breeding ecology of a burrow-nesting passerine, the … · 2018. 6. 11. · this study occurred in...

BREEDING ECOLOGY OF A BURROW-NESTING PASSERINE,THE WHITE-RUMPED SNOWFINCH MONTIFRINGILLA TACZANOWSKII

ECOLOGÍA REPRODUCTIVA DE UN PASERIFORME NIDIFICANTE EN MADRIGUERAS, EL GORRIÓN ALPINO DE MANDELLI

MONTIFRINGILLA TACZANOWSKII

Xianhai ZENG* and Xin LU* 1

SUMMARY.—Breeding ecology of a burrow-nesting passerine, the white-rumped snowfinch Monti-fringilla taczanowskii.

This work provides reproductive data about the white-rumped snowfinch Montifringilla taczanowskiiand learn how avian life history respond to cavity-nesting and altitudinal gradients. The study was carriedout in an alpine meadow in the northeastern Tibetan plateau, in Gahai National Nature Reserve (34° 14’N, 102° 20’ E). During two breeding seasons individuals were marked and their nests contents weremonitored. Nests were placed in pika Ochotona curzionae burrows and constructed by females only. Egg-laying occurred between late April and early June. Some pairs (9 %) made two breeding attempts in asingle year. Clutch size averaged 4.7 (2 - 6) and brood size at fledgling average was 3.5 (2 - 6). Femalesincubation lasts 9 to 15 days (13) and both sexes provide parental care until nestlings fledged at 18 to 24days (21). Overall, 69 % of the nesting attempts produced at least one fledgling. The habit of cavity-nest-ing might allow the snowfinches to start breeding earlier, produce larger clutches, reduce nest attentive-ness and enjoy a higher reproductive success than several local open-nesting passerines. Compared to theirhigher-altitude conspecifics, the lower-altitude snowfinches reach a greater annual productivity mainlythrough rearing larger broods.

Keywords: alpine meadow, cavity-nesting, life history, Montifringilla taczanowskii, reproduction, Ti-betan plateau.

RESUMEN.—Ecología reproductiva de un paseriforme nidificante en madrigueras, el gorrión alpinode Mandelli Montifringilla taczanowskii.

El trabajo ofrece una serie de registros reproductivos de una especie poco conocida, proporcionandoinformación sobre cómo un nidificante en madrigueras responde a los gradientes altitudinales. Se reali-zó en praderas alpinas del noreste de la altiplanicie tibetana, en la Reserva Natural de Gahai (34º 14’ N,102º 12’ E). Durante dos estaciones reproductoras se marcaron los individuos e inspeccionó el contenidode los nidos. Los nidos se ubicaron en madrigueras de pika Ochotona curzionae y son construidos ex-clusivamente por la hembra. La puesta acontece a finales de abril y principios de junio. Algunas parejas(9 %) realizan dos intentos de cría en una misma estación reproductora. El tamaño medio de la puesta es de4,7 huevos (2 - 6) y el de pollos de 3,5 (2 - 6). La incubación corre a cargo de la hembra durante 9 - 15 días

* Department of Zoology, College of Life Science, Wuhan University. Wuhan, 430072. China.

1 Corresponding author: [email protected]

Ardeola 56(2), 2009, 173-187

INTRODUCTION

The genus Montifringilla contains sevenspecies all well adapted to treeless alpine mead-ow or rocky environments in the Tibetan plateau(Vaurie, 1959; Sibley and Monroe, 1990;Cramp and Perrins, 1994; Zheng, 2000). Oc-cupying altitudes ranging from 3,000 to 5,000m, the snowfinches represent the highest alti-tude distributed passerine birds in the world.Adaptive radiation of the avian genus is thoughtto have occurred 2 - 2.25 mya with dramaticclimatic changes resulting from the uplift ofthe Tibetan plateau (Qu et al., 2006).

Snowfinches are secondary cavity breed-ers, nesting in burrows of small mammals,rock crevices or building holes. The harshhigh altitude environments in terms of cli-mate and vegetation structure (Landmann andWinding, 1993, 1995a, b) provide limitedspaces for recourse partitioning among thesnowfinch species. As a result of interspecif-ic competition, most Montifringilla snow-finches are separated by altitudes or micro-habitats although they may overlap in overallgeographical distribution (Zheng, 1983; Quet al., 2002). The white-rumped snowfinchM. taczanowskii (40 g in body mass) is oneof the largest species among its genus and oc-curs across much of the Tibetan plateau.Being dominant over other small-sized con-geners, white-rumped snowfinches occupylower altitudes where ecological conditionsare relatively good, excluding other symmet-

rically-breeding snowfinch species to high-er altitudes or poor-quality habitats (Zengand Lu, 2009).

Breeding of the white-rumped snowfinchis poorly known so far. Zhang (1982) only pro-vides a sample list of breeding season, clutchsize and egg size of this species occurring ina 3,300 m alpine meadow in northern Qing-hai. We also collected a few data on nestingecology of the birds at a higher site in northTibet (4,300 m; Lu et al., 2009). In this paper,we report a two-year study on an individual-ly marked population in the northeastern Ti-betan plateau. The knowledge will contributeto our understanding of how birds, in gener-al, cope with extreme environments (Martinand Wiebe, 2004; Bears et al., 2009). More-over, alpine animals well adapted to extremeconditions are more vulnerable to humanactivities, especially global climate change(Smith and Foggin, 1999; Wu et al., 2005).Thus, the current data may aid conservationof the alpine ecosystem.

METHODS

Study site and species

This study occurred in Gahai National Na-ture Reserve (34° 14’ N, 102° 20’ E) in thenortheasternTibetan plateau from April to Sep-tember in 2006 and 2007. The study area isrounded by relatively low mountains (3,450 -

(13) y los pollos son cuidados por los dos padres hasta la edad de 18 - 24 días (21). Del total de los inten-tos de cría, el 69 % sacaron al menos un pollo. El tipo de nido en madriguera permite a los gorriones al-pinos de Mandelli comenzar temprano la reproducción, producir muestras más grandes, dedicar menostiempo a la atención del nido y disponer de un grado más elevado de éxito reproductor que otros paseri-formes locales que crían en nidos abiertos. Comparado con conespecíficos de altas latitudes, los gorrio-nes alpinos de Mandelli que nidifican en bajas latitudes tienen una productividad anual mayor al realizarcrianzas más grandes.

