explanation couldbe the immaturity of females which wouldtend to waste their eggs owing to inexperi-ence. Another possibility could be that somefemales were not inseminated, due to a lowdensity or low fertility of males or due to adeficiency in the aerial copulation. In thesecases, the eggs would be infertile and thebirds would have the capacity to distinguishthis and to reject them by dropping them.This behavior has not been documented forother species. However, aerial copulation hasalready been considered disadvantageous or

unlikely for Cypseloidinae (Marín & Stiles1992, Marín 1999).

Another factor that could be related tothe appearance of broken eggs and with theexpulsion of eggs from the nests would be alow density of appropriate nest sites. Thiswould cause more than one pair to try tooccupy the same nest site during the samereproductive period. Females would competefor the same nest in which to lay their eggs,explaining the observed cases of expelledeggs. Those females that were not successfulin getting a nest site tend to let their eggs fallfreely on the cave floor. A competition fornest sites has been described for GlossySwiftlet (Collocalia esculenta) (Spenneman 1928fide Medway 1962) and Common Swift (Lack1956 fide Medway 1962). Nest site competi-tion has not been recorded until now for thegenus Streptoprocne.

Some authors have previously com-mented on the presence of broken eggs ofswifts close to nests. This was usually inter-preted as an accidental ejection, or caused byfighting birds (Lack & Lack 1951, Medway1962, Snow 1962). In another colony of Bis-cutate Swifts, the presence of broken eggsbelow nest sites has been noted, but noexplanation was proposed (Andrade etal.1985). Broken eggs of the White-napedSwift found upon the guano accumulation onthe floor of the cave has been also noted(Rowley & Orr 1962). Whitacre (1989) saidthat eggs being rolled out of the nests are theprincipal cause of reproductive failure inWhite-collared and White-naped swifts inMexico.

An experiment was conducted with thetwo eggs captured by the tulle net, in order todetermine their fertility. One of them wasplaced in a nest that contained another eggand then observed to see if it would hatch.After eight days of incubation, the foreignegg disappeared, probably having beenejected. In this case, the ejection might have

74

PICHORIM

happened for two reasons: infertility or rejec-tion due to a lack of recognition. The otheregg was put in an electric incubator at 39°C,with relative humidity controlled by the pres-ence of a wet sponge nearby; the position ofthe egg was changed every eight hours. After30 days, this egg had still not hatched and noembryo was found in it. Apparently both eggswere infertile. In Common Swift, the expul-sion of infertile eggs in the beginning of theperiod of oviposition had already beenreported (Koskimies 1950). However, it isalso possible that the eggs of the BiscutateSwift recovered by the tulle net did notdevelop due to internal damages resultingfrom the fall that they had suffered. Thus, inspite of the indications of infertility, theseresults should not be interpreted as conclu-sive.

If the dispute for space really exists, itwould explain the loss of eggs of females thatdoes not find places to lay. But when consid-ering the whole internal area of the studiedcave and taking in consideration only thedimensional characteristics of the nest sites,there appeared to be several unused placesthat were very similar to other commonlyused as nest sites. Also, it was observed thatsome nests, though having been built, did notreceive eggs. In 1994, nests were built at thesites S 21 and S 25, but there were no indica-tions of laying or of predation or any otherreason that would justify the disappearance ofthe eggs. The same occurred in 1995 in thesites S 1 and S 8. In spite of the nests spaceavailable, the broken eggs on the cave floorand the probable disputes for nests contin-ued. Perhaps, apart from the dimensionalaspects, there are also other factors importantin the choice of the place to built nests. Onepossibility could be the degree of access ofsites to predators.

In spite of predation mostly not beingdirectly related to the observed broken eggs,it sometimes happened and it could be

detected. In seven nests, eggs were foundwith a great opening at the side or at one pole;in some of these nests, totally broken eggswere found. In all these cases, no remains ofthe eggs’ internal content was found. Thebreeding pair could hardly have accidentallydamaged these eggs in this fashion and thesecases are probably due to predation. Apartfrom this, predation of the eggs and one adultbird were recorded in five nests. At the placeswhere this kind of predation happened, onlypieces of eggshells were found and somefeathers of the depredated birds, includingremiges and rectrices that had the calamusvisibly gnawed. In two cases, the metallicbands that had marked the birds were foundin the nests. In a depredated nest (S 12), a car-cass was found with its wing, back and tail stilltogether. This was identified as being a male,as the gonads were intact. In the places wherethis kind of predation took place, no foot-prints were found or any other type of sign toidentify the predator. The structure of thedepredated nests was not damaged andremained intact.

