DECEMBER 2004 SHORT COMMUNICATIONS 367 j RaptorRes. 38(4):367-371 ¸ 2004 The Raptor ResearchFoundation, Inc.

NEST PROVISIONINCOF THE ORIENTALHONEY-BUZZARD ( PTILORHYNCUS) 1N NORTHERN TAIWAN

KUANG-YING HUANG YangmingshanNational Park Headquarters,I&ngmingshan, 7aipei, 112, Taiwan,R. O.C. and Instituteof Ecologyand EvolutionaryBiology, National Taiwan University,Taipei, 106, Taiwan,R.O.C.

YAO-SUNG LIN Instituteof Ecologyand EvolutionaryBiology, National Taiwan University,Taipei, 106, Taiwan,R.O.C.

LUCIA LIU SEVERINGHAUS 1 Instituteof Zoology,Academia Sinica, Taipei,115, Taiwan,R. O.C.

KEYWORDS: Oriental Honey-buzzard; Pernis ptilorhyncus; the color of the seal on cells containing pupae. Obser- nestprovisioning; paper wasps; Polistes; Parapolybia; Taiwan. vations were made from 12 July-19 August, the day be- fore the nestling fledged. Because it was impossible to determine the exact sizes Raptors in the genus Pernishave a unique diet consist- of the wasp nestsfrom the videotapesdue to filming an- lng primarily of the larvae, pupae, and adults of social gles,we collected empty waspnests discarded under the (Clark 1994, Orta 1994, Bijlsma 1999, Ga- honey-buzzardnest for speciesidentification and count- mauf 1999). The European Honey-buzzard(P. apivorus) ed the number of cells per waspnest. Basedon the sizes has been studied in some detail (Kostrzewa1987a, 1987b, of these wasp nests,we categorized all the wasp nestsin 1987c,Steiner 1992, Saporettiet al. 1994,Selas 1997, Van the videotapesinto small, medium, or large classes(Table Manen 2000), but the biology of the Oriental Honey- 1). buzzard (P. ptilorhyncus)has not been studied in depth To understand the relationship between wasp activity (Clark 1994, Orta 1994, Morioka et al. 1995). and prey capture rate, we identified the paper waspsac- tive in July and August.We searchedfor waspnests along Based on our monthly raptor surveysin northern Tai- three trails in the study area through wooded areaswith wan's YangmingshanNational Park (25ø10'N, 121ø33'E) small cabins,each 1 km in length. We scannedthe veg- between 1993 and 2003, the Oriental Honey-buzzardwas etation from canopy to the shrub layer and checked a common spring and autumn migrant, a rare winter vis- buildings carefully. Each transect line was searched at itor, and an uncommon summer resident. We found one least twice to ensure the discoveryof all waspnests. For Oriental Honey-buzzardnest in 1994 and one in 1999. each wasp nest found, we measured height above This paper reports the composition,seasonal variation, ground, its length and width, recorded the number of and relative importance of the prey speciesprovisioned cells, and describedits shape.We collected one actively- to the nest in 1999 and compares the male and female used nest for each speciesfound in order to obtain the proportion of cells occupied by eggs,different larval in- contributionsto the nestling. starsand pupae, and measured the massof larvae at each instar. METHODS Biomass per wasp nest was calculated with the follow- We constructed a hide eye-level with the nest on a ing equation:Biomass = the number of cells/nest X pro- steepslope about 30 m away.We monitored the nest pro- portion of cellsoccupied X the mean biomass/larva. The wsioning of the parents and recorded the time and the number of cellsfound on each wasp nest was related to gender each time an adult returned to the nest. The size (Table 1). We used the wasp nestswe collected as male could be distinguishedbased on an orange-brown standardsto determine cell occupancyand larval mass iris and broader dark tail bands, while the female has a Biomassestimates of reptiles and frogs were based on the yellow iris and narrower dark tail bands (Morioka et al. mean massof >10 individualsper speciescaught in the 1995). We simultaneouslyvideotaped the nest-provision- study area. lng events.From these videotapes,we identified prey by comparing these with reference specimensin terms of RESULTS structure, shape, color, and size of the wasp nests, the color and placement of the stem of the wasp nests,and Food Composition and Seasonality.We observed the honey-buzzardnest for 26 d (204.7 hr) and recorded 123 food items delivered by parents. Among these, 78.9% 1 Correspondingauthor's e-mail address:zobbowl@gate. were complete wasp nests (N = 97), 16.3% were Swin- slnica.edu.tw hoe's brown frogs (Rana swinhoana;N = 20), and 4.9% 368 SHORT COMMUNICATIONS VOL. 38, NO. 4

