j Raptor Res. 28(4):236-241 ¸ 1994 The Raptor ResearchFoundation, Inc.

EFFECTS OF RAPTORS ON THE ACTIVITY OF

PETER N. FERNS AND SHELLEY A. HINSLEY Schoolof Pure and Applied Biology,University of Wales,College of Cardiff, P.O. Box 915, Cardiff,CFI 3TL, UnitedKingdom

ABSTR•CT.--Raptorsaccounted for 55% of the disturbanceincurred by two speciesof sandgrouse(Pterocles alchataand P. orientalis)in breedinghabitat in La Mancha, Spain, during springand summer.The main speciesof raptors were the golden eagle (Aquila chrysaetos)in spring and Montagu's harrier (Circus pygargus)in summer.During the breedingseason, Montagu's harriers carried out the majority of their foraging at thosetimes of day when male sandgrousecollected water for their chicks.This presumably enabledthe harriers to locate chicksmore easily. Sandgrouselost no more than 0.5 hr of feedingtime per day as a result of disturbanceby raptors, and yet were still able to rest for at least 3 hr a day at timeswhen they couldhave been feeding. Predators as a whole were probablythe major factorresponsible for the different dispersionpatterns adopted by sandgrouseat different times of year. KEY WORDS: goldeneagle; Montagu's harrier; Pteroclesalchata; Pteroclesorientalis; raptor disturbance; sandgrouse;vigilance.

RESUMEN.--Avesrapaces fueron responsablespor 55% de las perturbacionessufridas por dos especies de gangas(Pterocles alchata and P. orientalis)en susareas de reproducci6nen la Mancha, Espafia,durante la primaveray el verano.Las especiesde avesde rapifia mils prominentesfueron el figuila real (Aquila chrysaetos)en la primaveray el aguiluchocenizo (Circus pygargus) en el verano.Durante la estaci6nde reproducci6nlos aguiluchos cenizos 11evaron a cabo la mayorlade su forrajeoen las horasdel dia en que las gangasmachos estaban recogiendoagua para sus pollos. Esto supuestamenteles permiti6 a los aguiluchoslocalizar los pollosmils facilmente.Las gangasperdieron no mils de media hora del tiempo de alimentaci6ndiario debidoalas perturbacionespor avesde rapifia sin embargoestuvieron inactivos por lo menosdurante 3 horasal dia cuandohubieran podido estar alimentando.Las avesde rapifia en generalfueron probablemente el factormils importante en determinarlos distintos partrones de dispersi6n de las gangasen distintas•pocas del afio. [Traducci6n Autores]

Raptors can exert a significantinfluence on the rowhawksattacked particular tit (Parusspp.) flocks flocking behaviorof , both in the short term about once per day on average,and disturbedthe and the long term. In responseto attacksby spar- birdsfor only about2 min. Longerdisturbances can rowhawks (Accipiternisus), redshanks (Tringa tot- beinferred from detailedstudies of merlinsand spar- anus)deserted their winter feedingterritories for up rowhawks attacking wintering waders (Page and to an hour and formed flocks, while turnstones (Ar- Whitacre 1975, Boyce 1985, Cresswelland Whit- enariainterpres) reduced their individualspacing from field 1994), thoughno actualestimates are available threebird lengthsto onebird length(Whitfield 1988). in these cases. Myers (1984) found that winter feedingterritories In to derive estimates of the total time lost were abandonedby sanderlings(Calidris alba) in by pin-tailedsandgrouse (Pterocles alchata) and black- years when merlins (Falcocolumbarius) were more bellied sandgrouse(P. orientalis)as a result of dis- abundant. These studies focused on the influence of turbanceby raptors, we recordedthe amount of time raptors on the flocking and vigilance of potential the birds spendbeing vigilant, the number of inci- prey (seealso Metcalfe 1989). The amountof time dentsof disturbanceand the factorsresponsible. This for which target organismsare preventedfrom car- was done as part of the compilationof time and rying out otheractivities has seldom been measured. energy budgetsfor thesetwo speciesof sandgrouse In one early study, Morse (1973) found that spar- in Spain.