I have never observed or heard bats in thecave and there are no carnivorous bats regis-ters in the region, so I presumed the predatorwas a small terrestrial mammal. To capturethe possible predators, 15 live traps were setin several parts of the cave, all of them baitedwith bacon. Over 12 days the traps capturedone roof rat (Rattus rattus frugivorus) (Rodentia:Muridae), three grass mice (Akodon sp.)(Rodentia: Cricetidae) and five common grayfour-eyed opossums (Philander opossum) (Mar-supialia, Didelphidae). The rodents werecaptured in the traps placed in the entrance ofthe cave and the P. opossum were capturedinside the cave, in less accessible and darkerplaces. One of the opossums was capturedwithin 1 m of a nest that had been recentlydepredated.

To test its ability to depredate swifts eggs,a female P. opossum was maintained in captivity

75


for five days. It was given eggs of JapaneseQuail (Coturnix japonica), similar in mass andsize to Biscutate Swift eggs, and those ofDomestic Fowl (Gallus gallus). The opossummanaged to open only the eggs of JapaneseQuail, sipping the content without spilling.The shell of the offered eggs was broken atthe sides or at the poles, just as in depredatedeggs of Biscutate Swifts. Therefore, the pred-ator of the studied swift is probably the P.opossum, a species that is common in the studyarea and possesses a great abilities as a preda-tor. Research has already shown that thismarsupial can locate prey (at least frogs)acoustically in aphotic places (Tuttle et al.1981), and this might be happening in thecase of predation on Biscutate Swifts.

In the three years of the study, adult birdpredation occurred only during egg layingand incubation periods, perhaps due to thefact that a bird on the nest is more vulnerableto predation than when it is at a vertical over-night roosting perch. It is also probable thatthe birds avoid leaving their eggs when thepredator appears, which eases their capture.Finally, the broken eggs found on the cavefloor at the beginning of each reproductiveseason can be a stimulus to the predator toexplore the entire cave, which in turn mayresult in the discovery of adult birds and eggsin the nests.

The five nest sites that lost one of theadult birds by predation were not reused inthe following reproductive season. Amongstthe seven observed nest sites at which onlythe eggs were apparently depredated, justthree were reused in the following year. Theseobservations suggest a relationship amongstthe nest site and the history of predation ofthe chosen place. This could be one of themain factors that influences choice of an nestsite. The non reuse of sites where an adultbird was depredated could also be related to adissolution of the pair. This could be the caseif the species is monogamous and the pairsalways reuse the same place for breeding asalready have been shown in part for BlackSwift (Cypseloides niger) (Marín 1997). The indi-vidual that survives a predator’s attack butlooses its mate might abandon the site previ-ously used due to the absence of the mate.Some evidence was obtained that this canhappen. In the breeding season of 1995, abanded pair was captured while reconstruct-ing the nest in site S 17. In the followingmonths, the reproduction of this pair wasmonitored. In 1996, the same site was beingrenewed prior to laying, but one of the birdswas depredated during the first days of incu-bation. When the remains of this bird werefound, it was possible to recover its band,which turned out to belong to one of theindividuals that had used the same site in1995. This observation proves that at leastone of the birds was faithful to the same nestsite for two consecutive reproductive seasons.If that is the pattern for all pairs of the col-ony, this would not explain why new pairsdoes not occupy abandoned nest sites.

Incubation. Incubation began in the beginningof November, after the last egg of each nesthad been laid, and it finished near the end ofthe same month or in the first week ofDecember. The average duration of the incu-bation period was 24 days (SD = 1.7, n = 24;

TABLE 6. Biscutate Swift incubation periodsobserved in the reproductive seasons of 1994 and1995 at the Anhangava Hill, southern Brazil.

Years Incubation periods (days)

18–22 20–24 22–25 23–27 24–28 n19941995Total

101

606

325

808

224

20424

Mean1 = 24, SD = 1.671The mean is based upon the median values ofeach incubation period.

76

PICHORIM

see Table 6). These periods differ consider-ably from those estimated for the White-col-lared Swift (between 30 and 35 days,according to Marín & Stiles 1992).