Table 1. Waspnest-size classes and their cell numbers. Table 2. Relative biomass of different prey types brought to the Oriental Honey-buzzard nest in northern Taiwan. SPECIES SIZE RANK CELL NUMBER

Polistis tenelaiocosus Small <39 TOTAL Medium 40-69 SPECIES BIOMASS(g) PERCENT Large > 70 Polistisrothneyi Small <119 Polistis tenebriocosus 1003.00 31.59 Medium 120-219 Po. rothneyi 689.34 21.71 Large >220 Po.•gas 244.50 7.70 Polistisg igas Small 10-19 Parapolybiavaria 90.84 2.86 Medium 20--29 Unidentified nests a 611.16 19.25 Large >30 Frogs 500.00 15.75 Polistissp. Medium 780 Lizards 36.00 1.13 Parapolybiavaria Total 3174.84 100.00 Small < 179 a Eithcr Po. tenebriocosusor Po. rothneyi.We calculated the biomass Medium 180-349 by using the mean massand mean cell occupancyof the two Large >350 species. Unidentified wasp comb Small 60 ( Po. tenelaiocosusor Medium 80 Po. rothneyi) Large 100 83.1% (Table 2). Frogswere delivered in July and early August, and lizards were delivered in July only. By mid- August, honey-buzzardsprovisioned only paper wasps were yellow-mouthedjapaluralizards (Japalurapolygonata (Fig. l). The patterns of seasonalvariation were similar xanthostoma;N = 6). All 97 waspnests belonged to paper by prey frequencyand by biomass.The biomassdelivered wasps(, ), but two belonged to an un- to the nest per hour of observationfluctuated between known speciesand 24 could not be distinguishedbe- 5-40 g throughout the nestling period except on the tween Po. tenelaiocosusand Po. rothneyibecause either the third d before fledging (Fig. 2). We did not monitor the nestlingblocked the cameraor the speedof deliverywas nest on 18 August.and so were unable to determine if too rapid. Among prey itemsthat could be identified, Po. this increased rate of prey delivery took place two con- tenelaiocosusnests (N = 36) constituted29.3%, Po.rothneyi secutivedays betbre tledging. 13% (N = 16), Po. •gas 9.8% (N = 12), Parapolybiavaria Nest Height Distribution. The 29 paper 5.7% (N = 7), and Polistissp. 1.6% (N = 2). The ti'e- waspsnests we found along trails hung from vegetation quencydistribution of wasp nestsbrought back to the (N = 10) or eaves (N = 19) from 0.5-11.5 m above the nestlingwas not different from those found along our ground. More than 86% were between0.5-4 m high, the transect lines (nests recorded: 29, Po. tenebriocosus= 21, remaining four nestswere above 6 m (3 Po. te.nebriocosus Po. rothneyi= 3, Po. gigas= 2, and Pa. varia = 3, Polistis and I Po. rothneyi). Sexual Differences in Contribution. The male made sp. = 0, X• = 5.657, df = 4, P> 0.05). The body sizesof thesefive speciesof paper waspsvar- ied from the world's largestpaper wasp (Po. gigag4.5 cm for adult males) to a new species,Polistis sp. (1.3 cm). By Frequency By Biomass The colonysizes of thesewasps also varied from 12 cells in a Po. gigasnest to more than 400 cells in a Pa. varia nest. Based on biomass estimates from the nests we col- lected, we found that the pupae and the fourth and fifth •Pa_ varfa instars of Po. tenebriocosus,Po. rothneyi,Po. gigas,and Pa. varia constituted 93.4%, 95.4%, 95.7%, and 87.6% of the total biomassof a nest, and occupied 44%, 45%, 56%, o ,11,Eh,I,• '111,111•ß /•BUnidentified n•ts and 39.6% of the cells, respectively.We did not find any nests of the new Polistissp. to obtain larva/pupa mass measurements. Because nests of this species were brought back only twiceduring the entire studyperiod, we decided not to include this speciesin our biomass calculations. Figure 1. Diet of Oriental Honey-buzzardnestling based Consideringthe cumulativebiomass of all prey types on the frequency of prey deliveriesto the nest. Paper delivered to the honey-buzzardnest, frogs and lizards to- waspsin diet included:Polistis tenebriocosus, Po.rothneyi, Po. gether made up 16.9%, while Polistinaewasps made up gigas,and Parapolybiavaria. DECEMBER 2004 SHORT COMMUNICATIONS 369