236 DECEMBER 1994 RAPTOR DISTURBANCE OF SANDGROUSE 237

STUDY AREA AND METHODS Table 1. Number of raptorsobserved while compiling Observations were made in semi-arid farmland in the sandgrousetime budgets. provinceof La Mancha, Spain, in spring (29 March to 21 April) and summer (22 July to 10 August) 1986. NUMBER OF Sandgrouseoccurred in flocks during the spring, com- SIGHTINGS prisingon average26 (SD = 23, N = 31) individualsin pin-tailed sandgrouse,with a maximum flock size of 75. OF EACH Most daytimeflocks of black-belliedsandgrouse contained RAPTOR 2-7 birds, though slightly larger groups (maximum 28) SUM- roostedtogether overnight. In summer, both speciesoc- SPRING MER curredin scatteredfamily groups.When compilingtime budgets,we scan-sampledbird activity at 1 min intervals. N= iV= In both seasons,the day was divided into 10 equal time RAPTOR 23 da 20 da periods.These time periodswere longer in summer (92 Black kite (Milvus migrans) 4 min) than in spring (82 min). The field area and study Red kite (M. milvus) 6 methodsare describedelsewhere (Hinsley 1994, Hinsley and Ferns 1994). A total of over 46 000 observations Montagu's harrier (Circuspygargus) 1 23 were made,involving on average29 pin-tailed sandgrouse Common buzzard (Buteobuteo) 3 4 and 6 black-belliedsandgrouse each day in spring, and Imperial eagle (Aquila heliaca) 2 family groupsof 2-5 pin-tailed sandgrousein summer(at Golden eagle (A. chrysaetos) 11 leasttwo differentfamilies were watchedeach day, and Bootedeagle (Hieraaetuspennatus) 1 over 40 familieswere studiedin total). Every potential Common kestrel (Falco tinnunculus) 1 predatorthat was observedclose enough to the focal birds Peregrine falcon (Falcoperegrinus) 1 2 to disturb them was recorded. If the same source of dis- Little owl (Athene noctua) 1 turbance causedmore than one group of birds to react, this was treated as a single incident, even if the events occurreda considerabletime apart (actual maximum = 7 min). sandgrouse adopted alert upright postures or The observationsin the spring were undertaken at a crouchedclose to the ground (thesebehaviors were rangeof 300-1000 m (typically700 m) to avoiddisturbing alsorecorded as vigilance). the birds, and it was not possibleto distinguishgender at The most common identified source of disturbance this time of year. Observationsin the summer were un- was raptors. During a total of 43 d of observations, dertakenat a range of 200-800 m (typically 400 m). In the summer,groups split up into family partiesin which the number of disturbancesdue to raptors was 60. males,females and juveniles (1-2-mon-old at the time of A further 49 disturbances were attributed to other the observations)were distinguishable. causes.The speciesof raptors involved (Table 1) To estimatethe amountof time that sandgrousespent differed significantlybetween spring and summer, beingvigilant when disturbed,we performedstepwise re- gressionon the percentageof time spent being vigilant though the number of incidentswas very similar. (arcsinetransformed) in eachof the 10 daily time periods The mostimportant species in springwas the golden againstthe number of recordsof disturbancecaused by eagle. The most important speciesin summer was all factorsthat we were ableto identify.These were divided Montagu's harrier (goldeneagles were absentfrom into five categoriescomprising the numbersof the most the area during the summer).Because the samein- commonraptors in eachseason (golden eagle [Aquila chry- saetos]in spring, Montagu's harrier [Circuspygargus] in dividualraptor may havecaused disturbance on more summer);other raptors; other birds (mainly red-legged than oneday, theremay havebeen some unavoidable partridges[Alectoris tufa] and great grey shrikes[Lanius pseudoreplication.However, the proportion of dis- excubitor]);mammals (rabbits, sheep and dogs);and hu- turbancescaused by the mostabundant raptor (com- mans(including noises caused by humanactivities). This method of measuring the affect of disturbancehas the pared with all other birds) in the two seasonswas advantageof taking into accountlosses of feeding time significantlydifferent (Fisher's exact test, P < 0.005). through increasedalertness even when this lastedfor some A greater diversity of raptors was thus responsible time after the disturbance ended. for disturbanceduring the spring (Table 1). Red kites (Milvus migrans) and black kites (M. milvus) RESULTS were recordedin springbut not summer,both being In the absenceof disturbance,sandgrouse vigi- migrantsin the area. A flock of 106 black kites that lancewas typically restrictedto shortbouts with the passedover on migrationon the eveningof 3 August headup. The durationof thesebouts was longestin was not included since it caused no disturbance. male pin-tailed sandgrouseaccompanying chicks (• Golden eagleswere observedcircling quite high = 6.5 sec, SD = 3.9, N = 47). When disturbed, (about30-50 m) overthe fieldsand hill slopes,and 238 PETER N. FERNS AND SHELLEY A. HINSLEY VOL. 28, NO. 4

14 a. SPRING alsoperched on vantagepoints overlooking the fields. Both goldeneagles and red kitesregularly take birds 12 the size of adult sandgrouse(Cramp and Simmons