During the breeding season of 1995, theincubation behavior in the nest located at siteS 17 was closely observed. The two birds thatbuilt this nest were captured and marked withmetallic bands and with phosphorescent disks(see Methods). It was observed that the incu-bation was done only by both of the twomarked birds. The sex of these two moni-tored birds could not be identified, but it ispresumed that they were a male and a female.It thus appears typical that no extra-parentalcooperation occurs in Biscutate Swift,although this behavior has been shown forother swifts (Dexter 1951, 1952). However,the possibility of these birds being twofemales that used the same nest should not beexcluded, since indications of oviposition ofmore than one female per nest exist, and thiscould also result in a cooperative incubation.During the breeding season of 1994, a malewas observed participating in the incubationof the eggs of site S 12. This male was depre-dated while sitting on the eggs. These obser-vations suggest that the both members of thepair participate in incubation, although thishas not been proven completely.

The pair marked with phosphorescentdisks was observed during 42 h and 22 min insix days. Of this time, the bird marked withdisk “A” remained on the eggs for 19 h and21 min (45.7%) and the “B” for 19 h and 37min (46.3%), showing a considerable equiva-lence of effort. The whole period of unatten-dance lasted 3 h and 24 min (8%). Theindividual periods of incubation for each birdwere also similar. Four individual periods ofincubation were observed for bird “A” andfive for the “B”, the average of them being 4h and 12 min and 3 h and 43 min, respectively(Table 7). At least in the studied case, theincubation was biparental as is the case in the

Black Swift (Marín 1997), but it was quitesimilar in magnitude for both sexes.

The incubation intervals were long, per-haps related to the need of the pair to flygreat distances for feeding, as was alreadynoted for other Cypseloidinae swifts (Marín& Stiles 1992). The bird that incubates stayson the nest for a long interval and, in somecases, it abandons the nest before the matehas returned. Two entire periods of pro-longed unattendance were observed, andaveraged 98 min. They did not cause theembryo’s death. Perhaps, these unattendanceperiods do delay the development of theembryo, culminating in an extended incuba-tion periods. The great variation of incuba-tion periods that were observed for the nestsreinforces this idea (Table 6).

The replacement of the incubating birdwas always made in a similar way. First of all,the bird that was outside the cave arrived andperched on the vertical rock wall about twometers below the nest. Next, it uttered somesharp swishes as that were sometimesanswered by a similar sound emitted by thebird that was on the nest. After 1–3 min, therecently arrived bird climbed the wall in thedirection of the nest. Using its feet, it crawledover the rock and flapped the wings freely.Then, it stopped nearer the nest and made thesame sound again. After that, the bird thatwas sitting on the nest left and perched on anearby wall leaving its place on nest free forthe returning bird. Finally, the returning birdclimbed the last part of the wall and settled onthe eggs.

Probably, the behavior of the returningbird is a way to announce itself to the birdthat is incubating, as a visual contact is largelyimpossible due to the darkness at the site.This behavior may also fill the gap of timenecessary for visual conditioning to darkness.In the cases where the nest was already aban-doned, the returning bird approached the nestlike described above. It landed and remained

77


quiet close to the nest for similar periods.This could indicate that the bird that arrivescan not see if the other bird is on the nest,and really needs some time to accommodateto the darkness of the cave.

During the observed individual incuba-tion periods, it was not possible to see anyassociated behavior, due to the darkness.However, some noises from the nest wereheard constantly. On two occasions, the birdthat was incubating was observed to leave thenest and fly to another place inside the cavewhere there was an accumulation of plantmaterial, including leaves and mosses. There,it collected some leaves in the bill andreturned to the nest, where I heard the samenoises already registered. These probablywere made by incubating birds during thearranging of the nest material, or perhapswhen turning the eggs. In addition, the birdthat was incubating occasionally uttered theascending call that is characteristic of the col-lective flights outside the cave. This reactionwas apparently related to the observer’s pres-

ence in the cave, as it happened in responseto some noises from inside the observationtent.

Nestlings. During the three years of study,nestlings hatched between the end ofNovember and early December. In caseswhere the clutch size was two, the secondnestling hatched usually one day after thefirst. In at least seven of 12 nests observed,hatching of the two chicks took place on dif-ferent days. As previously noted, in the clutchsizes larger than two, always one or more ofthe eggs were expelled during incubation,which resulted in a maximum of two nest-lings per nest.

