Phylogenetic Patterns of Parental Care in Calidridine Sandpipers

The Auk 116(4):1107-1117, 1999

PHYLOGENETIC PATTERNS OF PARENTAL CARE IN CALIDRIDINE SANDPIPERS

OKSANA A. BOROWIK • AND DEBORAH A. MCLENNAN 2'3 •RoyalOntario Museum, 100 QueenõPark, Toronto,Ontario M5S 2C6, Canada;and 2Departmentof Zoology,Centre For Comparative Biology and Biodiversity, University of Toronto,25 HarbordStreet, Toronto,Ontario M5S 3G5, Canada

ABSTRACT.--Weexamined the sequenceof parental-careevolution in calidridinesandpip- ersby mappingparental-care characters onto the two treesproduced by a maximum-like- lihoodand parsimonyanalysis of moleculardata. Our analysisindicated that asymmetric biparentalcare (male incubates and caresfor young,female incubates) is plesiomorphicfor the group.This state has been maintained in at least10 of the 22 speciesinvestigated. There havebeen four changesfrom the ancestralcondition: (1) three to four increasesin female carecoupled with a completeloss of male care;(2) an increasein femalecare with the maintenanceof male care,producing symmetric biparental care; (3) an increasein femalecare followed at a later date by three independentlosses of male care in Calidrismelanotos, C. fuscicollis,and Tryngitessubruficollis; and (4) a decreasein female care in C. pusilla.Received 23 May 1997, accepted20 April 1999.

QUESTIONSABOUT the evolutionof avianpa- systemsin all birds (vanRhijn 1990:160),(2)fe- rental care have fascinated researchers for de- male-only care is extremelyunlikely to evolve cades,in part becausebirds show such a wide into anothercare pattern,and (3) biparental range of strategiesand becausethe factors careis unlikely to evolveinto either type of uni- shapingthe evolutionof thesestrategies are parentalcare if both parentsshare incubation very complex(Clutton-Brock 1991, Ligon 1993, duties.Both models make very explicitpredic- Ketterson and Nolan 1994, Temrin and Sill•n- tionsabout the sequenceof parental-careevo- Tullberg1994). Given this complexity,one way lution that canbe examinedwithin a compar- to disentangleall of the potentialfactors is to ative framework. break the systeminto simple,definable com- The phylogeneticcomparative approach is a ponentsand model the interactionsamong powerfulway to disentanglecharacter origin them.There are two generalscenarios for the from subsequentcharacter modification and to sequenceof parental-careevolution in Aves. study the sequenceof charactermodification The first (Fig. 1A) proposesthat uniparental over long periodsof time (Ridley 1983,Wann- care alwaysarises from biparentalcare, with torp 1983, Brooks 1985, Brooks and McLennan the sexof the singleparent being determined 1991).One of the strengthsof this approachis by the relativecosts and benefits of careversus that it allows the collection of data about the desertionto eachparent (Jenni1974, Pitelka et types of evolutionarytransitions that hap- al. 1974,Emlen and Oring 1977).Hild•n (1975) pened most often, that happened once and postulatedthat the intermediatestate between were maintained for long periods of time, and biparentaland uniparental care might be a sys- thatnever happened within a givenclade. This tem in which the female rapidly laid two informationmay then be used to examinethe clutchesof eggs(double clutching), each clutch beingcared for by oneparent. Van Rhijn (1985, predictions of evolutionary models and to 1990;see also Handford and Mares 1985) pro- highlightareas in the modelsthat need to be poseda more complicatedscenario (Fig. lB). In modified (Brooks and McLennan 1991, 1994; its simplestform, this scenariomakes three McLennan 1996). general predictions:(1) male parental care is McKitrick(1992) investigated the macroevo- the precursorto the radiationof parental-care lutionary patterns of parental-careorigin and diversificationacross major avian lineages. She concludedthat the ancestralparental-care sys- 3Address correspondence to this author.E-maih tem for Aves was either asymmetricor sym- [email protected] metricbiparental care (biparentalor femalein-

1107 1108 BOROWIKAND MCLENNAN [Auk, Vol. 116

(A) Imale parental care]-'•'---•- biparental care• femaleparentalcare

a I biparentalcareI

increasedcarebysecond maleparental care filr•parent i [femaleparentalcare ] FIG.1. Pathwaysof parental-careevolution postulated by (A) Emlenand Oring (1977)and (B) van Rhijn (1990).Bold arrows denote the mostprobable transitions, and light arrowsdenote unlikely transitions. cubation + biparental care of young). In no althoughwe can infer its presencebecause casedid the analysissupport the hypothesis maledesertion of the clutchpresumably could that male-onlycare was the ancestralstate for not existprior to theorigin of increasedfemale birds. Sz6kelyand Reynolds(1995) narrowed investment.In the secondcase, biparental care the scopeof the investigationto oneavian lin- is detectableon a macroevolutionaryscale (still eage,the Charadriides(excluding Labroidea). present in extant species).The comparative The macroevolutionarypatterns indicated that phylogeneticanalysis thus indicated that mod- biparental care (not male-only) was plesio- els of parental-careevolution should incorpo- morphicfor this groupof shorebirds,reinforc- rate informationabout the factorsinfluencing ing McKitrick'sconclusion that paternal care the rate of a population'smovement through couldnot be viewedas the precursorto all oth- thebiparental state into the explanatoryframe- er parental-caresystems. Within the group, the work. dominant transitionswere male-only to bipa- McKitrick (1992) examined patterns of parental (5 to 11 times),male-only to female-only rental care on a large scale,whereas Sz6kely (6 to 8 times)and biparentalto male-only(2 to and Reynolds(1995) narrowed their focusto 6 times).Transitions from biparentalto female- the shorebirds.Continuing in this vein,we in- only careand vice versawere very rare (0 to 3 vestigatedthe sequenceof parental-careevo- timeseach). The data confirmedprevious sug- lutionwithin onegroup of shorebirds,the cal- gestionsof a link between male-only and bi- idridine sandpipers.We chosethis group be- parentalcare and confirmedvan Rhijn's(1990) causerelationships within it have been ana- predictionthat biparentalto female-onlycare lyzed phylogenetically(Borowik 1996), and should be rare. becausesandpipers display a wide rangeof pa- Theanalysis also highlighted two interesting rental-care strategies. We were interested pointsfor furtherresearch. First, there has been mainly in (1) discoveringwhether the domi- a trend toward increasingfemale carerelative nantsequences of parental-careevolution with- to malecare in shorebirds.The authors hypoth- in the sandpiperswere similarto thosedetect- esized that sexual selection favors male deser- ed on a largerphylogenetic scale, and (2) using tion becauseextrapair copulations present the the powerof the comparativephylogenetic ap- only meansopen to a male to enhancehis re- proachto highlightareas for futureresearch. productive success.Second, the transition