10 1979). In spring, a juvenile imperial eagle (Aquila heliaca)took a taxidermic mount of a sandgrouse 8 •Pin-tailedS.vigilance Black-bellied /,• (usedto measureoperative temperature) from the S. vigilance // \ \ Numberof raptors 6 groundand was only preventedfrom flying off with it by the attacheddata-logger. Montagu's harriers 4 and red kitesquartered the fieldsat a heightof only // .- \ a few meters,and occasionallycircled at a greater 2 elevation.In summer, Montagu's harriers were ob- servedattacking young sandgrouse,but not adults. The young of ground-nestingbirds form a consid-

b. SUMMER erable part of this harrier's diet during the summer ; 50 months(Cramp and Simmons1979). Vigilance of adult sandgrousein eachtime period ß 40 (Fig. 1) peakedduring the middle of the day in E •.Adult Pin-tailedS.0•• spring,and during the morningand eveningin sum- ß 30 mer. The gap betweenthe summer peaks coincided with a periodof reducedactivity of bothraptors and sandgrousein the middleof the day, inducedby high •= 20 temperature.The vigilance of juvenile sandgrouse reacheda peak earlier in the morning than that of o lO adults. Adult males spentmore time being vigilant No.ofraptors• in summerthan in spring (19% of daylight hours • o u comparedwith 3%), presumablybecause of the vul- nerability of their offspringduring the former pe- riod. This difference was statisticallysignificant • 12 (Kruskal-Wallis test, H = 11.3, P = 0.001. While male and female vigilancein the 10 daily //•• c.SUMMER time periods were correlated significantly during summer (r = 0.69, P ( 0.02, N = 10), juvenile o 8 vigilancewas not correlatedwith that of either par- ent (r = 0.46 with males and r = 0.12 with females, E 6 z P • 0.10 in both cases).This is largely because ilePin-tailedS. vigilance juveniles spent most of the day feedingor resting, //I • 'X• NumberofMontagu• Harriers relying on their parentsto actas sentinels (especially ; \ • their fathers).They showedmost alertness when he wasaway collectingwater for them duringthe morn- ing and when he returned.Juveniles were lesssen- 2 3 4 5 6 7 8 9 10 sitive to disturbanceby Montagu's harriers in the Time period evenings(Fig. 1), probablybecause the latter spent mostof their time hunting rabbitsduring this period F•gure 1. Selectedraptor activity(numbers) and sand- of the day. grousevigilance (percentage of time budget)throughout Sandgrouseresponded to raptors differently in the daylightperiod. The total numberof raptorsis shown •n spring(a), the total numberof raptorsother than Mon- spring and summer, and this reflected the different tagu'sharriers (b), and numberof Montagu'sharriers in dispersionpattern they adoptedin the breedingsea- summer (c). sonbecause of the vulnerabilityof their young(Lima and Dill 1990). In neither spring nor summerdid the sandgrouseform densergroups when disturbed; if anythingthe flockstended to split up. In spring, DECEMBER 1994 RAPTOR DISTURBANCE OF SANDGROUSE 239 they merely flew to anotherof the severalfields in that causedby humans (t = 4.8, P = 0.003). The which they normally foragedduring the courseof larger size of this speciesapparently made it less the day. In summer,the first responseof both adults vulnerableto disturbanceby mostraptors. and youngto the presenceof a raptor was to crouch and freeze.If a family groupwas located by a raptor, the adultsusually mobbedit beforeflying off, while DISCUSSION the young ran or flew into the nearestdense vege- While the spring flocks of sandgrousemay have tation. Consequently,their activity was affected been reasonablyeasy for golden eaglesand other mainly by a directloss of time availablefor feeding, raptorsto locate,they did not providea particularly preening,drinking and otheractivities. We sawthree easytarget as indicatedby the rarity of the attacks direct attacks by Montagu's harriers on juvenile we witnessed.Young sandgrouseduring the breed- sandgrouse,all unsuccessful,and adultswith young ing seasonwere much more vulnerable,though they mobbedMontagu's harriers on four additional oc- must have been more difficult to locate in the well- casions.Male vigilance showedno significantcor- dispersedfamily groups. It is thus not surprising relation with disturbance factors, mainly because that Montagu's harriers concentratedmost of their they spentsuch a high proportionof the time alert, foragingactivity in the periodwhen male sandgrouse evenin the absenceof any obviousdisturbance (19% returned with water from the waterholes, since this of daylight hoursspent alert, comparedwith 12% in providedthem with a potential clue to the where- females). aboutsof young. Such predation pressuremay have Since disturbanceoften causedsandgrouse to fly led in turn (c.f. Lima and Dill 1990) to a wider in spring,there was significantlymore sandgrouse spreadof watering times amongstmales in this area, alertnessin time periods in which the birds spent including evening watering. The two species of more time flying (r = 0.80, P < 0.01, N = 10 in all sandgrousewe observedtended to foragein different cases).In summer, reducedlevels of alertnessin both typesof habitat (Hinsley 1994), but we do not believe sexesof pin-tailed sandgrousewere associatedwith that this choice was influenced by raptor activity. periodsof resting (males, r = -0.68, P < 0.05; The pin-tailed sandgrousewas the more vulnerable females,r -- -0.67, P < 0.05). Differencesin flock species,but it foraged in open fields where it was sizeswere not significantin differenttime periods, more visiblethan on the hill slopesfavored by black- nor was alertnesssignificantly correlated with flock bellied sandgrouse.As suggestedby Lima and Dill size in either species.Therefore, alertnesswithin (1990), vigilancecosts were higher during the breed- seasonswas not significantlycorrelated with any ing season.Adults with young were also prepared variable that might have confoundedits correlation to run greater risks by mobbingraptors during the with disturbance,including flock size or distanceto summer. cover(Elgar 1989). Predation of young sandgrouseprobably repre- Stepwiseregression analysis indicated that a high sentsa major sourceof mortality (Maclean 1985). proportionof the time spent being vigilant was ac- However, young are likely to be evenmore vulner- countedfor by the observedsources of disturbance, able to raptors at water holes (Cade 1965) and this despitethe small samplesize (N = 10 in all cases). may explain why malescontinued to carry water to In spring,48% of the variation in pin-tailed sand- them even after they had becomecapable of flying grousevigilance between time periodswas accounted to water holesfor themselves.Raptors recordedat- for by the overall number of raptorsrecorded (t = tacking or consumingsandgrouse in other areas in- 3.2, P < 0.02) and 20% by human disturbances(t cludepallid harrier (Circusmacrourus), golden eagle, -- 2.4, P = 0.05). In summer,46% of femalevigilance greater kestrel (Falcorupicoloides), sooty falcon (F. was accountedfor by raptorsother than Montagu's concolor),lanner falcon (F. biarmicus)and Barbary harriers (t = 2.5, P < 0.05) and 25% by mammals falcon(F. pelegranoides)(Ali and Ripley 1983, Cramp (t = 2.5, P < 0.05). Also in summer,68% of juvenile 1985, Urban et al. 1986). vigilancewas accountedfor by the number of Mon- The amountof time maleswith youngspent being tagu's harriers (t = 4.1, P = 0.003). Fifty-seven vigilant (19% of daylight hours) was much lessthan percentof black-belliedsandgrouse vigilance in spring that of male barnacle geese(Branta leucopsis)es- was accountedfor by disturbancecaused by dogs, cortingtheir broods(48%) (Forsland 1993). In both sheepand rabbits (t = 5.6, P = 0.001), and 19% by species,the males devotedmore time to vigilance 240 PETER N. FERNSAND SHELLEYA. HINSLEY VOL. 28, NO. 4 than the females. Walters (1990) found no difference ACKNOWLEDGMENTS in the responseof long-toedlapwings (Vanellus cras- We are most grateful to the Fundaci6n Josg Maria szrostris)and blacksmith plovers (V. armatus) ac- Blanc for allowing us to work on their estatein Spain and cordingto whether or not they had young,but they to D.H. Thomas for locating sucha goodplace to study sandgrouse.SAH was supportedby a SERC research did respondmore strongly to harriersthan to eagles. studentship.We would also like to thank three referees The intensityof predatorydisturbance at our study for numerousimprovements to the manuscript. site was relatively low comparedwith someothers. For example, at Bolinas Lagoon in California, a singlemerlin mountedabout 19 attacksper day on LITERATURE CITED shorebirds(Page and Whitacre 1975). However,the ALI, S. AND S.D. RIPLEg. 