The nestling period varied from about28–39 days, the average being 32.7 days (SD= 3.4, n = 17) (Table 8). After leaving thenest, they stayed perched on the nearby rockywalls where they continued to be attended byboth parents. They stayed inside the cave andwere cared by adult birds for a period thatcould not be measured precisely. However, it

TABLE 7. Periods spent incubating eggs and periods of unattendance observed in a pair of Biscutate Swiftin November of 1995 at Anhangava Hill, southern Brazil.

Periods spent incubating the eggs, periods of unattendance, and the respective day an time of observation (h:min)

Mean (h:min)

Bird A

Bird B

Unattendance4

03:061

1413:40–16:46

02:143

1416:46–19:00

01:3022

14:25–15:55

03:151

1011:05–14:20

02:221

1014:20–16:42

01:4510

09:20–11:05

04:572

1708:40–13:37

03:552

2210:30–14:25

–

05:302

2006:00–11:30

04:141

1714:35–18:49

–

–

05:482

2409:07–14:55

–

04:12SD = 01:12

03:43SD = 01:28

01:38SD = 00:11

1Period recorded from the exact moment of the arrival until departure of the bird of the nest.2Period recorded in the morning when the observation started with the bird on the nest.3Period recorded in the afternoon when the observation finished with the bird on the nest.4Only entire unattendance periods were considered.

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PICHORIM

is known that at the time of abandoning thenest, one nestling had a wing 150 mm inlength approximately, and the wing growthrate of the nestlings was about 4 mm per day.Considering that the nestlings only start toleave the cave when their wings measureabout 90% of the adult wing (mean = 207.4mm, SD = 4.3, n = 66), it is possible to esti-mate as 10 days the minimum time fledglingsremain inside the cave after leaving the nest.The earlier young bird captured outside thecave occurred on 20 January; its age was esti-mated to be between 48 and 52 days.

The recently hatched nestlings (0–2 daysof life) have the eyes closed and are nakedwith the pterylae little visible; the posteriorpart of the pteryla spinalis is most visible. Inthe dorsal posterior border of each wing,there is a line of small filamentous tips feath-ers (not surpassing 1 mm in length). It is fromthis line that later the greater coverts will

grow. Due to the absence of pigmentationand the skin’s transparency, tarsi, nostrils andthe tip of the bill are pinkish. The base of themaxilla and a small area at the base of themandible are gray. The claws are pinkishwhite, but a small portion of their bases andthe extreme tips of the toes are light gray. Thechicks remain quiet before being touched andmaintain the head prostrate on the border ofthe nest. After being touched, they do anx-iously lift the trembling head and utter a lowsharp peep. When being removed from thenest, they hold fast to the material of the nestcup with the feet, which are already anisodac-tylous. Nestlings of this age are generallybrooded by both parents and, when beingmanipulated, they drop body temperaturequickly. The extremities of the body are whit-ish.

At 2–4 days of life, the nestlings begin toacquire the first feather coat, which is consti-tuted of covering of gray down-like semi-plumes, as in other swifts (Collins 1963,Collins 1968b, Marín & Stiles 1992). Thesefeathers are visible especially on the back. Onthe ventral surface of the body, the feathers ofthe pteryla ventralis are visible on the flanks;however, no pinfeathers are erupted throughthe skin. The nostrils have become grayishand the dark pigmentation of the bill, tip ofthe toes and base of the claws has increased.The rest of the body still possesses a pinkishcoloration. These nestlings are quiet and,when being touched, they raise the head, leanon the belly and leave the tarsi forward. Theypeep and open the bill more frequently thanin the previous stage. The eyes remain closedand, when the nestlings are removed, theyhold on to the nest material. They cool downquickly. The extremities of their body arewhitish and they tremble a lot when handled.It is common to observe an adult bird on thenest or close to it.

Between the sixth and the tenth days oflife, the semiplume covering has grown over

TABLE 8. Nestling and fledgling periods observedfor the Biscutate Swift between 1994 and 1996, atthe Anhangava Hill, southern Brazil.

Nestling periods (days)

Sample size

Fledgling periods1 (days)

Sample size

27-2928-3030-3232-3434-3636-3838-40

Mean2 = 32.7SD = 3.4

1425131

n = 17

1-54-85-9----

Mean2 = 5.6SD = 1.5

131----

n = 5

1This is a partial fledgling period, in which the nest-ling had already left the nest but stayed near thenest on rock walls. The birds left the cave later andso the whole fledgling period could not be mea-sured because it was impossible to distinguish theyoung.

2The mean is based upon the median values ofeach period.

