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PAIR COPULATIONS, EXTRA-PAIR COPULATIONS, AND INTRASPECIFIC NEST INTRUSIONS IN MERLIN ’

NAVJOT S. SODHI Department of Biology, Universityof Saskatchewan,Saskatoon, Saskatchewan S7N 0 WO, Canada

Abstract. This paper reports three extra-pair copulations(EPCs) and two EPC attempts in Merlin (Falco columbarius). Three hypotheses of frequency of pair copulations were evaluated. The Merlins copulated both during fertile and non-fertile periods, providing support for the social bond hypothesis. Sixty copulations per pair were estimated for the whole breeding season.This copulation rate is high compared to other solo breeding non- raptorial birds and to that necessaryto fertilize a clutch of four or five. As male Merlins cannot guard their mates continuously and there are possibilities of extra-pair copulations in the study area, this high copulation rate may be an insurancefor genetic paternity, thus providing support for the sperm competition hypothesis.The majority of intraspecificnest intruders were chased from the vicinity of the nests during the fertile period. Key words: Merlin; Falco columbarius;copulations; extra-pair copulations;intraspe&c nestintruders; sperm competitionhypothesis.

INTRODUCTION According to the copulation trading hypothesis, Like most other birds (Birkhead et al. 1987, Birk- males decrease the risk of EPCs by feeding the head 1988), little is known about the copulation females, thus limiting their need to visit other behavior of the Merlin (Falco columbarius). males for food (Birkhead and Lessells 1988) and Feldsine and Oliphant (1985) however, de- the females, in turn, trade copulations for food scribed displays associated with copulations in to ensure a continuous food supply (Poole 1985). this primarily monogamous falcon and Laing The prediction of this hypothesis is that the ma- (1985) noted 11 copulations at four nests at De- jority of copulations would be solicited by the nali National Park, Alaska. Virtually no data ex- females after prey deliveries by the males. The ist concerning behaviors of intraspecific nest in- sperm competition hypothesis states that, if truders and responseof resident Merlins towards chancesof EPCs are high, males should attempt them. Cramp and Simmons (1980: 313) stated to displaceor devalue the sperm of possiblecom- that there is no record of aggressiveencounters petitors by copulating at a high rate (Birkhead et between conspecificMerlins during the breeding al. 1987). Because most male raptors are not season. James and Oliphant (1986) also found known to guard their mates (Birkhead et al. 1987, that a resident pair generally tolerated an extra Moller 1987a; but seePoole 1985) and are away yearling male near the nest. from the nests (and females) foraging for varying Here, I report three extra-pair copulations amounts of time during the female’s fertile pe- (EPCs), two EPC attempts, and examine the con- riod, this high copulation frequency would pos- cordance of copulation behavior of the Merlin sibly dilute the possibility of fertilization by EPCs in relation to current hypothesesabout copula- that may have occurred in their absence. tion frequency in birds. Three main hypotheses I also describe behavior of intraspecific nest have been proposed to explain the copulation intruders and the response of residents toward behavior of birds (Birkhead et al. 1987). The them. I tested two predictions of the sperm com- social bond hypothesis statesthat copulation be- petition hypothesis,viz. majority of intraspecific havior is associated with formation and main- nest intruders are males seeking EPCs and male tenance of the pair bond (Nelson 1965, Newton nest intrusion rate should be higher during the 1979) and a resulting prediction is that copu- fertile period than non-fertile period (Moller lations occur outside the female’s fertile period. 1987b). METHODS

I Received 11 October 1990. Final acceptance 18 I spent 679 hr watching 13 nests between May January 1991. and July, 1988-l 990. All observationswere made 14331 434 NAVJOT S. SODHI