1983. Handbook of the birds 5000 potential prey in this area were divided into of India and Pakistan. Oxford Univ. Press, Oxford, groupsof at mostseveral hundred, and thereforethe U.K. disturbanceincurred per bird was much lower. Cal- BOYCE, D.A. 1985. Merlins and the behavior of win- vo (1993) recorded more than 10 disturbancesper tering shorebirds.Raptor Res. 19:94-96. day (an order of magnitudemore than that caused CADE,T.J. 1965. Relationsbetween raptors and colum- biform birds at a desert water hole. Wilson Bull. 77: by raptorsat our site)at breedingcolonies of collared 340-345. pratincoles(Glareola pratincola) in southwestSpain. CALVO,B. 1993. Influencesof agricultural land-use and Black kites and commonkestrels (Falco tinnunculus) habitat modificationon the breedingbiology and con- were responsiblefor most pratincole disturbance, servationof collaredpratincoles Glareola pratincola in though Montagu's harriers were also seen taking SW Spain. Ph.D. dissertation,Univ. Glasgow,U.K. chicks. CRAMP,S. [ED.]. 1985. The birds of the western Pale- Most of the time sandgrousespent being vigilant arctic. Vol. 4. Oxford Univ. Press, Oxford, U.K. as a result of the activities of raptors, humans, and -- AND K.E.L. SIMMONS.[EDs.]. 1979. The birds othermammals was time theywould otherwisehave of the western Palearctic. Vol. 2. Oxford Univ. Press, spentfeeding. In the middle of the day, when birds Oxford, U.K. CRESSWELL,W. AND D.P. WHITFIELD. 1994. The effects rested in the shade of shrubs, alertness and distur- of raptor predation on wintering wader populationsat bancelevels were relatively low andthe smallamount the Tyninghame estuary,southeast Scotland. Ibis 136: of disturbancethat did occurthen was usually caused 223-232. by red-leggedpartridges. ELGAR,M.A. 1989. Predator vigilanceand group size None of the results describedhere suggestthat in mammalsand birds:a criticalreview of the empirical d•sturbanceby raptors presentedsandgrouse with evidence. Biol. Rev. Cam& Philos. Soc. 64:13-33. any difficultyin meetingtheir daily energyrequire- FORSLAND,P. 1993. Vigilance in relation to brood size ments. The time of the year when the highestpro- and predator abundancein the barnacle goose,Branta portionof the day was occupiedby foragingwas the leucopsis.Anirn. Behav. 45:965-973. spring,and eventhen black-belliedsandgrouse were HINSLEY, S.A. 1994. Daily time budgets and activity patternsof sandgrouse(Pteroclididae) in contrasting still able to devoteover 3 hr, and pin-tailed sand- arid habitats in Spain and Israel. J. Arid Environ. 26: grouseover 4 hr, to restingat timeswhen they could 373-382. presumablyhave been feeding.The aboveregres- • ANDP.N. FERNS. 1994. Time and energybud- sions enable us to estimate that raptors in spring getsof breedingmales and femalesin sandgrousePter- causedpin-tailed sandgrouseto lose about 24 min oclesspecies. Ibis 136:261-270. of foragingtime per day. Mammals causedblack- LIMA, S.L. AND L.M. DILL. 1990. Behavioral decisions belliedsandgrouse to lose10 min per day at the same made under the risk of predation: a review and pro- time of year. In summer,Montagu's harriers caused spectus.Can. J. Zool. 68:619-640. juvenile pin-tailed sandgrouseto lose9 min per day. MACLEAN,G.L. 1985. Sandgrouse:models of adaptive Other raptors causedadult femalesto loseabout 25 compromise.S. Aft. J. Wildl. Res. 15:1-6. METCALFE,N.B. 1989. Flocking preferencesin relation min. Raptors may be the largest single sourceof to vigilance benefits and aggressioncosts in mixed- disturbance,but man and other mammals alsocaused speciesshorebird flocks. Oikos56:91-98. some,even in this thinly populatedarea. Predators MORSE, D.H. 1973. Interactions between tit flocks and as a whole were probablya major factorresponsible sparrowhawksAccipiter nisus. Ibis 115:591-593. for the different dispersionpatterns adopted by pre- MYERS, J.P. 1984. Spacing behavior of nonbreeding breeding and breeding sandgrouse. shorebirds.Pages 271-321 in J. Burger and B.L. Olla DECEMBER 1994 RAPTOR DISTURBANCE OF SANDGROUSE 241

[EDS.], Behavior of marine . Vol. 6. Shorebirds. wings: field evidenceof discriminative abilities. Wilson Migration and foraging. Plenum Press,NY U.S.A. Bull. 102:49-70. PAGE,G. ANDD.F. WHITACRE. 1975. Raptor predation WHITFIELD,D.P. 1988. SparrowhawksAccipiter nzsus on wintering shorebirds.Condor 77:73-83. affect the spacingbehavior of wintering turnstoneAr- URBAN,E.K., C.H. FaY AND C.S. KEITH. [ED$.]. 1986. enaria interpresand redshankTringa totanus.Ibis 130. The birds of Africa. Vol. 2. Academic Press, London, 284-287. U.K. WALTZaS,J.R. 1990. Anti-predatory behavior of lap- Received22 February 1994; accepted30 July 1994