Palabras clave: altiplanicie tibetana, estrategias vitales, Montifringilla taczanowskii, nidificante enmadrigueras, praderas alpinas, reproducción.

ZENG, X. H. and LU, X.

Ardeola 56(2), 2009, 173-187

174

3,800 m) covered with alpine Kobersiasteppe meadow. Detailed information on cli-mate and vegetation can be found in Wang etal., 2007 and Zeng and Lu, 2009.

White-rumped snowfinches are sexuallymonomorphic in size and plumage. They nestin burrows of the black-lipped pikas Ochotonacurzoniae, the most dominant small mammalsin the area (mean density of pika burrow = 90per 100 ha; Zeng, 2008). Pika burrows are 10- 80 cm under the ground and a burrow systemconsists of branched tunnels which lead to onechamber at the end and one open on soil sur-face. Active burrows currently used by the pikasare preferred over inactive ones previously used(Zeng and Lu, 2009). Distance of the nearestsnowfinch nest neighbours varies from 2 to1,400 m (averaged 65 m) and territory size from1,029 to 5,131 m2 (average 1,715 m2) in whichthe birds displayed most foraging activities.Within the study plot, the densities of breed-ing snowfinches were 13 pairs per 100 ha in2006 and 17 pairs per 100 ha in 2007. Moder-ately-steep slopes, abundant burrow openingsand large bare-patches around the nest burrowentrance character snowfinch nest burrows incomparison to random-sampled burrows.

Another snowfinch species sympatricallybreeding in the alpine meadow is the rufous-necked snowfinch M. ruficollis (30 g). Beingsmaller in size and thus lower in social rankthan the white-rumped snowfinch, this speciesexhibits no territoriality, nests in deserted pikaburrows located in marginal habitats, and hasa much low breeding density (2 pairs per 100ha) compared with the white-rumpedsnowfinches (Zeng and Lu, 2009).

Data collection

A study plot of 390 ha extending between3,400 and 3,650 m was set in the alpine mead-ow. Nests were systematically searched overthe plot by following nesting-related activities.Nests located were checked every day or every

other day to monitor their breeding progressand fate. Around the expected time of hatch-ing and fledging nest visits were made daily.Adult snowfinches were mist-netted at theirbur row entrance during the incubation(mainly females) and or nestling period (main-ly males). For each individual captured, wemeasured its body mass (with an electronic bal-ance to the nearest 0.1 g) and linear dimension(body, bill, wing, tail and tarsus length, witha calipers to nearest 0.1 mm) and marked itwith colour leg rings and an aluminum ring.Adults were sexed by behaviour and incuba-tion patches and further by DNA analysis us-ing the brood samples taken upon capture(Zeng, 2008). Behavioural data, including nestselecting, nest building, mate guarding (pairdistances and the sex initiating a movement),copulation, incubating and young-caring, werecollected for randomly-selected focal pairs ornests from a distance of 40 - 50 m at which thebirds behaved normally. Through locating allnesting attempts in the study plot throughoutthe breeding season, we may determine howmany broods a pair produced per year.

To check nest contents, we dug a verticalhole at the end of the snowfinch nest place-ment. The hole then was re-covered with soil-filled bags to facilitate subsequent inspection.These operations were made for a few nestsand did not lead to burrow collapse or otheradverse effects on breeding activities of thebirds. Nest dimension measured include: ex-ternal diameter (the widest part of the nest out-side wall), internal diameter (the widest partof the nest inside wall), cup depth (the verti-cal distance from the entrance rim to the bot-tom of the inner cup) and cup height (the dis-tance from the entrance rim to the bottom ofthe outside of the nest). Eggs were measuredfor their fresh mass (using an electronic bal-ance to the nearest 0.1 g), and maximum lengthand width (using a calipers to nearest 0.1 mm).Nestling development was regularly monitoredthrough measuring their body mass and lineardimensions.

Ardeola 56(2), 2009, 173-187

BREEDING ECOLOGY OF THE WHITE-RUMPED SNOWFINCH 175

Nestlings near fledging received food fromparents at the burrow entrances. The behavioursallowed us to count brood size, captured, markedand measured the young (with the same methodas taken in adults). The sex of young was mol-ecularly analyzed using blood samples collect-ed at capture. We considered the egg-laying dateto be when a female frequently made briefvisits to the nest with her mate, which occurreda few days after the female ceased carrying softnest materials. Incubation was thought to startwhen we failed to observe the female aroundher nest for at least one day, and hatching datewas determined when the female came back thenest with food for the first time (this usuallycorresponded to the time egg shells were foundnearby the burrow). The nestling period was thespan from the hatching to fledging date, the dayon which the nestlings firstly appeared in theburrow entrance (in some cases this was con-firmed by the fresh droppings of nestlings).Food items delivered to nearly fledged youngwere collected by neck-collaring. Each nestlingwas neck collared once for 15 - 20 min, lead-ing no effect on its survival although no foodwas fed after the operation. We identified thepossible causes of nesting failure based on di-rect observations or analyzing the remains with-in or near the nests.

Data analysis

We used the methods of Gjerdrum et al.(2005) to calculate the first-egg date accord-ing to 38 daily-monitoring nests (where themean ± SD discovery date was 3.7 ± 2.8 daysafter nesting started). Comparisons were per-formed with parametric analyses and relation-ships between two variables with Pearson’s orpartial correlations. Effects of nesting variableson nest fates were examined with logistic re-gression analysis. The significant level was setat P < 0.05 and summary statistics are present-ed as mean ± SD. A total 190 nests were locat-ed during the two-year study. However, sam-

ple size varied among different nesting param-eters because of limited survey efforts made incollecting some of these parameters.

RESULTS

Annual turnover and recruitment of thesnowfinch population

More breeders in both sexes than youngmarked in 2006 were rediscovered in the studyplot in 2007 spring (table 1). However, the pro-portions of individuals that were found to nestin the plot were lower in adults (6 % of 17 malesand 20 % of 15 females) than young (62 % of13 males and 86 % of 7 females). All thoseadults re-mated in 2007. In additional, a 2006breeding pair divorced in 2007, with both themale’s and female’s nests being located outsidethe study plot (distance from the previous nestsite, the male 1 km and the female 2 km).