that introduced sperm will lead to fertilization are high (Moller 1987b). As predicted by the social bond hypothesis, I recorded copulations during the fertile and non- fertile periods. Twenty-six copulations were ob- served during the fertile period in 130 hr (0.20 copulations/hr). The frequency of copulations re- corded at Saskatoon during the fertile period of the femalesis lower than recordedelsewhere (0.67 copulations/hr; Laing 1985), but Laing’s data were based on only 16 hr of sporadic observa- -10 0 10 20 30 40 50 tions. DAYS OF NESTING CYCLE Fifteen copulations were recorded in 549 hr FIGURE 1. Seasonalvariation in copulation rate in during the non-fertile period (0.03 copulations/ Merlin. Zero denotes start of egg-laying for a modal hr). I recorded copulations between seven days clutch of five. Note that initiation of egg-laying was determined (seeMethods for details) for each observed prior to and 35 days after egg-laying (Fig. 1). In female (n = 13). If more than one female was observed other words, pair copulations were observed up on a particular day of the breeding cycle an averageof to mid-nestling period and on 39 days out of 84 copulation rate was obtained to plot this figure. days of the non-fertile period. No copulations were observed during the fledging period, per- haps because males and females rarely come in at Saskatoon (52%7’N, 106”38’W), Saskatche- contact with each other during this period. wan, Canada. The study area is described by Assuming the fertile period of 14 days and a Warkentin and James (1988). The breeding Mer- daily activity of 15 hr, I estimate 42 copulations lin population was 20.5,25.4 and 24.6 pairs/100 per clutch. For 39 days of the non-fertile period, km2 respectively during 1988, 1989, and 1990; when I observed pair copulations, with 15 hr of which is the highest density for this speciesany- daily activity, I estimate 18 copulations per pair. where recorded (Sodhi et al., unpubl. data). In other words, a total of about 60 copulations/ The falcons were observed from a car using pair during the breeding season. Evidence from 7 x binoculars, mostly during first and last four domestic birds suggeststhat a single insemina- daylight hours. However, some dawn-to-dusk tion may fertilize an entire clutch (Lake 1975). observations were also made (pre-laying peri- Other studieshave also recorded high copulation od-4 days, incubation period-4 days, and nest- frequency in raptors, viz. the Peregrine Falcon, ling period-2 days). For some analyses, I di- F. peregrinus(30 copulations/pair; Ratcliffe vided the Merlin breeding seasoninto the fertile 1980); American Kestrel, F. sparverius(690 cop- (pre-laying and egg laying) and non-fertile (in- ulations; Balgooyen 197 6); European Kestrel, F. cubation, nestling, and fledging) periods. I de- tinnunculus(374 copulations; T. Meijer in Birk- termined these periods by behavior of the resi- head and Lessells 1988); Goshawk, Accipitergen- dent pair and/or backdating from estimated ages tilis (> 500 copulations; Msller 1987a); Osprey, of young (assuming 32 days incubation, egg-lay- Pandionhaliaetus (160 copulations;Birkhead and ing interval 2 days; Palmer 1988). I assumedthat Lessells 1988); and Prairie Falcon, F. mexicanus the females became fertile 4 days prior to egg- (194 during the pre-incubation period; Holthu- laying (Berry 1972, Boyd et al. 1977). Resident ijzen 1989). The high copulation rate in raptors falcons were either radio-marked, had a year- compared with other monogamous birds is con- specificcolor band, or wore a U.S. Fish and Wild- sidered insurance against extra-pair fertilizations life Service aluminum leg band. (Birkhead et al. 1987). Of 4 1 copulations, only eight (19.5%) occurred RESULTS AND DISCUSSION within half an hour after the males gave food to PAIR COPULATIONS the females and only three of thesewere initiated In all, I observed 41 pair copulations. The fre- by solicitation by the females. It appearsunlikely quency of pair copulations peaked just prior to that female Merlins trade copulations for food. and during egg-laying (Fig. l), when the chances In summary, the Merlins copulate in the fertile COPULATIONS AND NEST INTRUSIONS IN MERLIN 435 as well as non-fertile period, which implies that the nest tree and perched about 25 m from the copulations in Merlins have a role in mainte- female and the other male. After a few minutes, nance of the pair bond. Other studies on raptors the intruder male flew toward and dived at him; also reveal that the intrapair copulations occur the resident male crouched and gave weak tic both in fertile and non-fertile periods, e.g., the calls (Feldsine and Oliphant 1985). The intruder Cape Vulture, Gypscoprotheres (Robertson 1986) male soared near the nest for approximately 5 Goshawk (Moller 1987a), Osprey (Birkhead and min and then flew away. The lack of aggression Lessells 1988), and Prairie Falcon (Holthuijzen by the resident male toward the intruder could 1989). Males cannot remain with their mates possibly be due to two reasons: 1. the intruder continuously during the fertile period becauseof male was stronger than him (Parker 1974), and foraging needs and extra-pair copulations oc- 2. the female had laid a full clutch, so there was curred in my study (see next section). Perhapsto no