enccd by the accessibilityof prey and its energy content in relation to the handling cost. Hornets are aggressive and usually defend their combs vigorously (Evans and Eberhard 1970, Kuo and Ych 1987). Ranking the aggres- sivenessof waspsinto five classes(1 being most aggres- sive), Po. tenebriocosusand Po. •gas would in be class.5, Po. rothneyiand Pa. varia in class3, while the Vespaspecms

12'141618202224262830 1 3 5 7 9 1113151719 would be in classes1-3 (Kuo and Ych 1987). Although July August the stomachcontents of European Honey-buzzardscon- tained small numbers of hornets (Loskutova 1985), and adult Oriental Honey-buzzards probably consume hor- Figure 2. Biomassdelivered to an Oriental Honey-buz- nets, preying on hornet nests no doubt demands a high zard nest in northern Taiwan per hour of observation. energy cost. Specifically,honey-buzzards would need to The nestling fledged on 20 August. The mean biomass evade the attack of a large number of hornets and would delivered per hour for each 10-d period is given at the have a high risk of iqjury. top of the histogram. Wild are common in Taiwan, but most nest •n rock crevices and tree cavities (Kuo and Ych 1987). Pol- istinae nests in Taiwan always hang by a stem, which 49.6% of the visits and the female 29.3%; the sex was makes them easyfor honey-buzzardsto remove in flight uncertain in the remaining visits.Among the biomassde- When paper waspsare abundant, there should be little hveredby adultsof knownsex, the male contributed56% incentive for a honey-buzzardto open logs or remove and the female 44% in July and in early August.After 9 rocks to access a nest. August, female contribution ceasedcompletely. The dif- Seasonal Variation in Prey Composition. Paper wasps ference in biomass contribution between sexes across in Taiwan generally establishcolonies in late April or t•me periodswas significant (X 9 = 305.31,P < 0.0001). May, and colony expansion usually occurs in June and Even if all the unknown feedings were made by the fe- July,followed by a mating period in July or Augustbefore male, the male still would have contributed more biomass they enter the dormant wintering stage,when breeding than the female during the final 10 d before fledging. and foraging activitiescease (Kuo and Yeh 1987, Lu et al. 1992). Based on this chronology,wasp nestswould be DISCUSSION small in the early part of the breeding season(July). Dur- Prey Choice. Oriental Honey-buzzardscaptured prey ing this period, the Oriental Honey-buzzardsdelivered that were on the ground, such as fi-ogsin the shrub layer, wasp nests to the nestling and supplemented the nest- or in the sub-canopypaper wasp nests.The pair we stud- ling's diet with frogs and lizards.By mid-August,although md in Yangmingshanprimarily brought Polistesnests as frogs and lizards were still common, wasp colonieswere food fbr their young. Among known wasp prey, the fre- large and the honey-buzzardsdelivered only paper wasp quency of different speciesof waspnests they brought to nests.European Honey-buzzardsalso foraged almost en- the nestling was proportional to those available in the tirely on wasp nests when waspswere available (Marun environment. However, they ignored the nests of the 1992, Ferguson-Leeand Christie 2001). small paper wasp, Po. takasagonus,even though these European Honey-buzzardsfind wasp nestsby watching nestswere as common as the Po. tenelniocosusnests along the insectsreturn from foraging trips (Grigor'yev et al our transect lines. A colony of Po. takasagonuswas con- 1977, Martin 1992, Ferguson-Leeand Christie 2001). Wc structing a nestjust below the honey-buzzardnest, but do not know if Oriental Honey-buzzardscould determine the honey-buzzardsnever showedinterest in it. The bio- whether a wasp was departing fi•om or returning to •ts massof the largestPo. takasagonusnest we found weighed nest. However, by following a flying wasp,honey-buzzards lessthan 9 g, lessthan the smallestnest brought back by could either find the waspforaging or come upon a nest parents (9.91 g). There may be a minimum-sizethresh- Timing of Breeding. If the two nestswe tbund are typ- old for a waspnest to be energeticallyprofitable fbr hon- ical for this species, the Oriental Honey-buzzard has a ey-buzzards. much later breeding seasonthan the other speciesof Another potential prey are l•spa hornets (Vcspidae, raptors in Taiwan. The hatching of eggs in July appears Vcspinae), which are large, conspicuous,and usually to be timed with the increase of paper wasp colonies •n number by the hundredsper colony.The nestsof some our study area. The delayed onset of its breeding season speciesare built on high branchesand can be as large as could result from the unavailabilityof wasp nestsearlier 60 cm in diameter (M.C. Kuo pets. comm.). Hornets and in the