Breeding season

Egg-laying was initiated in mid-April (earli-est 16 April) and ended in late June (latest 22


Ardeola 56(2), 2009, 173-187

176

TABLE 1

The turnover of breeders and recruitment ofyoung of the white-rumped snowf inch in analpine meadow, northeastern Tibetan plateau.[Balance de reproductores y reclutamiento de jó-venes del gorrión alpino de Mandelli en una pra-dera alpina del noroeste de la planicie tibetana.]

Breeder Young

Male Female Male Female

No. of birds 24 30 61 43marked in 2006No. of birds 17 (71) 30 (50) 13 (21) 7 (16)rediscoveredin 2007 (%)

June), lasting about 70 days. The average datesof the first egg were the same (27 may ± 12 days)in 2006 (N = 67) and 2007 (N = 80). Most pairs(91.2 % of 147) yearly bred one brood and a few(8.8 %) two broods. For single-brooded pairs,the laying date averaged 9 May (± 11 days, N= 126). On average the first attempt of double-brooded pairs started on 5 May (± 14 days, N= 12), and the second on 25 May (± 13 days; fig.1). No pairs marked after the middle of breed-ing period were found to produce a replacementclutch after failure (N = 13), but the possibilityof re-nesting existed for those pairs that failedearly in the season (N = 3).

Nest construction

Snowfinches placed their nest at the cham-ber or the middle of tunnel of a pika burrow,

36 cm (± 50, 15 - 60, N = 23) to the groundsurface and 159 cm (± 53, 80 - 225) to theburrow entrance. Of 190 nests located, 182were built in initially active pika burrows (thepikas were present when the birds selectednest burrows), and only 6 in inactive pika bur-rows (already deserted by the pikas). Nestconstruction was undertaken by females alonefor 2 to 10 days (5.6 ± 2.7, N = 11). Double-brooded females took longer to build theirfirst nests (7.0 ± 2.3 days, 5 - 10, N = 7) thanthe second ones (3.6 ± 1.3 days, 2 - 5). Nestmaterials, mostly grass stems, were trans-ferred at a rate of 10.0 times per h (± 10.1, 0- 33, 521 minutes of observations for 15 nests.The nests were cup-shaped, with external di-ameter being 23.7 cm (± 3.2, 17.8 - 28.0, N= 8), internal diameter 9.4 cm (± 4.4, 7.5 -15.0), cup depth 6.3 cm (± 0.7, 5.6 - 7.5) andcup height 9.3 cm (± 2.5, 6.5 - 12.0).

Ardeola 56(2), 2009, 173-187


FIG. 1.—Temporal distribution of the date of laying the first egg by the white-rumped snowfinch in analpine meadow, northeastern Tibetan plateau. The time of clutch initiation is arranged in 5-day periods.[Distribución temporal de la fecha de puesta del primer huevo del gorrión alpino de Mandelli en unapradera alpina de la altiplanicie tibetana. La fecha de inicio de puesta está ordenada en periodos de5 días.]

FIG. 2.—Growing curve of nestling body weight of the white-rumped snowfinch in an alpine meadow,northeastern Tibetan plateau. The figures above the standard deviation bars are sample size.[Curva de desarrollo del peso de los pollos del gorrión alpino de Mandelli en una pradera alpina de la alti-planicie tibetana. Las barras indican la desviación estándar y encima figura el tamaño de muestra.]

Egg-laying, egg and clutch size

One egg was deposited daily (observationfor 30 eggs in 9 nests), usually before 08:00 h(observations for 5 eggs in 5 nests). Duringthe laying period both sexes did not roost inthe nest burrow during night based on inspec-tion in early morning for 6 nests. The egg-lay-ing period lasted 4 - 7 days (4.7 ± 0.8, N = 23).The eggs were elliptical in shape and purewhite in coloration. Fresh mass of six eggs av-eraged 3.6 g (± 0.2, 3.4 - 3.8), length 25.7 mm(± 0.8, 24.8 - 26.2) and width 16.9 mm (± 0.8,16.5 - 17.8). Clutch size ranged from 2 to 6eggs (4.7 ± 1.5, N = 7).

Incubation

Only females undertook incubation. During1,026 minutes of observations on 14 pairs, a fe-male spent 48 % of her daytime in the nest, withon-nest bout averaging 26.3 min (± 13.1, 10 -65, N = 14 pairs of 24 observations) and off-nest 7.4 min (± 6.0, 2 - 29, N = 14 pairs of 22observations). Over the observational period,

we recorded no male with food entering the nestin which the female was sitting. The incubationperiod ranged from 9 to 15 days (12.7 ± 1.6, N= 34 pairs, not including the four where incu-bation was delayed by pika excavation activi-ties that blocked the nests). Clutches started lat-er tended to have a longer incubation duration(r = 0.39, N = 34, P = 0.02).

Nestling development and parental care

Newly-hatched young were naked, with acluster of gray down on the forehead and oc-ciput. Eyes opened at about day 7 after hatch-ing (N = 11 nestlings from 3 nests). Nestlingsfledged at age of 18 to 24 days (21.3 ± 2.0,N = 16 nests) when they had plumage similarto the adult’s and reached 79 % (± 8, 59 - 99,N = 241) of the adult female weight. Growthof nestling weight followed a logistic model(w = 32.6 / (1+e1.499–0.212t, r2 = 0.90, N = 14nestlings from three broods, fig. 2).

Direct watches on young caring activitywere made of 21 pairs for 2,598 minutes in to-tal (mean watch length 1009 ± 33 minutes,


Ardeola 56(2), 2009, 173-187

178

range 58 - 191). Females spent 27 % (± 23, N= 21, 0 - 71) of their daytime brooding in theearly nestling period (< day 10), with thebrooding bouts lasting 29.7 minutes (± 28.2,5 - 91). Both parents fed their young and a par-ent carried one or more prey items eachfeeding trip. Of 730 trips recorded across thenestling period, 405 were made by females and325 by males. Average feeding rate per hourin females was 6.5 (± 5.1, 0 - 16.8, N = 21pairs) and 6.1 (± 7.6, 0 - 34.7) in males, notdiffering between sexes (paired-samples t-test,t20 = 0.32, P = 0.76).