79


nearly the entire back, with the posterior por-tion covered by a layer about 5 mm thick. Onthe wings, the number of feathers is less andnude areas still exist. There is a line of smallsemiplumes in the pteryla of the greater sec-ondary coverts. The pinfeathers of the rem-iges are already visible, but the tips of thefeathers have not yet erupted. On the head,the semiplumes between the eyes start toappear. On the belly, the semiplumes coverthe flanks leaving a great central nude apte-rium and, on the throat, the first emergingfeathers are grayish white. The entire bill isgrayish black, including the margins of thegape. Only the tip is paler (pearl gray) and theegg tooth is still visible as a small white point.The nostrils are entirely dark gray. Theopened eyes have an opaque blue color withthe pupil not distinguishable. The eyes openbetween the sixth and the tenth day of life.This variation seems to be related to theamount of light at the nest site; nestlingsopened their eyes earlier at the illuminatednests than at the darker sites. The tarsi aredistinctly gray, the callus of support beingdarker. The tip of the toes and the convexpart of the claws are gray. The nestlings arequiet and let the head rest on the edge of thenest. When handled, they do not try to escapeor to peck, but hold fast to the material of thenest cup. Upon first contact, they raise thehead, lean with the tarsi forward, peep andopen the bill. They still cool down duringhandling, but less than in the previous stage.

Between 12 and 16 days of life, the backof the nestlings is totally covered by graysemiplumes with a thickness of 10 mm in theposterior region. A small bare pinkish area onthe neck can only be seen when the neck isstretched. On the head, the bare areas of theforehead and crown are gray and pinfeathersof the teleoptile feathers are visible but thetips are still sheathed. The bare skin of thewings is gray and the pinfeathers of thegreater coverts begin to show unsheathed

tips. The remiges measure approximately 15mm and their unsheathed tips measure 2 mm.The rectrices are 10 mm long. Outer rectriceshave only the tip of the rachis unsheathedand the central ones already show part of thevanes. The ventral bare area is pinkish and isrestricted to a small portion of the neck andabdomen, where sheathed teleoptile feathersexist without erupted tips. The bill is blackwith only the extreme tip being paler and stillshowing a tiny portion of the egg tooth. Theeyes have a dark brown iris and an opaqueblue pupil. The tarsi are brownish gray withthe callus being darker. The toes are dark grayand the claws gray, with the tips and the con-vex part of them paler than the rest. Thenestlings at this age are quiet and rest thehead on the edge of the nest when they arenot disturbed. When being removed from thenest, they hold fast to the nest material butneither try to escape nor to peck. When han-dled, they peep and are agitated until they canfix their feet in some substratum. At this age,they emit a strong peep with quite variablenotes. They do not cool down and are notclosely brooded by an adult bird as in the pre-vious phases.

Between 16 and 20 days of life, the upper-tail coverts show unsheathed tips. In the bareareas of the crown, forehead and face the firstcontour feathers appear, mainly in the areabelow the eyes. The feathers of the whitepatch of the nape show tips 1–2 mm inlength, which are not readily visible as theyare hidden under the gray semiplumes. Thewhite patch is less developed on the lowerthroat and upper breast. The ventral bare areastill exists, but is only visible when the neck isstretched. The unsheathed tips of the greaterwing coverts begin to expose and theunsheathed tips of the remiges have reached5 mm in length. The rectrices all have thesame size (± 10 mm, including the pin), butthe internal ones have longer rachis tips thanthe external ones. The throat and the ventral

80

PICHORIM

portion of the neck have light gray semi-plumes. On the belly, there are no eruptedtips of the pinfeathers and the central nudearea is quite reduced. The bill is all black witha whitish tip and the egg tooth has disap-peared. The nostrils are black. The tarsi aredark gray as well as the toes and the claws,which have a whitish tip. The nestlings of thisage are quiet and always stay still on the nest.When being removed from the nest, theyhold fast to the nest material. When held theypeep less than at the previous ages and getcalm when they manage to hold on to somesubstratum.