spring. Wasp abundance has been known to influ- wild bees (Apidae) were activewithin the home range of ence the breeding successof European Honey-buzzards the honey-buzzardpair, but the nestsof these families (Kostrzewa1987c, Saporetti et al. 1994, Steiner 2000). were never delivered to the nestling. Sexual Differences in Provisioning.From mid-Julyto The honey-buzzards'food choice was most likely influ- earlyAugust, the female Oriental Honey-buzzardcontnb- 370 SHORT COMMUNI(LATIONS VOL. 38, NO. 4 uted more than 30% of the biomass delivered to the nest- lier draft of this paper; and Mr. Wayne Hsu for English ling, and the male at least 40%. After 9 August, the re- editing. male's contribution ceased completely even though she LITERATURE CITED remained in the vicinity of the nest. Using a modeling analysis,Brodin et al. (2003) showedthat whether a fe- BIJLSMA,R.G. 1999. Do honey buzzards Perhisapivorus male raptor assistedwith hunting for the young late in produce pellets?Limosa 72:99-103. the nestling period depended on the hunting successof BRODIN,A., K.I. JOENSSON,AND N. HOI.MGREN.2003. Op- the male, environmental conditions, and the energy de- timal energy allocation and behaviour in female rap- mands of the young. Becausethe pair of honey-buzzards torial during the nestling period. Ecoscience10 we monitored had only one nestling, perhaps the male 140-150. alone could provide sufficient prey for the young (re- CIAm½,W.S. 1994. Barred Honey-buzzardßPage 112 inJ ported clutch size for Oriental Honey-buzzard is two del Hoyo, A. Elliott, andJ. Sargatal [EDS.],Handbook eggs;Sung et al. 1991). of the birds of the world. Vol. 2. Lynx Edicions, Bar- Our study advanced what was known about Oriental celona, Spainß Honey-buzzard.We found that adults primarily brought EVANS,H.E. ANDM.J. EBERHARD.1970. The wasps.Univ. paper waspsas prey for their nestling, and the frequency Michigan Press,Ann Arbor, MI U.S.A. of each speciesof wasp nest brought back reflected prey FERGUSON-LEE,J. AND D. CHRISTIE.2001. Raptors of the availability.Low energetic profitability most likely made world. Houghton Mifflin Company, New York, NY some speciesof wasp nestsundesirable. In addition, our U.S.A. results from one nest showed that the female delivered GAMAUF,A. 1999. Is the European Honey-buzzard (Perms food less often and contributed less biomass to the nest- apivorus)a feeding specialist?The influence of' social ling than the male. Hymenoptera on habitat selection and home range size. Egretta42:57-85. RESUMEN.--Seconoce muy poco sobre la ecologqay el GRIC,OR'YEV, N.D., V.A. POPOV, AND Y.K. POPOV. 1977. comportamientode Perhisptilorhyncus. Con base en cen- Otryad sokoloobraznye.Pages 76-116 in V.A. Popov sosrealizados entre 1993 y 2003, se determin6 que esta [ED.], Ptitsy volzhsko-kamskogokraya. Nauka Press, especie es un visitante poco com6n durante el verano en Moscow, Russia. ¾angmingshan,Taipei, Taiwan. Encontramosun nido en Kuo, M.S. ANDW.H. YEH. 1987. Ecologicaland natural 1994 y otto en 1999. A trav6s de observacionesdirectas history research for Taiwan Vcspidae (III): l•spa, Pol- y de grabacionesde video realizadasen 1999, registramos lsres,Parapolybia, Ropalidia. Ann. Res.Rep. of Chai-D las presas11evadas al nido durante 26 dfas, entre el 12 de Ag•l Coll.16:77-104. julio y el 19 de agosto (N = 204.7 hr, N = 123 presas). KOSTRZEWA,A. 1987a. Territorial behavior competition Nuestros resultadosrevelaron que el 78.9% (83.7% en and nest use of three tree-breedingraptors accipitres t6rminos de biomasa) de los ftems alimenticios rueton J. Ornithol.128:495-496. mdos de avispas,el 16.2% (15.3% en biomasa) rueton ß 1987b. Quantitative analysesof nest habitat sep- ranasy el 4.9% (1.1% en biomasa)rueton lagartijas.Cin- aration in the Buteobuteo, goshawk co especiesde avispasque construyennidos de papel rue- Accipitergentiles, and honey buzzard Perhisapivorus. J ton identificadas:Polistes tenebriocosus, Po. rothneyi,Po. gi- Ornithol. 128:209-230. gas,Parapolybia varia y Po. sp. Las ranasy lagartijasfheron ß 1987c. The effect of weather on densityand re- registradass61o entre el 12 de julio y el 10 de agosto.La production successin honey buzzard Pernisapivorus dmta de la crla de P ptilorhyncusreficj6 la fhuna disponi- Vb•elwarte34:33-46. ble de avispasy el ciclo anual de 6stasen el •rea de es- ß1996. A comparativestudy of nest-siteoccupancy tudio. [,os machos y hembras no contribuyeron igual- and breeding performance as indicators for nesting- mente a alimentar a su crfa. Las hembras dejaron de habitat quality in three European raptor speciesßEthol. 11evaralimento diez dfas antes de que el pich6n aban- Ecol. Evol. 8:1-18. donara el nido. LOSKUTOW%N.M. 1985. Khishchnyeptitsy i sovyBashkir- [Traducci6n del equipo editorial] skogozapovednika. Pages 45-58 in V.M. Galushin and