Most double-brooded pairs (18 of 24) start-ed their second clutches during the nestling pe-riod of the first clutch and the remaining didso after completion of the f irst one. In theformer cases the females alternatively carriedfood to the nestlings and nest materials to thenew nest. The distances between the first andsecond nests were less than 50 m.

Shortly after fledging (less than 3 days), ju-veniles received food at the nest burrow en-trance from their parents. Observations basedon 16 trapping attempts in the early morningfor 8 nests showed that at this stage parentalbirds did not roost in the burrow at night. Thejuveniles moved away the nest burrows as theygrew up and during the night they roosted inrandomly selected pika burrows. Parents fedthe juveniles continuously for 2 to 3 weeks un-til they were able to feed themselves (observa-tions for 5 broods).

Nestling diet

Nestling diet consisted entirely of arthro-pods. Of 63 food items collected from 17nestlings in 6 broods before mid-May, 95 %belonged to larvae of Lepidotera andColeoptera. In contrast, among 72 items from13 young in 7 broods after mid May, 85 % wasadult insects (Hymenoptera 35 %, Coleoptera29 %, Diptera 21 %), and only 15 % Lepi-dotera larvae.

Breeding success

Brood size at fledging was 3.3 ± 0.8 (2 - 5,N = 36) in 2006 and 3.6 ± 0.8 (1 - 6, N = 31)in 2007, without statistical difference betweenthe two years (t = 0.55, df = 69, P = 0.59). Onaverage, successful single-brooded pairs pro-duced 3.4 fledglings (± 0.9, 1 - 5, N = 38); dou-ble-brooded pairs fledged 3.7 young (± 1.1, 2- 6, N = 12) in their first broods, statisticallysimilar to 3.3 (± 1.0 young, 1 - 5) of the sec-ond broods (t11 = 0.94, P = 0.36). There wasno significant difference in brood size betweensingle- and double-brooded pairs (t67 = 0.31,P = 0.76). Brood size was independent of lay-ing date (partial correlation coefficient con-trolling for year, r = 0.002, N = 66, P = 0.99).

Overall reproductive success, measured asthe percentage of broods from which at leastone young survived to fledge, was 54 % (N =82) in 2006 and 75 % (N = 108) in 2007. Dou-ble-brooded pairs reached a reproductivesuccess in their f irst attempts (100 %, N =12) similar to that in the second attempts (93%, N = 15; χ

21 = 0.83, P = 0.36). Overall, the

proportions of successful single-brood pairs(60 %, N = 132) were signif icantly lowerthan those of double-brooded pairs (96 %, N= 27; χ

21 = 13.28, P < 0.001). Snowf inch

nests placed in active pika burrows were morelikely to be successful (67 %) than those in in-active burrows (17 %). Nest fates were relatedto laying date, late broods having a higher like-lihood of success (Logistic regression: Beta= 0.078, Wald = 11.6, P = 0.001).

Of 65 failed attempts, 18 (28 %) occurredbefore laying, 12 (19 %) during incubation, 28(43 %) during the nestling period and 7 (11 %)shortly after fledging. For 51 nests where thereasons of failure were identif ied, 37 %failed due to nest collapse caused by excavat-ing activities of underground-dwelling mam-mals and other 37 % due to desertion; killingof nestlings, fledglings or parents by carnivo-rous mammals and birds accounted for 18 %and 8 %, respectively (table 2). Brood mor-

Ardeola 56(2), 2009, 173-187


tality involved complete (nest predation or col-lapse of nest burrow, N = 30 nests) or partialbrood losses (some nestlings died of starvationor cold, N = 5 nestlings in 3 nests).

Social behaviour

Mating of the snowfinches shows them tobe socially monogamous. Pair bonds were firstseen in late March, when they began to estab-lish territory by fighting with conspecifics orother small animals (including pikas and sev-eral passerines) at some specific points (hourlyaggressive frequency, 36.7 ± 53.9, 1 - 300, N= 43 pairs of 47.7-h observation). At thesame time, followed by her mate, the femalefrequently visited and checked pika burrowsto locate nest-sites. This process lasted a fewdays until they found a suitable one. Males con-tinued guarding their mates during nest-build-ing and egg-laying period (pair distances, 2.1

± 1.6 m, 0.2 - 6.0, N = 39; movement initiatedby female, 84 % of 82 records). When femaleswere incubating, males were not seen nearthe nest. However, near the off-nest time,they always came to the burrow entrance to calltheir mates or entered the burrows if there wasno response from the females (11 records for7 nests). If the females stayed outside the nestfor more than 10 minutes (59 records of 300off-nest events for 21 pairs), the males routine-ly (97 % of the 59 records) flew in a semicir-cular trajectory over the females (less than 20cm) and gave a short, loud call. In response tothe males’ display, the females returned to thenest to incubate.

A total of 16 copulation attempts, all beinginitiated by males, were noted for 13 pairs dur-ing 521 minutes of observation within threedays after completion of nest construction, butnone was successful. During observations of1,239 minutes for 14 pairs during the incuba-tion period and of 3,638 minutes for 25 pairs


Ardeola 56(2), 2009, 173-187

180

TABLE 2

The causes of nesting failure of the white-rumped snowfinch in an alpine meadow, northeastern Tibetanplateau.[Causas del fallo en la reproducción del gorrión alpino de Mandelli en una pradera alpina del noroestede la planicie tibetana.]

Reasons of breeding failure 2006 2007 Both years(N = 38) (N = 27) (N = 65)

Preyed by raptor birdsblack-eared kite Milvus lineatus 1 0 1upland buzzard Boteo hemilasius 1 1 2sake falcon Falco cherrug 0 1 1

Preyed by carnivorous mammalsstone marten Martes foina 1 5 6domestic cat 0 3 3

Destroyed by ground-dwelling mammalsblack-lipped pika Ochotona curzoniae 7 2 9striped hamster Cricetulus barabensis 2 3 5common zokor Myospalax frontanieri 3 2 5

Desertion 13 6 19Unknown 10 4 14

during the nestling period, copulation attemptswere never observed.