possibility of cuckoldry. There was no ap- increase the likelihood of genetic paternity, Mer- parent change in the behavior of the resident lins copulate at a higher frequency than is needed male after the EPC, he provided food for the to fertilize a clutch of four or five eggs.My data female (and chicks; two young were successfully provides indirect support for the sperm com- raised) and did not show any aggressiontoward petition hypothesis. Very few (7.3%) copulations her. were solicited by the females after the males gave On 15 June 1988 (nestling period), at about them food, providing no clear support for the 06:00, I observed a yearling male giving copu- copulation trading hypothesis. lation chutters near a nest. He seemed to be ig- nored by the resident pair. On 7 June 1990, at EXTRA-PAIR COPULATIONS 06:30, I saw a non-resident female near a nest On 3 May 1988, approximately at 09:00, I ob- in which the resident female was brooding. The served a non-resident adult male Merlin landing resident male, perched nearby, gave copulation about 20 m from a resident female which was chutters and flew towards the intruder female, perched about 10 m from her nest. The male but no copulation occurred and she flew off from gave a copulation chutter (Chrrr; Feldsine and view. Oliphant 1985) while the female solicited cop- As no intruder was individually color-marked, ulation by bowing and fanning her tail. Then the I could not determine their breeding status. Be- male tlew toward her and mounted her. After causetwo EPCs occurred when the females were copulating, the male flew from the vicinity of the potentially fertile, it appearsthat EPCs have some nest. On 5 May 1989, at 12:30, I observed a non- reproductive significance in Merlins (Cheng et resident adult male copulating with the resident al. 1982, Welsh and Sedinger 1990); EPC could female about 25 m from her nest. After copu- serve as a secondary reproductive strategy (Mi- lating, the male perched near the nest for about neau and Cooke 1979). The third EPC occurred 10 min during which he frequently called ki-ki- after the female completed her clutch and was kee (Feldsine and Oliphant 1985). In both in- thus probably infertile. Extra-pair copulationsand stances,the resident females were egg-laying and attempts at EPCs outside the female’s fertile pe- thus potentially fertile. The resident males (ra- riod probably occur becauseit is sometimes dif- dio-tagged) on both theseoccasions were hunting ficult for intruder males to accurately assessthe away from the nests. Because the copulations fertility ofthe females (Mineau and Cooke 1979). lasted about 5-10 set, it seemslikely that in both these EPCs the males had cloaca1 contact and INTRASPECIFIC NEST INTRUDERS ejaculation. I observed 28 nest intrusions, of which 19 (68%) On 17 May 1990, at about 19:15, I observed were by males, four (14%) by females, and five an adult non-resident male flying near a resident (18%) by unknown sex (x2 = 14.2, df = 2, P < female while the resident male was incubating. 0.01). The frequency of male intruders during The female gave a copulation chutter and fol- the fertile period was double (O.O5/hr) than dur- lowed the intruder male and then both birds ing the non-fertile period (O.O2/hr). perched and copulated. The resident male came Twelve intraspecific nest intrusions were re- out of the nest but did not try to supplant the corded during the fertile period (0.09 intrusions/ intruder male. The resident male then flew from hr or an estimated 19 intrusions during the whole 436 NAVJOT S. SODHI period), seven (58%) were by males (three year- truders were males and the frequency of male lings, four adults), two (17%) by females, and intruders was higher during the fertile period. three (25%) by Merlins of unknown sex. Two intrusions by males resulted in EPCs (described ACKNOWLEDGMENTS above), four males were immediately chased by I thank G. Peat and J. Freeland for field assistance, the resident males when the intruders landed near and L. W. Oliphant, P. C. James, R. G. Clark, R. N. the nests. One intruder male called ki-ki-kee for Rosenfield, and an anonymous reviewer for making about five min near a nest. He seemed to be comments on the manuscript. Funding was provided ignored by the resident female; the resident male by a Natural Sciencesand EngineeringResearch Coun- cil of Canada grant to L. W. Oliphant and a University was away hunting. Both intruder females went of SaskatchewanGraduate Scholarshipto the author. into the nests (intraspecific brood parasitism at- tempts?) while the resident pair was sitting with- LITERATURE CITED in 25 m from the nest, both these females were B-YEN, T. G. 1976. Behavior and ecologyof the chased by the resident pair. Three Merlins of American Kestrel (F&o sparveriusL.) in-the Si- unidentified sex flew over the nests and did not erra Nevada of California. Univ. Calif. Publ. Zool. elicit any responsefrom the resident pair. 103:1-83. Sixteen nest intrusions occurredduring the non- BERRY, R. B. 1972. Reproduction by artificial insem- fertile period (0.03 intrusions/hr or estimated 38 ination in captive American Goshawks. J. Wildl. Manage. 