The head of nestlings 22–26 days old hasmore contour feathers than semiplumes. Thefeathers of the forehead and throat are gray-ish white. The white patch of the nape is verydistinct, however it is narrower than in anadult bird as the feathers have not fully devel-oped. The ventral white patch is also visible,but it has the form of a small triangle and notof a belt. The upper breast still shows a nar-row bare strip. The back is predominantlycovered by semiplumes, but many contourfeathers form a longitudinal band. The largestof these feathers have exposed tips 10 mm inlength and occur in the lower part of theback. On the flanks and on the undertailcovert area, the first contour feathers aremixed with the semiplumes. The tips of thegreater coverts are about 5 mm out of thesheath, leaving the dorsal wing face almostentirely covered, and without semiplumes. Onthe ventral face of the wings, there are someunsheathed pinfeathers and few semiplumes.The remiges are well developed and all haveabout the same size. All rectrices have theirdistal portions with vanes erupted from thesheath. The bill is black with a small whitishtip. The nostrils are black and the pupilsremain opaque blue. The tarsi are brownishblack as well as the toes. The claws are darkgray with whitish concave part. When a per-son approaches, the chicks hide in nearby

crevices, but do not fly and only rarely climbthe nearby vertical rocks. When handled, theyhold fast to the nest and do not peep, butsometimes emit a strident call.

When the nestlings are between 28 and 32days of life, they have the contour plumage ofthe body completely developed. On the dor-sum, semiplumes are still visible only in a nar-row strip from the nape to the uppertailcoverts. On the ventral part, semiplumes arestill present on the flanks and in the center ofthe belly; however, the contour feathers aremore obvious than the semiplumes. Thegreater coverts cover the whole dorsal surfaceof the wings, and all semiplumes have beencovered. The tips of the under coverts areabout 8 mm long. The remiges and rectriceshave reached half the size they will have whenadult. The bill is all black, as well as the nos-trils. The pupils remain opaque blue. The tarsiand toes are brownish black and the clawsdark gray with the concave part much paler.The nestlings still stay on the nests, but even-tually they can be seen perched on the nearbyvertical rocky walls at distances of up to 50cm. When threatened, they still do not fly, buttry to flee by climbing the rock wall with acertain difficulty. When captured they holdfast to the wall and scream.

At the stage of 32–40 days of life, thenestlings stay clinging to the vertical wallswithin about 2 m of the nest; whenapproached, they try to flee by climbing therock and flapping the wings (they still do notfly). It is possible that this type of behavioralso serves as an exercise for the wings, mak-ing them stronger and prepared to the firstflights. The dorsum is entirely covered bycontour feathers, without any semiplumesshowing. On the venter, semiplumes are seenonly on the flanks and thighs, and the contourfeathers have a narrow whitish edge. At thisage, the wing (flat) and the tail have reachedrespectively 80% and 90% of the length of anadult bird. The pupils are less opaque and the

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tarsi, nostrils and bill are black.The nestlings 40–48 days old are totally

feathered but appear more sooty than theadults. The forehead, chin and wing edges arewhitish. Besides, the feathers of the ventralpart have a narrow grayish white edge and theremiges, particularly the secondaries, have anarrow gray margin in the internal vexillum.The nestlings stay clinging to the verticalwalls within about 5 m from the nests. Theyare captured with difficulty, as they climb therock with much agility and flee amongst crev-ices of the nearby walls. They do not leave thecave and are thus still fed by the adults.

The whole post-embryonic developmentof the studied nestlings are summarized inTable 9.

Nestling measurements and development. Thestructures that had linear growth were thewing (flat) and tail (Figs 4A and 4B). How-ever, the tail starts to develop only after the

eighth day of life, and this can hinder the ageevaluation of younger individuals. In thesecases, the exposed culmen would be the via-ble option for aging because it had a lineargrowth in the first 10 days of life (Fig. 4C).

The mass increase was hardly linear (Fig.4D). Just after hatching, the chicks weighedabout 77% of eggs mass in average (mean =9.0 g, SD = 0.6, n = 12 ). The mass rate gainwas very high during the first 20 days of lifeand, at the end of this period, the mass of thenestlings was 13 times higher than when justhatched. After 20 days of life, the rate of massgain decreases day by day and the mass peakstabilizes at an age of about 27 days. Nest-lings of this age had an average mass of 136.2g (SD = 5.6, n = 9), which surpasses by12.3% that of the adults. In the breeding sea-son of 1994, a 28 days old nestling weighed147 g, which exemplifies the high growth rateof this species in the first month of life. Thestabilization of the mass coincides with theperiod of larger growth of the remiges, rec-trices and contour plumage. After the thirti-eth day of life, the nestlings begin to showmass recession. This loss of mass is probablyrelated to the abandonment of the nest andto the behavior of climbing the nearby rocks.Such events and activities certainly consumemore energy and the success of a nestling inthis phase should be related to the fat accu-mulation that was obtained during the previ-ous period. Chicks 41 days old weighed inaverage 123 g (SD = 5.7, n = 2), which indi-cates a loss of 9.7% from the 27 days oldnestlings mass prior to the birds having leftthe nest cave. The sub-adults captured inFebruary and March had an average mass of91.0 g (SD = 3.6, n = 3), which showed a lossof 33.2% of the peak mass of the chicks asthey left the nest. Certainly, the cause of thisis the intense physical activity and thereduced ability to obtain food. It is probablethat only the nestlings that manage to accu-mulate great fat reservations in the first 30