DISCUSSION

Cavity-nesters may gain direct or indirectfitness benefits from thermal protection pro-vided by the cavities (Stoleson and Beissinger,1995; Beissenger et al., 2005; Godard et al.,2007). The benefits should be more obviousfor the snowfinches nesting in the harsh alpinehabitats where the daily temperature during thebreeding period changes sharply (-4.7 to23.4ºC). Indeed, the birds initiated breeding 2- 5 weeks earlier than several open-nestingpasserines in the alpine meadow habitats (table3). The early onset of reproduction resultedin a wide breeding window (about 70 days) andallowed some snowfinches to have secondclutches. This could also contribute to the im-proved survival probability of snowfinchnestlings reared in the later broods. The dou-ble-brooded pairs did not start their first clutch-es earlier than those producing a single clutch,a result of reduced time constraint on the cav-ity-nesting birds. Nevertheless, like some sub-alpine birds that breed twice per season (citedfrom Badyaev, 1997), overlaps between the twoattempts where only the male snowfinches con-tinued to provision the first brood while the fe-male snowfinches incubated a second clutchshould be an adaptive strategy to deal with thelimitation of breeding time available.

Being protected from inclement climatesand nest predators, birds nesting in cavity en-joy a high breeding success compared withopen-nesting species (Martin and Li, 1992;Clark and Shutle, 1999). The same situationmay be seen in the passerines breeding in thealpine meadow (table 3). The white-rumpedsnowfinches, along with three other local cav-ity-nesters, produce larger clutches than do thefour open-nesters. Martin (1993) argued thatthe larger clutches of secondary-cavity nestersare a response of increased reproductive efforts

to the limited availability of nest sites or breed-ing opportunities. This hypothesis could notapply to the white-rumped snowfinches in ourstudy area where pika burrow densities are veryhigh and competition among the birds for nestburrows was expected to be less severe (Zengand Lu, 2009). It is also the case for two othersecondary-cavity nesters, the rufous-neckedsnowfinch (nesting in pika burrows) and theblack redstart Phoenicurus ochruros (nestingin natural holes or burrows created by the Ti-betan ground tit Pseudopodoces humilis).Adaptation to the low nest predation rates whichcharacterize cavity-nesting birds should bean acceptable explanation for the difference inclutch size between the two types of nester(Slagsvold, 1982; Lima, 1987). Similarly, thereduced nest predation risk also permits a pro-longed young development period of these cav-ity-nesting species (Lack, 1948, 1968).

Species with females as the sole incubatormust balance the thermal demands of embryosby staying on the nest with their own nutrition-al needs by leaving the nest to forage (Conwayand Martin, 2000). Snowfinch females takelong on- and off-nest periods compared to sev-eral open-nesting alpine passerines (table 3).Warmer microclimates in nest burrows, allow-ing the eggs to remain unattended for longer(Conway and Martin, 2000), should be respon-sible for the differences. In many bird species,males often feed incubating females and thebehaviour can reduce energy constraints on thefemales, and in turn increase nest attentivenessand improve hatching success (e.g. Lifjeld andSlagsvold, 1986; Halupka, 1994; Martin andGhalambor, 1999). Nest attentiveness shownby the snowfinches was relatively short com-pared to that shown by the open-nesting species,although they received no food from theirmates. This may be associated with the advan-tage of microclimates in nest burrows (Whiteand Kinney, 1974; Lifjeld et al., 1987; Nilsonand Smith, 1988). Interestingly, the absence ofmale feeding of females in the snowfinchesis different from the general pattern in that the

Ardeola 56(2), 2009, 173-187



Ardeola 56(2), 2009, 173-187

182TA

BL

E3

Aco

mpa

riso

nof

life

hist

ory

trai

tsw

ith

resp

ectt

one

stty

pefo

rse

vera

lpas

seri

nesp

ecie

sbr

eedi

ngin

the

alpi

nem

eado

wha

bita

ts,n

orth

wes

tern

Ti-

beta

npl

atea

u.[C

ompa

rati

vade

los

rasg

osbi

ológ

icos

resp

ecto

alti

pode

nido

deal

guna

ses

peci

esde

pase

rifo

rmes

que

cría

nen

hábi

tats

depr

ader

asal

pina

sen

elno

roes

tede

laal

tipl

anic

ieti

beta

na.]

Bre

edin

gC

lutc

hIn

cuba

tion

On-

nest

%ne

stM

ale

beha

vior

Nes

tlin

g*R

ef.

star

tda

tesi

zepe

riod

leng

that

tent

iven

ess

duri

ngpe

riod

(d)

(min

)in

cuba

tion

horn

edla

rkla

teA

pril

2.4

118.

762

nest

defe

nse

11.3

1E

rem

ophi

laal

pest

ris

orie

ntal

skyl

ark

mid

-May

2.8

1225

.275

nest

defe

nse

8.8

1A

laud

agu

lgul

a

robi

nac

cent

orm

id-M

ay3.

211

.5–

–fe

edin

gfe

mal

e11

.93

Pru

nell

aru

becu

loid

es

twit

ela

teJu

ne4.

515

24.8

88fe

edin

gfe

mal

e14

.04

Car

duel

isfl

avir

ostr

is

blac

kre

dsta

rtea

rly

May

4.8

13.5

–71

nest

defe

nse

5P

hoen

icur

usoc

hrur

os

Tib

etan

grou

ndti

tea

rly

May

6.8

1522

.963

feed

ing

fem

ale

17.9

6P

seud

opod

oces

hum

ilis

whi

te-r

umpe

dsn

owfi

nch

mid

-Apr

il4.

713

.127

.048

nest

defe

nse

21.3

7M

onti

frin

gill

ata

czan

owsk

ii

rufo

us-n

ecke

dsn

owfi

nch

earl

yA

pril

4.0

12.5

39.0

68ne

stde

fens

e21

.98

M.r

ufic

olli

s

*1.

Zha

nget

al.,

2000

;Z

hao

etal

.,20

02;

3.L

iet

al.,

2003

;4.

