Mate Replacement and Male Brood Adoption in Lapwings <I>Vanellus

Mate replacement and male brood adoption in Lapwings Vanellus vanellus

TERJE LISLEVAND •*, GAUTE BiDGRiDNSTiDL •, INGVAR BYRKJEDAL2 & JO ESTEN HAFSMO •

•Departmentof Zoology,AIl•gaten 41, N-5007 Bergen,Norway, e-maih terje.lislevand@zoo. uib. no; 2Museumof Zoology,Mus•plass 3, N-5007 Bergen,Norway

Lislevand,T., Gronst½l,G.B., Byrkjedal,I. & Hafsmo,J.E. 2001. Mate replacementand male broodadoption in Lapwings Vanellusvanellus. Wader StudyGroup Bull. 95: 55-58.

Mate replacementand male broodadoption has been reported in a rangeof bird species,but doesnot seem to havebeen reported before now in waders.We presentdetails of a casewhere a bigamousmale Lapwing Vanellusvanellus died at the onsetof egg laying, whereuponhis territorywith the two femaleswas divided betweenand taken over by two neighbouringmales. One of the replacementmales incubatedon the nest of his new mate, while the otherbehaved indifferently. Based on currentbrood adoptiontheory, it is suggestedthat the males' behaviour could arise from either(1) the chanceof gainingfuture fitness benefits, or (2) confidenceof paternityor (3) a combinationof both.

INTRODUCTION 1998, from 20 March to 10 May, covering the period from territoryestablishment until late chick-rearing.We recorded The degreeof parentalcare by malesshould depend on their pair bondsby makingfield sketchesof the birdsthat showed certainty of paternity (Trivers 1972, Westneat & Sherman characteristicplumage markers (Byrkjedal et al. 1997) and 1993, Houston1995). Yet, observationsof replacingmales madeit possibleto separateall studiedindividuals. Territory adopting and caring for offspring apparently fathered by boundarieswere mappedby plotting the locationsof males anothermale existfrom at least 17 speciesof birds(Rohwer and their flight displayroutes. The main studyincluded 32 1986, Meek & Robertson1991). Parentalcare for the young territorial males with 46 nestingfemales in a total area of of othermales thus appears altruistic, and the adaptivevalue c. 20 ha. Figure 1 showsa map of the territoriesof the birds of this behaviourmay not be obvious. referredto in this paper and other birds nestingin the same Rohwer(1986) discussedwhether adoption is just misdir- field. ectedparental care not costlyenough to be selectedagainst Observationsof Lapwing behaviour were carried out (maladaptiveview), or a resultof naturalselection (adaptive daily between 08:00 and 15:30 from hides or a car at the view). In the latter case, replacementscould gain future perimeterof the fields,by watchingindividual birds continu- matingbenefits by increasingtheir breedingexperience, get ouslyfor standardperiods of 20 minutesthrough 15-45•-> tel- accessto limited resources,or increasethe probabilityof re- escopesand binoculars. Nests were foundduring the obser- matingwith thefemale by demonstratingtheir parental abil- vation bouts, or at other times by regularly searchingthe ity to her. Meek & Robertson(1991) pointedout that obser- fields visually for incubating birds. All observationsof vationsof broodadoption often lack quantitativeinformation copulationswere recorded,including those seen outside the aboutpaternal care, and arguedthat it is importantto distin- standardobservation periods. guishbetween full andpartial adoption based on the amount of care that is provided. Further they suggestedthat confi- RESULTS denceof paternityin somecases may play a role when replacementmales are providing parental care. If so, what Male No. 30 (M30), who was mated to females Nos 22 and looks like full brood adoptionactually differs little from 27 (F22, F27), disappearedpermanently from the field on 30 normalpaternal care. or 31 March 1998. Subsequentlytwo neighbouringmales, Here we report a caseof mate replacementand apparent M36 andM34, eachtook over half the territoryof M30 along broodadoption in two maleLapwings Vanellus vanellus who with F22 and F27, respectively.Figure 2 showsthe phenol- took over the matesof a bigamousneighbour that was killed ogy of events,and the details were as follows: by a predatorat the onsetof his mates' egg-laying.Subse- M30 was unmateduntil 23 March, when F22 (primary quent observationsof the replacementmales may indicate female) appearedand settledon his territory. On 25 March, that their behaviourreflected confidence of paternity. F27 (secondaryfemale) was also present.M30 was seen copulatingwith F27 on 30 March,just a few hoursbefore he METHODS disappeared.He was last seenin the afternoonof 30 March. Feathersof a depredatedmale Lapwing, that we assumewas We studiedthe breedingbehaviour of Lapwingsin two grass M30, were found on a field about 150 m from his territory fields at Gimramyra, Sola, Southwest Norway, in spring at about14:00 the next day. On the dayM30 disappeared,the

*Correspondingauthor.