TABLE 9. Morphological and behavioral changesduring the nestling development of BiscutateSwifts at the Anhangava Hill, southern Brazil.

Morphological and behavioral changes

Estimated age (days)

Semiplumes emergeEyes openRectrices emerge out of pinfeather

sheathsRemiges emerge out of pinfeather

sheathsSemiplume plumage totally developedContour feathers emerge out of pin-

feather sheathsFirst escape behaviors noticedClimbing of the nearby vertical rocks

with return to the nestClimbing of the nearby vertical rocks

with abandonment of the nestBody contour plumage completeFirst flights made inside the caveFirst flights outside the cave

3 68

13

1315

2427

32

344048

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PICHORIM

days of life can survive this intense physicaldrain. This fact perhaps indicates the exist-ence of some control mechanism to maximizenestling size, perhaps limiting to two the max-imum brood size to be raised by one pair.

The tarsi showed a rapid growth, reachingmaximum development at the 19th day of life(Fig. 4E). This pattern can be related to theneed for the nestlings to have the hind limbdeveloped quickly for holding themselves inthe nests, avoiding accidental falls or expul-

sions. Certainly, the capacity of holding itselfin the nest is the major defense mechanismthat a nestling has. Therefore, the ideal periodto band the nestlings with metallic bands isafter the 19th day of life.

In general, the development of the plum-age and the growth pattern observed in Bis-cutate Swifts was similar to that observed byMarín & Stiles (1992) for White-collaredSwift. For both species the length of the wingis the best age indicator and the mass reaches

FIG. 4. Growth curves of wing, tail, exposed culmen, mass and tarsus in Biscutate Swift nestlings. Dashedline represents the mean adult size.

83


its highest value at about the 30th day of life,and then decreases about 10% to 15% afterleaving the nest site. The most conspicuousdifferences in these two species concern theincubation and growth periods, the values forBiscutate Swifts were shorter than those esti-mated for White-collared Swifts by Marín &Stiles (1992). Biscutate Swifts observed at theAnhangava Hill had greater body masses thanWhite-collared Swifts from Costa Rica andstill grew more quickly and had a shorterincubation. Although these differences couldbe explained by the geographical position ofeach study area or by other ecological factors,I think they can also be explained by the factthat the White-collared Swift data were esti-mated, and maybe are unreliable. Thus, forthe genus Streptoprocne, the data about incuba-tion and nestling periods presented in thispaper are the only ones based on exhaustiveobservations.

ACKNOWLEDGMENTS

The Conselho Nacional de DesenvolvimentoCientífico e Tecnológico (CNPq) and theFundação O Boticário de Proteção ÀNatureza supported this study. The ManometObservatory for Conservation Sciences pro-vided binoculars and the Centro de Pesquisaspara Conservação das Aves Silvestres/Insti-tuto Brasileiro do Meio Ambiente e RecursosNaturais Renováveis (CEMAVE/IBAMA)provided the bands. I am grateful to BiancaL. Reinert, Marcos R. Bornschein e Paulo H.E. Labiak for the indispensable help duringthe field activities. For suggestions and col-laboration I thank Prof. Emygdio L. A. Mon-teiro Filho. Prof. Dante M. Teixeiracollaborated at the beginning of the study.Marcelo P. Marcelli, Olga Yano, Paulo H. E.Labiak and Sandro Menezes Silva identifiedthe nest material (lichens, bryophytes, pteri-dophytes and angiosperms, respectively).Darci P. Zakrzewski supplied maps about the

topography of the studied cave. I thank EvaC. R. Avelar Dalmolin and André A. R. deMeijer for checking the English style. I amalso grateful to the referees Charles T. Collinsand Manuel Marin who improved the manu-script.

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