Zha

oet

al.,

2003

;5.

Mu

etal

.,20

08;

6.D

uan

dL

u,20

09;

7.T

his

stud

y;8.

Our

own

data

.*

1.Z

hang

etal

.,20

00;

Zha

oet

al.,

2002

;3.

Li

etal

.,20

03;

4.Z

hao

etal

.,20

03;

5.M

uet

al.,

2008

;6.

Du

and

Lu,

2009

.P

rese

nte

estu

dio;

8.R

egis

tros

prop

ios.

behaviour is more common or extensive in cav-ity-nesting than open-nesting birds (Lyonand Montgomerie, 1987; Martin and Ghalam-bor, 1999).

All the eight passerine species inhabitingthe alpine meadow are socially monogamousand both parents feed the young. However, maleparental behaviour during the incubation peri-od differs and two distinct strategies may beidentified: (i) defending the nest without incu-bation feeding, and (ii) feeding the femaleswithout nest guarding (table 3). The white-rumped snowfinch adopts the former. The dif-ference may reflect a species-specific trade-off between paternity protection and femaleenergy supplement (Wright, 1998).

Seasonal decline in clutch size of single-brooded temperate passerines is thought tobe an adaptive response to reduced food avail-ability, along with shortened day length (Per-rins, 1970; Klomp, 1970). Brood size at fledg-ing in the white-rumped snowfinches, whichis mainly a single-brooded nester, does notchange with laying date after accounting forthe number of breeding attempts. This suggeststhat the birds suffer no food shortage in the latebreeding season, as indicated by increased nest-ing success with laying date.

Altitude creates environmental gradientsalong which breeding performances and lifehistories of birds varies. Because of ecologi-cal severity at high altitudes, birds nesting therestart to lay later than those nesting at low alti-tudes (Bears et al., 2009). It is the case for thewhite-rumped snowfinch breeding at three dif-ferent altitude sites in the Tibetan plateau (table4). It has been shown that high-altitude birdsproduce fewer broods, smaller clutches, larg-er offspring, and make greater parental effortsthan their lowland conspecifics (Krementz andHandford, 1984; Badyaev, 1997; Badyaev andGhalambor, 2001; Lu, 2005; Bears et al., 2009).This shows that birds shift their life historystrategy from r- to k-selection as altitudes in-crease (Pianka, 1970). The comparisons amongthe three populations showed that the higher

altitude snowfinches have smaller clutch andbrood sizes, longer incubation and nestling pe-riods, and more frequent feeding trips, support-ing the predication.

However, unlike what was expected, the av-erage number of broods produced per year bya snowfinch pair is the same at the 3,600-mand 4,300-m sites. Also, the birds at the two al-titudes enjoy a similar high reproductive suc-cess. It is likely that the nature of cavity-nest-ing reduces the constraint of seasonal time onreproduction and the nest predation. Large eggsmay lead to well-surviving offspring becausethey contain more yolk and lose heat less rap-idly in cold climates due to a lower surface area-to-volume ratio (Rhymer, 1988; Williams,1994; Smith and Bruun, 1998; Martin, 2008).An important method used by birds to copewith stress conditions is to trade off betweenoffspring number and quality (Partridge andHarvey, 1988; Blackburn, 1991). However, in-consistent with the predication, we f indsnowfinch eggs to be smaller in the north ofTibet. This may be attributed to the small fe-male body size of the highland population. Ad-ditionally, the harsher ecological conditions athigher altitudes could constrain the productionof eggs, not only on their numbers but also ontheir sizes. Johnson et al. (2006) observedsmaller eggs at a passerine inhabiting the high-er altitude and argued that selection mightfavour sacrificing egg size before sacrificingegg number (clutch size).

Overall, the harsher ecological conditionsexperienced by high altitude breeders must lim-it their annual reproductive output. It is the casefor the snowfinches. The lower productivityalong with poorer resources also contributesto lower population densities of the higher-al-titude sonwfinches. Nevertheless, the reducedinvestment in the current reproduction by thebreeders will potentially increase their chanceof surviving to the future breeding seasons andthus contribute to their lifetime success (Bearset al., 2009). The “slow life history” performedby high altitude birds also highlights a conser-

Ardeola 56(2), 2009, 173-187


vation priority for the ecosystem in harsher en-vironments.

ACKNOWLEDGEMENTS.—We are grateful to N. F.Liu for his advice and to B. Du, H. J. Zhang, M. Yangand H.Y. Mu for their assistance in the field. Thiswork was conducted in the Field Research Stationfor Tibetan Wildlife, which is jointly administeredby Wuhan University and Tibet University. Finan-cial support was provided by the National SciencesFoundation of China (grants 30425036 and30670337).

BIBLIOGRAPHY

BADYAEV, A. V. and GHALAMBOR, C. K. 2001. Evo-lution of life histories along elevational gradients:tradeoff between parental care and fecundity. Ecol-ogy, 82: 2948-2960.

BADYAEV, A. V. 1997. Avian life history variationalong altitudinal gradients: an example with car-dueline finches. Oecologia, 111: 365-374.

BEARS, H., MARTIN, K. and WHITE, G. C. 2009.Breeding in high-elevation habitat results in shiftto slower life-history strategy within a singlespecies. Journal of Animal Ecology, 78: 365-375.


Ardeola 56(2), 2009, 173-187

184

TABLE 4

A comparison of nesting parameters of the white-rumped snowfinch at three different altitudes. Shownare means ± SD, followed by sample sizes in parentheses and ranges.[Comparativa de los parámetros reproductivos del gorrión alpino de Mandelli en tres altitudes diferen-tes. Se indican las medias ± ds, seguidos de los tamaños de muestra entre paréntesis y el rango.]