55 Bulletin 95 August 2001 56 Wader Study Group Bulletin

F40 / / / / F22 M36 ! ß F43 ! I F27 ! M30 M32 t

/ F24 M33 F13 ß F26 F20 F25

F21 M31 ß

I I 100 rn

Figure 1. Map showing the Lapwing territories where mate replacement was observed and other territories on the same field. Territory borders are indicated by solid lines and the number of the defending male (M) is presented within each territory.The broken line indicates the border of the area defended by the replaced male. Nest placement is shown by solid dots and the number of the associated female (F). A road (grey-scale line) runs along one edge of the field, but otherwise it is surrounded by other farmland.

primary female (F22) had alreadylaid oneegg, while his sec- actedindifferently towardsthe eggsof F27 (Table 1), and ondary female (F27) was still in her pre-laying period. was never seenon this nestat othertimes of sporadicobser- By 31 March, the males M34 and M36, which held terri- vations. His total incubation effort was not lower than that tories on opposite sides of M30's territory, had divided of M36, however, as he spent39.6% of the time incubating M30's territoryas well ashis two matesbetween themselves. the clutches of his other two females. M34, who was already mated to two females, adoptedF27 Althoughhe died before mostof the eggswere laid, it is as his tertiary female, while M36 took over F22 to become possiblethat all eggsin bothclutches were fertilized by M30, his secondaryfemale. becausefemale birds are ableto storesperm for severaldays On 3 April, the nest of F22 contained3 eggs and, on 6 (Birkhead & M011er1992). The possibility,however, that April, 4 eggs.All four eggshatched on 2 May and all chicks someeggs had been fertilised by M34, M36 or other males were presenton 10 May, when they were checkedfor the last cannotbe discountedbecause no information on paternity time. F22 and M36 were seencopulating once, on 21 April. exists from the studied nests. In comparison,we observedtwo copulationswith his primary female during the sameperiod (20 March-21 April). DISCUSSION M36 took part in the incubationon the nest of F22 as well as on that of his primary female (Table 1). As far aswe are aware,this is the first reportof male replace- On 31 March, M34 attemptedto copulatewith F27 twice mentand apparentbrood adoption in any shorebird.The two during 20 secondsat 12:35, but she refusedboth times. At male Lapwings clearly differed in the parental behaviour 12:43 the sameday, anotherneighbour (M32) attemptedto they exhibited towards the clutchesof their new females. copulate with her, but also in this case she refused. He re- However, as male incubation contribution in this species spondedby peckingat her and chasingher into the air. Then rangesfrom 0 to 90%, with an averageof about30% (Liker M36 attackedM32, and the copulationattempt turned into & Sz•kely 1999, own unpublisheddata), the two males' in- a territory dispute. cubationcontributions did not differ from the normalpattern. The nest of F27 was found containing two eggs on 3 There are at least two types of potential costsincurred by April, and four eggs on 6 April, suggestingthat the clutch caring for the offspring of other males: (1) reducedtime to was completedon 5 April. At 11:45 and 12:00, on 5 April, court other females and (2) reduced time to care for own M34 madethree attempts to copulatewith F27 duringabout offspring in other nests. We suggestthe following three 20 seconds,but wasrejected each time. At 10:30 on 21 April, hypothesesfor the behaviourof the replacementmale Lap- M34 flew over to F27 andtried to copulatewith her, but she wings: refused.The nestbecame heavily sprayedwith manureon 28 April and was subsequentlydeserted by F27. (1) Brood adoption was adaptivebecause of future repro- From the disappearanceof M30 until F27 desertedthe ductive benefits to the replacement males (Rohwer nest,no successfulcopulations with M34 were observed.He 1986). Lapwings seemto showrelatively high breeding

Bufferin 95 August 2001 Lislevand et aL: Lapwing mate replacement 57

F27

F22

M30

IIIIIIIIIIIIIIIIIIIII IIIIIIIIllll IIIIIIIIIIIIIII IIIIII 20 01 10 20 01 I0 March April May

DATE

Figure 2. Phenoloõ¾of male 30 and the replacementnests. Periodswhen M30 was a bachelor(Ba), monoõamous(Me) and biõamous (Bi) are indicated,toõether with prelayinõ,eõõ laging,incubation and chickrearinõ periods for the females.The date that male 30 disappeared is shown by a vertical line.