36:1283-1288. intrusions, assuming 84 days of non-fertile pe- BIRKHEAD,T. R. 1988. Behavioral aspectsof sperm riod with 15 hr of daily activity). Twelve (75%) competition in birds. Adv. Stud. Behav. 18:35- were by males (six yearlings, six adults), one re- 72. sulted in EPC and an attack on the resident male BIRKHEAD,T. R., AND C. M. hSSELIS. 1988. Copu- lation behaviour of the Osprey Pandion haliaetus. and one was an attempted EPC (both described Anim. Behav. 36:1672-1682. above). Three adult males attacked the resident BIFXHEAD, T. R., L. ATKIN, AND A. P. MILLER. males, one intruder tried to land on a resident 1987. Couulation behaviour of birds. Behaviour male. As stated earlier, thesemales were possibly 101:101-i38. stronger than the residents. Five males stayed BOYD, L. L., N. S. BOY-D,AND F. C. DOBLER. 1977. Reproduction of Prairie Falcon by artificial insem- near the nests for a few minutes when present; ination. J. Wildl. Manage. 4 1:266-27 1. all these males seemed to be ignored by the res- CHENG,K. M., J. T. BURNS,AND F. MCKINNEY. 1982. ident males. A yearling male brought a sparrow- Forced copulation in captive Mallards (Anus sized bird and fed the nestlings and another male platyrhynchos):II. Temporal factors. Anim. Be- hav. 30:695-699. attacked a nest climber. Although extra birds &, S., ANDK. E. L. SIMMONS[EDS]. 1980. Hand- near Merlin nests have been observed to defend book of the birds of Europe, the Middle East and nests and deliver prey to the resident female north Africa. Vol. 2. Oxford Univ. Press,Oxford. (Jamesand Oliphant 1986), this is the first report FELDSINE,J. W., AND L. W. OLIPHANT. 1985. Breed- of an extra bird feeding the chicks. ing behavior of the Merlin: the courtship period. Raptor Res. 19~60-67. Two (12.5%) nest intruders were females. The HOLTHUIJZEN,A.M.A. 1989. Behavior and produc- resident male tried to copulate with one (de- tivity of nestingPrairie Falcons in relation to con- scribed earlier) and the other extra female food- struction activities at Swan Falls Dam. Final Re- beggednear the nest and was chased by the res- vort. U.S. Bureauof Land Manage.. Boise. Idaho. JAM&, P. C., ANDL. W. OLIPHANT. ident female. Two (12.5%) Merlins of unknown 1986. Extra birds and helpers at the nests of Richardson’s Merlin. sex flew over the nest, one was chased by the Condor 88533-534. resident male and the other did not elicit any LAING, K. 1985. Food habits and breeding biology apparent responsebehavior by the resident pair. of Merlins in Denali National Park, Alaska. Rap- In summary, the majority of nest intruders tor Res. 19:42-5 1. LAKE,P. E. 1975. Gamete production and the fertile were chasedfrom the nestsby the resident males period with particular reference to domesticated during the fertile period, but intruders often were birds. Symp. Zool. Sot. Lond. 35~225-244. tolerated during the non-fertile period: This be- MINEAU,P., ANDF. COOKE. 1979. Rape in the Lesser havior is consistent in avoiding EPCs while min- Snow Goose. Behaviour 70:280-29 1. MBLLER,A. P. 1987a. Copulation behaviour in the imizing risk of personal injury by avoiding fights Goshawk,Accipiter gent&. Anim. Behav. 35:755- when paternity is not at risk. As predicted by the 763. sperm competition hypothesis, most of nest in- MILLER, A. P. 1987b. Intruders and defenders on COPULATIONS AND NEST INTRUSIONS IN MERLIN 431

avian breedingterritories: the effect of sperm com- POOLE,A. 1985. Courtship feeding and Osprey re- petition. Oikos 4847-54. production. Auk 102:479-492. NELSON, J. B. 1965. The behaviour of the Gannet. RATCLIFFE,D. 1980. The Peregrine Falcon. Buteo Br. Birds 58223-288, 313-336. Books, Vermillion, ND. NEWTON,I. 1979. Population ecologyof raptors. Bu- ROBERXC~N,A. 1986. Copulationsthroughout breed- teo Books, Vermillion, ND. ing in a colonial Accipitrid vulture. Condor 88: PALMER,R.S. [ED.]. 1988. HandbookofNorthAmer- 535-539. ican birds. Vol. 5. Yale Univ. Press, New Haven, WARKENTIN,I. G., AND P. C. JAMES. 1988. Nest-site CT. selectionby urban Merlins. Condor 90:734-738. PARKER,G. A. 1974. Assessment strategy and the WELSH,D., ANDJ. S. SEDINGER.1990. Extra-pair cop- evolution of fightingbehaviour. J. Theor. Biol. 47: ulations in Black Brant. Condor 92:242-244. 223-243.