Nesting parameter South North NorthGuansu Qinghai Tibet

Latitude (°N) 34.2 37.6 30.5Altitude (m) 3,600 3,300 43,00Annual mean temperature (°C) 1.2 -1.4 1.3Annual total precipitation (mm) 626 484 481Population density 15 14 5

(pairs per 100 ha)Body size (body mass/tarsus) 1.7 ± 0.2 (69), 1.1-2.1 – 1.6 ± 0.1 (15), 1.4-1.9Duration of egg-laying period (d) early April- late April- early May-

late June mid-July late July% double-brooded pairs 9 (147) – 14 (14)No. of broods produced annually 1.1 – 1.1Egg volume 7.3 ± 0.3 (6), 7.1-7.9 7.0 (4) 7.0 ± 0.5 (4), 6.6-7.5

(length x width2, mm3)Clutch size 4.7 ± 1.5 (7), 2-6 4.5 ± 0.3 (8), 3-6 3.3 ± 0.6 (3), 3-4Incubation period (d) 12.7 ± 1.6 (34), 9-15 10-12 (6) 16.5 ± 0.7 (2), 15-16Female feeding trip per h 6.5 ± 5.1 (21), 0-17 – 7.7 ± 3.2 (6), 0-18Male feeding trip per h 6.1 ± 7.6 (21), 0-35 – 6.7 ± 4.9 (6), 0-18Nestling period (d) 21.3 ± 2.0 (16), 18-24 15-16 (6) 19 (1)Brood size at fledging 3.5 ± 0.8 (67), 2-6 3.5 (6), 2-6 2.9 ± 0.3 (10), 2-3Annual productivity 3.9 – 3.2

(brood size x brood number)% nests with ≥ 1 fledgling 66 (190) – 67 (15)Ref. This study Zhang, 1982; Lu et al., 2009

Zhang & Deng, 1986

BEISSINGER, S. R., COOK, M. I. and ARENDT, W. J.2005. The ‘‘shelf life’’ of bird eggs: testing eggviability using a tropical climate gradient. Ecol-ogy, 86: 2164-2175.

BLACKBURN, T. 1991. An interspecific relationshipbetween egg size and clutch size in birds. Auk,108: 973-977.

CLARK, R. G. and SHUTLER, D. 1999. Avian habi-tat selection: Pattern from process in nest-site useby ducks. Ecology, 80: 272-287.

CONWAY, C. J. and MARTIN, T. E. 2000. Evolution ofpasserine incubation behavior: influence of food,temperature, and nest predation. Evolution, 54:670-685.

CRAMP, S. and PERRINS, C. M. 1994. The Birds ofthe Western Palearctic, Vol. IX: Buntings and NewWorld Warblers. Oxford University Press. Oxford.

DU, B. and LU, X. 2009. Bi-parental vs. cooperativebreeding in a passerine: fitness-maximizing strate-gies of males in response to risk of extra-pair pa-ternity? Molecular Ecology, 18: 3929-3939.

GJERDRUM, C., ELPHICK, C. S. and RUBEGA, M. 2005.Nest site selection and nesting success in satmarshbreeding sparrows: the importance of nest habi-tat, timing, and study site differences. Condor,107: 849-862.

GODARD, R. D., WILSON, C. M., FRICK, J. W., SIEGEL,P. B. and BOWERS, B. B. 2007. The effects of ex-posure and microbes on hatchability of eggs inopen-cup and cavity nests. Journal of Avian Bi-ology, 38: 709-716.

HALUPKA, K. 1994. Incubation feeding in meadowpipit Anthus pratensis affects female time budg-et. Journal of Avian Biology, 25: 251-253.

JOHNSON, L. S., OSTLIND, E., BRUBAKER, J. L. andBALENGER, S. L. 2006. Changes in egg size andclutch size with elevation in a Wyoming popula-tion of mountain bluebirds. Condor, 108: 591-600.

KLOMP, H. 1970. The determination of clutch-sizein birds. Ardea, 58: 1-124.

KREMENTZ, D. G. and HANDFORD, P. 1984. Doesavian clutch size increase with altitude? Oikos,43: 256-259.

LACK, D. 1948. The significance of clutch size, PartIII. Ibis, 90: 24-50.

LACK, D. 1968. Ecological adaptations for breed-ing in birds. Methuen. London.

LANDMANN, A. and WINDING, N. 1993. Niche seg-regation in high-altitude Himalayan chats (Aves,

Turdidae): does morphology match ecology? Oe-cologia, 95: 506-519.

LANDMANN, A. and WINDING, N. 1995a. Adaptiveradiation and resource partitioning in Himalayanhigh-altitude finches. Zoology, 99: 8-20.

LANDMANN, A. and WINDING, N. 1995B. Guild or-ganization and morphology of high-altitudegranivorous and insectorous birds: convergentevolution in an extreme environment. Oikos,73: 237-250.

LI, M. C., ZHAO, L., LI, L. X., ZHANG, X. A. andYI,X. F. 2003. Effect of nestling positions in nestson the parental feeding rates in robin accentor(Prunella rubeculoides). Chinese Journal of Zo-ology, 38: 28-32.

LIFJELD, J. T. and SLAGSVOLD, T. 1986. The functionof courtship feeding during incubation in the piedflycatcher Ficedula hypoleuca. Animal Behav-iour, 34: 1441-1453.

LIFJELD, J. T., SLAGSVOLD,T. and STENMARK, G. 1987.Allocation of incubation feeding in a polygynousmating system: a study on pied flycatchers Ficedu-la hypoleuca. Animal Behaviour, 35: 1663-1669.

LIMA, S. L. 1987. Distance to cover, visual obstruc-tions, and vigilance in house sparrows. Behav-iour, 102: 231-237.

LU, X. 2005. Reproductive ecology of blackbirds(Turdus merula maximus) in a high-altitude loca-tion, Tibet. Journal of Ornithology, 146: 72-78.

LU, X., KE, D. H., ZENG, X. H. and YU, T. L. 2009.Reproductive ecology of two sympatric Tibetansnowfinch species at the edge of their altitudi-nal range: response to more stressful environ-ments. Journal of Arid Environments, 73: 1103-1108.

LYON, B. E. and MONTGOMERIE, R. D. 1987. Eco-logical correlates of incubation feeding: A com-parative study of high arctic finches. Ecology, 68:713-722.

MARTIN, K. and WIEBE, K. L. 2004. Coping mech-anisms of alpine and arctic breeding birds: ex-treme weather and limitations to reproductive re-silience. Integrative Comparative Biology, 44:177-185.