site fidelity, and even mate fidelity (Thompsonet al. (3) Paternal care was contributed in relation to male confi- 1994, Parish& Coulson1998, own unpublisheddata). denceof paternity(Meek & Robertson1991). The fe- Thus,because of a relativelyhigh chanceof meetingthe malethat received help from the male wasseen copulat- female again, brood adoption could be viewed as a ing with him afterthe clutchwas completed, while the meansof increasingthe chanceof re-matingin the sub- femalewho incubatedalone rejected the male' s copula- sequentbreeding season. Possibly, it couldalso be a way tion attemptsseveral times. The exactfertile periodof of investingin future matingopportunities later in the femaleLapwings is not known,but is generallythought sameseason, replacement clutches being commonin to last until the laying of the penultimateegg (Birkhead Lapwingsif the first nestingattempt fails (Berg et al. & M011er1992). It is thereforepossible that paternal care 1992, own observations).Another possible benefit of wasassociated with paternitycertainty if the incubating brood adoption to males is that they gain breeding male alsocopulated with F22 duringthe egglaying pe- experiencethat may increasetheir futurereproductive riod.In addition,the egg laying phase of F22 seemedto success.Such a benefitshould be of relativelylittle im- last for aboutone day longerthan normal, possibly fur- portancein our case,however, since the incubatingmale ther increasingthe probabilityof her replacementmale already had a mate with a nest to care for when he fertilizing the last three eggs.Moreover, he could also adoptedthe clutch of his deadneighbour' s female. havefertilized the first eggthat waslaid just prior to replacement,because extra-pair matings have been occa- (2) Male brood adoptionwas maladaptive,but occurstoo sionallyrecorded in the species(own unpublished data). rarely to be selectedagainst (Rohwer 1986). From this view,brood adoption is misdirectedcare, male incubation Female solicitation of copulations may increase the simplybeing a responseto any clutchfound within the chanceof receivinghelp from a replacementmale, either borders of a male's territory. However, this cannot becauseshe is able to deceive him into believing that he adequatelyexplain the differencesin nest attentiveness sharespaternity in theoffspring (Robertson 1990) or because betweenthe two replacementmales described here. Fur- he actuallydoes so (Meek & Robertson1991). If F27 had a ther,males do notalways incubate on all nestswithin their chanceof receivingmale help by copulatingwith M34, her territories(Liker & Szrkely 1999,own unpublished data), motivesfor refusingare not obvious.In fact shehad more indicatingthat male incubation rules are morecomplex to offer thanF22, becauseshe had not laid a singleegg at the in Lapwingsthan assumed by themaladaptive hypothesis. timeher first mate died and therefore could give the replace- menta chanceof fertilizingall her eggs.One possible adaptive reasonfor not doing so could be that her original male Table 1. Male attentiveness,total nest attentivehessby either par- wasof bettergenetic quality than the replacement. ent and total observationtime (hours) on nests of the replacement males. Infanticideshould be adaptiveto replacementmales who do not sharepaternity in the adoptedclutch if the probabil- Male Female Male att. (%) Total aft. (%) Obs. time ity for femalesleaving them after nest failure is low andthey insteadstay and lay a new clutch sired by the new male 34 27 (adopted) 0 71.4 17.2 (Rohwer 1986, Freed 1986, Robertson 1990). In waders, 13 (alpha) 1.2 79.2 22.2 suchbehaviour is known in polyandrousfemale Jacanas 26 (beta) 38.3 74.3 19.5 Jacanasp. (Jenni 1996). Female Lapwings sometimes leave 36 22 (adopted) 12.2 79.2 17.7 their originalmate after clutchpredation (Parish et al. 1997, 40 (alpha) 26.2 74.1 15.5 own unpublisheddata). Thereforethe risk of losinga mate