ACKNOWI,FDGMENTS V.G. Krever [EDS.], Khishchnyepfitsy i sovyv zapov- ednikakh RSFSR. CNIL Glavokhoty Press, Moscow, We wish to thank Chung Kun-yen, Hsieh Shu-Shin, Russia. Huang Hui-Tzu, Huang Yung-Fen, Lee Tien-Fu, Liang Lu, S.S.,J.T. CHAO,AND L.L. LEFß.1992. Colony cycle of Chieh-Te, Tseng Wen-Shiu, Jack Yu, and Raptor Research Polistesjadwigae Dalla Torre (Hymenoptera: Vcspidae) Group of Taiwan for help in field data collection;Dr.J.T. Chao for helping to identify paper wasps;Prof. M.C. Kuo in northern Taiwan. Chin.J. Entomol.12:171-181. for information on waspnatural history;Drs. Ian Newton, MARTIN,B.P. 1992. Birds of prey of the British Isles.David N•gel Collar, R. Yosef; and two anonymous reviewersfor & Charles, Newton Abbot, Devon, U.K. their valuable suggestionsthat greatly improved an ear- MoPdoits, T., T. KANOUCTI,W. KAWATA,AND N. YAMAGATA DECEMBER2004 SHORT COMMUNICATIONS 371