MARTIN, T. E. and GHALAMBOR, C. K. 1999. Maleshelping females during incubation. I. Requiredby microclimate or constrained by nest predation?American Naturalist, 153: 131-139.

Ardeola 56(2), 2009, 173-187


MARTIN, T. E. and LI, P. 1992. Life history traits ofopen- versus cavity-nesting birds. Ecology, 73:579-592.

MARTIN, T. E. 1993. Evolutionary determinants ofclutch size in cavity-nesting birds: nest predationor limited breeding opportunities? American Nat-uralist, 142: 937-946.

MARTIN, T. E. 2008. Egg size variation among trop-ical and temperate songbirds: An embryonic tem-perature hypothesis. Proceeding of National Acad-emy of Sciences of United States of America, 105:9268-9271.

MU, H.Y., LIU, N. F. andYANG, M. 2008. Breedingof the black redstart Phoenicurus ochruros ru-fiventris in the southeastern Qinghai-Tibetanplateau. Acta Zoologica Sinica, 54: 201-208.

NILSSON, J. A. and SMITH, H. G. 1988. Incubationfeeding as a tactic for early hatching. Animal Be-haviour, 36: 641-647.

PARTRIDGE, L. and HARVEY, P. H. 1988. The ecolog-ical context of life history evolution. Science, 241:1449-1455.

PERRINS, C. M. 1970. The timing of bird’s breedingseasons. Ibis, 112: 242-255.

PIANKA, E. R. 1970. On r- and k-selection. Ameri-can Naturalist, 104: 592-597.

QU, Y. H., LEI, F. M. and YIN, Z. H. 2002. Habitatdistribution of snow finches (Montifringilla) inChina. Acta Zoologica Sinica, 48: 471-479.

QU, Y. H., LEI, F. M. and YIN, Z. H. 2006. Molec-ular phylogenetic relationship of snow finchcomplex (genera Montifringilla, Pyrgilauda,and Onychostruthus) from the Tibetan plateau.Molecular Phylogenetics and Evolution, 40: 218-226.

RHYMER, J. M. 1988. The effect of egg size variabil-ity on thermoregulation of mallard (Anasplatyrhynchos) offspring and its implications forsurvival. Oecologia, 75: 20-24.

SIBLEY, C. G. and MONROE, B. L. 1990. A worldchecklist of birds. Yale University Press, NewHaven.

SLAGSVOLD, T. 1982. Clutch size variation inbirds: the nest predation hypothesis. Oecologia,54: 159-169.

SMITH, A. T. and FOGGIN, J. M. 1999. The plateaupika Ochotona curzoniae is a keystone speciesfor biodiversity on the Tibetan Plateau. AnimalConservation, 2: 235-240.

SMITH, H. G. and BRUUN, M. 1998. The effect of eggsize and habitat on starling nestling growth andsurvival. Oecologia, 115: 59-63.

STOLESON, S. H. and BEISSINGER, S. R. 1995. Hatch-ing asynchrony and the onset of incubation inbirds, revisited: when is the critical period. Cur-rent Ornithology, 12: 191-270.

VAURIE, C. 1959. The birds of the Palearctiv fauna:Passeriformes. Vol. 1. Witherby, London.

WANG, C. T., LONG, R. J., WANG, Q. J., DING, L. M.and WANG, M. P. 2007. Effects of altitude onplant-species diversity and productivity in analpine meadow, Qinghai-Tibetan plateau. Aus-tralian Journal Botany, 55: 110-117.

WHITE, F. N. and KINNEY, J. L. 1974. Avian incu-bation. Science, 198: 107-115.

WILLIAMS, T. D. 1994. Intraspecific variation in eggsize and egg composition in birds: effect on off-spring fitness. Biological Reviews, 68: 35-59.

WRIGHT, J. 1998. Paternity and parental care. In, T.R. Birkhead and A. P. Moller (Eds.): Sperm com-petition and sexual selection, pp. 117-145. Aca-demic Press. London.

WU, S. H., YIN, Y. H., ZHENG, D. and YANG, Q. Y.2005. Climate changes in the Tibetan plateau dur-ing the last three decades. Acta Geographica Sini-ca, 60: 3-11.

ZENG, X. H. 2008. Study on breeding biology ofwhite-rumped snowfinches (Montifringillataczanowskii) in northeastern Tibetan plateau.Ph.D. thesis, Wuhan University. Wuhan..

ZENG, X. H. and LU, X. 2009. Interspecific domi-nance and asymmetric competition with respectto nesting habitats between two snowfinch speciesin a high-altitude extreme environment. Ecolog-ical Research, 24: 607-616.

ZHANG, X. A. and DENG, H. L. 1986. Seasonal vari-ations of the avian community structure in alpinemeadow, northern Qinghai. Acta Zoologica Sini-ca, 32: 180-188.

ZHANG, X. A. 1982. Studies on breeding biology of 10species of passerine birds in alpine meadow, northernQinghai. Acta Zoologica Sinica, 28: 190-199.

ZHANG, X. A., ZHAO, L. and LIU, Z. H. 2000.Breeding productivity of passerine birds in alpinemeadow in northern Qinghai. Acta ZoologicaSinica, 46: 265-270.

ZHAO, L., LIU, Z. H., ZHANG, X. A., YI, X. F. and LI,M. C. 2003. Feeding nestling in twite Acanthis


Ardeola 56(2), 2009, 173-187

186

flavirostris at the Haibei alpine meadow, Qing-hai. Zoological Research Sinica, 24: 137-139.

ZHAO, L., ZHANG, X. A. and LI, L. X. 2002. Incu-bating behavior of the horned lark (Eremophilaalpestris) and small skylark (Alauda gulgula).Acta Zoologica Sinica, 48: 695-699.

ZHENG, Z. X. 1983. The avifauna of Tibet. SciencePress, Beijing, pp. 312-316.

ZHENG, Z. X. 2000. A complete checklist of speciesand subspecies of the Chinese birds. SciencePress. Beijing.

[Recibido: 05-11-2008][Aceptado: 01-06-2009]

Ardeola 56(2), 2009, 173-187


breeding ecology of a burrow-nesting passerine, the … · 2018. 6. 11. · this study occurred in...

Documents