Bulletin 95 August 2001 58 Wader Study Group Bulletin may meanthat indifference is a betteroption than infanticide Birkhead, T.R. & M011er,A.P. 1992.Sperm Competition in Birds.Evo- for malesin thisspecies. Possibly this is thereason why M34 lutionary causesand consequences.Academic Press,London. took no part in the incubationof F27's eggs.However, as Byrkjedal, I., Gr0nst01, G.B., Lislevand, T., Pedersen, K.M., Sandvik, H. & Stalbeim, S. 1997. Mating systemand territory in Lapwings male care also includesterritory defenceand chasingof Vanellus vanellus. Ibis 139: 129-137. potentialpredators (Parish & Coulson1998, Liker & Sz6kely Dickinson, J.L. & Weathers, W.W. 1999. Replacementmales in the 1999), the female may have gained indirectly from the westernbluebird: opportunity for paternity,chick-feeding rules, and male's presenceeven thoughhe did not carefor her eggs. fitnessconsequences of maleparental care. Behav. Ecol. Sociobiol.45' We believe that hypotheses1 and 3, or a combinationof 201-209. these,are most likely to accountfor thebehaviour that we ob- Freed, L.A. 1986. Territory takeoverand sexuallyselected infanticide •n tropical house wrens. Behav. Ecol. Sociobiol. 19: 197-206. servedin the Lapwing males. Recentpapers indicate that Houston, A.I. 1995. Parentaleffort andpaternity. Anim. Behav.50: 1635- male confidence of paternity often seemsto determine 1644. whether replacement males adopt broods or reject them Jenni, D.A. 1996. Family Jacanidae(Jacanas). Pp. 276-291 in: del Hoyo, (Meek & Robertson 1991, Dickinson & Weathers 1999). In J., Elliott, A. & Sargatal,J. eds. (1996). Handbookof the Birds of the WesternBluebirds Sialia mexicana,for example,males have World. Vol. 3. Hoatzin to Auks. Lynx Edicions,Barcelona. an "all or none" provisioningrule, where normal parental Kermott, L.H., Johnson,L.S. & Brinton, H. 1990. Brood adoptionand apparent infanticide in a north-temperate house wren population. care is providedonly when replacementtakes place during Wilson Bull. 102: 333-336. the females'fertile period(Dickinson & Weathers1999). As Liker, A. & Sz•kely, T. 1999. Parental behaviour in the Lapwing in the presentstudy, data on paternityhave oftenbeen lack- Vanellus vanellus. Ibis 141: 608-614. ing in reportsof male brood adoption,making it question- Meek, S.B. & Robertson, R.J. 1991. Adoptionof youngby replacement able whethermales actually do adopteggs or young,or sim- male birds: an experimentalstudy of easternbluebirds and a review ply take care of offspringsired by themselvesin extra-pair Anim. Behav. 42: 813-820. copulationsor after the original male disappeared.Hence, Parish, D.M.B., Thompson,P.S. & Coulson,J.C. 1997.Mating systems in the Lapwing Vanellus vanellus.Ibis 139: 138-143. carefullydesigned male removalexperiments combined with Parish, D.M.B. & Coulson,J.C. 1998.Parental investment, reproductive paternityanalyses (Kermott et al. 1990, Smith et al. 1996, successand polygyny in the lapwing, Vanellusvanellus. Anim. Behav Dickinson & Weathers 1999) would be very useful to dis- 56: 1161-1167. criminatebetween alternative hypotheses concerning male Robertson, R.J. 1990. Tactics and counter-tacticsof sexually selected replacementbehaviour in the Lapwings. infanticidein Tree Swallows.In Blondel, J. et al. (eds.) Population biology ofpasserine birds: 381-390. Springer,Berlin, Heidelberg& New York. ACKNOWLEDGEMENTS Rohwer, S. 1986. Selectionfor adoptionversus infanticide by replacement "mates" in birds. Current Ornithology 3: 353-395. We are gratefulto D.M.B. Parish,D.B.A. Thompsonand an Smith, H.G., Wennerberg, L. & yon Schantz, T. 1996. Adoptionor in- anonymousreferee for commentson earlier drafts of the fanticide: options of replacementmales in the EuropeanStarling. manuscript.Thanks also to A. Breist01for making the map. Behav. Ecol. Sociobiol. 38: 191-197. TL was supportedby a grantfrom the NorwegianResearch Thompson, P.S., Baines, D., Coulson, J.C. & Longrigg, G. 1994. Age at first breeding,philopatry and breedingsite-fidelity in the Lapwing Council (Project No. 138734/410). Vanellus vanellus. Ibis 136: 474-484. Trivers, R.L. 1972. Parental investment and sexual selection. In: REFERENCES Campbell,B. (ed.), Sexualselection and the descentof man.Pp. 136- 179. Chicago: Aldine. Berg,•., Lindberg,T. & K•illebrink,K. 1992.Hatching success ofLap- Westneat, D.F. & Sherman, P.W. 1993. Parentageand the evolution of wings on farmland: differences between habitats and colonies of parentalbehaviour. Behav. Ecol. 4: 66-77. different sizes. - J. Anim. Ecol. 61: 469-476.