1995. Birds of prey in Japan. Okumura Printing, To- --. 2000. Forest ti-agmentation,competition, and ch- kyo, Japan. matic dependence in the honey buzzard (Pernisap,- ORTA,J. 1994. Western Honey-buzzardand CrestedHon- vorus).J. Ornithol.141:68-76. ey-buzzard.Pages 111-112 in J. del Hoyo, A. Elliott, SUNG,Y.J., W.J. Lo, M. WEI, AND X.L. CHANG.1991. Pre- and J. Sargatal [EDs.], Handbook of the birds of the liminary studyon the breeding biology of the Orien- world. Vol. 2. Lynx Edicions,Barcelona, Spain. tal Honey-buzzard(Pernis ptilorhyncus). Science Print- SAPORETTI,E, W. GUENZANI,AND P. PAVAN.1994. Density, ing, Beijing, China. habitat,and breedingsuccess of diurnal raptorsin the VAN MANEN, W. 2000. Reproductive strategy of honey Prealpsof NW Italy.Riv. Ital. Ornitol.63:145-173. buzzardsPernis apivorus in the northern Netherlands. SELAS,V. 1997. Nest-siteselection by four syrupatticfbrest Limosa 73:81-86. raptorsin southernNorway. J. RaptorRes. 31:16-25. STEINER,H. 1992. The diurnal raptor community of a farmland area in upper Austria. Egretta35:96-110. Received 5 January 2004; accepted 3 September 2004

j RaptorRes. 38(4):371-374 ¸ 2004 The Raptor ResearchFoundation, Inc.

WINTER DIET OF THE GREATERSPOTTED (AQUILACLANGA) IN THE AMVRAKIKOS WETLANDS, GREECE

HARALAMBOS ALIVIZATOS 1 4 Zaliki Str., GR-115 24 Athens, Greece

DIMITRIS PAPANDROPOULOS 21 Zaimi Str., GR-26 500 Rion, Greece

STAMATIS ZOGARIS NationalCenter for MarineResearch, Institute of Inland Waters,P O. Box 712, 19 013 AnavyssosAttiki, Greece

KEYWORDS: GreaterSpotted Eagle,, Aquila clanga;diet;, win- international cooperation, monitoring, and research ter, wetland;Amvrakikos; ¸reece. (Meyburg et al. 2001). The biology of the Greater Spot- ted Eagle has not been examined to a great extent; ad- The Greater SpottedEagle (Aquilaclanga) is a globally- ditionally, its diet has been examined almost exclusively threatened raptor, which breeds from Eastern to during the breeding season(e.g., Priklonsky 1960, Gal- the Pacific coast of the northern Far East and winters ushin 1962, Pankin 1972, Ivanovsky1996). Few studiesof locally in southern Europe, , the Middle East, and any kind have been conducted in the winter quartersof sub-SaharanAfrica as thr south as Uganda and Kenya this species(Moltoni 1943,Francois 1992, Qingxia 1996) (Tucker and Heath 1994). The main reasonstbr its de- Although an important population of Greater Spotted cline are habitat destruction and degradation (in both Eagleswinters in the extensivewetlands of northern and forests,where the speciesnests, and wetlands,where it central Greece (45-85 individuals), up to now it has re- forages),disturbance during the breedingseason, illegal ceived very little attention (Hallmann 1989, Handrinos shooting (mainly in migration), and to a lesserextent, and Akriotis 1997). Here, we present the results of an nest robbing (Tucker and Heath 1994, Meyburg et al. examination of Greater Spotted Eaglesat a key wintering 2001). The primary proposed conservationmeasures in- site, the Amvrakikos wetlands, western Greece, where up clude the establishmentof protected areasin the breed- to 12 individualswinter each year. mg habitat of the species,preservation of a mosaic of STUDY AREA AND METHODS breeding-feedinghabitat, protection of wetlands,avoid- ance of disturbanceduring the breeding seasonwithin Our studyarea was in the Amvrakikoswetlands, west- 300 m of nests, as well as improvement of legislation, ern Greece (38ø59'-39ø11'N, 20ø44'-21ø07'E). Amvrak•- kos is a Ramsar Wetland, a Special Protection Area, and proposedNational Park. It is one of the largestwetlands E-mail address:[email protected] in Greececovering 220 kma includingriver deltas,coastal