Bulletin 95 August 2001 Features of breeding biology in Pacific and American Golden-Plovers nesting on the Seward Peninsula, Alaska

OSCAR W. JOHNSON*t, PHILLIP L. BRUNER2, ANDREA E. BRUNER2, PATRICIA M. JOHNSON •, RONALD J. KIENHOLZ 3 & PAUL A. BRUSSEAU 4

•Dept.of Ecology,Montana State Univ.,Bozeman, MT 59717, USA, e-marl:owjohnson2105@aol. com; 2Dept.of Biology,Brigham Young Univ.-Hawaii, Laie, HI 96762,USA; 3210 7th St. N.E.,Dfiworth, MN 56529,USA; 4po Box 142375,Anchorage, AK 99514, USA

Johnson, O.W., Bruner, P.L., Bruner, A.E., Johnson, P.M., Kienholz, R.J. & Brusseau, P.A. 2001. Features of breedingbiology in Pacificand American Golden-Plovers nesting on the SewardPeninsula, Alaska. Wader Study Group Bull. 95: 59-65.

We studiedsite-fidelity, nesting, and the chronologyof hatchingin Pacific and AmericanGolden-Plovers (Pluvialisfulva andP. dominica)from 1988 to 2000 on breedinggrounds near Nome, Alaska. Bandedmales of both specieswere stronglysite-faithful in subsequentseasons with 12 of 16fulva and 11 of 15 dominica (at returnrates of 77% and 80%, respectively)nesting near, and occasionallyin, previousnests. The fidelity of malesdid not appearto be reducedby lack of breedingsuccess, suggesting that familiaritywith a territory is of primary importance.Among females,only 2 of 12fulva and 1 of 11 dominica (at return rates of 25% and 15%, respectively)were seenin subsequentseasons. Each of thefulva femaleswas presentfor threecon- secutiveseasons including the seasonwhen captured;one matedwith the samepartner for two seasons,the other with the samemale in all seasons.The singledominica female paired for one seasonwith a different matethan shehad when captured. We estimatedthat dominica females produced replacement clutches in 12- 14 daysafter lossof the first clutch.Hatching began in late Juneand intra-clutchchronologies were similar in each species.The first indicationsof hatchingwere hairline cracksthat appeared5-50 hoursbefore more obviousbreakage (star-pip or tiny pip-hole).Most eggsprogressed from the latter conditionsto emergence of a chick in 10-20 hours.Intervals from the first hairline-crackedshells and the first obviousbreakage of shellsto four dry chicksin andaround the nestwere approximately2-4 daysand 1-3 days,respectively. Brood membersemerged sequentially over the courseof aboutone day, and often at leasttwo chickswere already foragingnear the nestbefore the last sibling had appeared.

INTRODUCTION nesting-sitefidelity in male shorebirdstogether with additional referencesis providedby Flynn et al. (1999). The Pacific Golden-Plover Pluvialis fulva and American Our studieson the SewardPeninsula began in 1988, and Golden-Plover P. dominica are seasonallymonogamous someof theplovers we bandedin earlieryears survived after shorebirds with male-biased breeding ground fidelity initial accountsof sitefidelity were published(Johnson et al. (Greenwood 1980, Johnsonet al. 1993, 1997a, Sviridova 1993, 1997a). We continuedto recordtheir breedingactivi- 2000). Males (sexesare dimorphicin breedingplumage) ties in subsequentseasons, and alsomarked additional birds. establishthe territories,build nests,and perform most defen- General knowledgeof reproductivebiology in Pacific and sive behaviours (Connors et al. 1993, Johnson & Connors American Golden-Plovers is reasonablygood, but many 1996, Byrkjedal & Thompson1998). Returningto a famil- detailsare lacking(Johnson & Connors1996, Piersmaet al. iar placepresumably lessens intra-sexual competition among 1997,Byrkjedal & Thompson1998). In thispaper, we quan- males and facilitates rapid re-occupancy in the spring tify fidelity more thoroughlyby combiningdata on return- (Greenwood& Harvey 1982, Flynn et al. 1999, Sviridova ing birdsin all seasonsup to and including2000, and report 2000). However,variation in the qualityof a male's territory findingson interannualspacing of nests,re-nesting, and time (relatedto timing of snowmelt)may reducehis attractiveness intervals associatedwith hatching. to femalesin certainseasons. Although some pairs probably form before arrival on breeding territories (Sauer 1962, STUDY AREAS AND METHODS Connors et al. 1993, Johnson & Connors 1996, Sviridova 2000), the responseof mostfemales to variable springcon- We conducted fieldwork from 1988 to 2000 at two sites on ditions appearsto be site-unfaithfulopportunistic pairing golden-plover breeding groundsnorth of Nome, Alaska. with males possessingsuitable territories (Tomkovich & Most data are from the Feather River site, an area of about Soloviev 1994, Johnsonet al. 1997a). A useful overview of 550 ha near mile 37 on the Nome-Teller Road (64ø5 I'N,

* Correspondingauthor

59 Buffetin 95 August 2001