"male-only to female-only" care is far more MATERIALS AND METHODS likely to occurthan is the sequence"male-only to biparentalto female-only"care (seeFig. 1). Data on parentalcare were obtainedfrom Pitelka The only differencebetween these two transi- et al. (1974),Johnsgard (1981), Sz6kely and Reynolds tionsis the persistenceof the intermediatebi- (1995),and sourceslisted in the Appendix.As sug- parentalstage. In the first case,biparental care gested by Temrin and Sil16n-Tullberg(1994), we is transitoryfrom a phylogeneticperspective, mapped parental-carebehavior separately for the October1999] ParentalCare in Sandpipers 1109

(ancestor2) J

Femaleonly incubates [] I FI•. 2. Parental-carestates optimized onto the most-parsimonioustree for calidridinesandpipers based on a maximum-likelihoodanalysis of 1,645characters (1,045 base pairs from cytochromeb, 600 basepairs from ATPase6; Borowik1996). Outgroups = BlackTurnstone (Arenaria melanocephala) and Ruddy Turnstone (A. interpres).Female care: white box = femaleincubates, black box = femaleincubates and caresfor young; malecare: white box = maleincubates and cares for young,black box = no malecare. Crosses = lossof male parentalcare, asterisk = reductionin femalecare, and F = increasein femalecare. See Figure 5 for the four equallyparsimonious optimizations of parental-careevolution in the Philornachuspugnax + Lirnicolafalcinellus + C. acurninata clade. sexesso that we couldstudy the interactionbetween of the genusCalidris and alsoin the additionof C. differentlevels of maleand femalecare. Based upon rninuta,C. ptilocnernis,C. subrninuta,C. tenuirostris, the data collected,we divided parentalcare into two Limicolafalcinellus, Aphriza virgata, and Philomachus characters:(1) male care(either male care absentor pugnaxto the analysis.Arenaria melanocephala and male incubatesand caresfor young),and (2) female Arenariainterpres were used as outgroups.Optimi- care (either female incubatesor female incubatesand zationswere checkedon McClade 3.01, using the caresfor young).Parental-care states were coded dif- Acctranand Deltran algorithms,but more options ferentlyfrom thoselisted in Sz•kelyand Reynolds werediscovered in a hands-onanalysis because com- (1995)for the followingspecies: (1) femaleincuba- puterprograms did not allow a combinationof both tion was added to Calidrisalpina, C. canutus,C. rnar- Acctranand Deltran optimizations for onecharacter. itima, C. pusilla,and C. ruficollis;and female incubation and care for young was added to C. bairdii,C. RESULTS mauri,and C. minutilla(see Appendix). The evolutionof parental-carebehaviors was ex- Optimizing parental-carestates onto both aminedby optimizing(Farris 1970, Maddison et al. trees indicates that "male iv•ubates and cares 1984)the behavioralstates onto two equallyparsi- moniousmolecular-based phylogenetic trees for the for young + femaleincubates then leaves"is calidridine sandpipers(details of tree construction the plesiomorphiccondition for parentalcare in Borowik1996). The phylogeneticpatterns used in in the calidridinesandpipers from which a this analysisdiffer from those used by Sz•kelyand numberof changesin parentalcare have oc- Reynolds(1995) in the relationshipsamong members curred (Figs. 2 to 4). All optimizationsagree 1110 BoRowmAND MCLENNAN [Auk, Vol. 116

MaleincubatesFemaleonly and incubates caresforyoung[] [] ] I F•G.3. Parental-carestates optimized onto the most-parsimonioustree for calidridinesandpipers based on a parsimonyanalysis of 1,645characters (1,045 base pairs from cytochromeb, 600base pairs from ATPase 6; Borowik1996). See Figure 2 for explanationof symbols. that (1) an increasein femalecare is coupled careand decreasein male carewere coupledin with a lossof male care in Calidrisferruginea; T. subruficollis(Fig. 4). Finally, both trees sup- (2) loss of male care has occurred indepen- port four equallyparsimonious, but complicat- dently in C. melanotos,C. fuscicollis,and Tryn- ed, optimizationsfor the evolutionof parental gitessubruficollis; and (3) lossof male carein C. carein the Philomachuspugnax + Limicolafalci- melanotosand C.fuscicollis occurred after an in- nellus+ C. acuminataclade (Fig. 5). crease in female care in a distant ancestor of the two species. DISCUSSION The sequenceof eventsproducing the parental systemof T. subrufi'collisis ambiguous, as is Our results indicate that asymmetricbipa- the position of this species.According to the rental care,with the femaleincubating and the maximum-likelihoodtree (Fig. 2), T. subruficol- male both incubatingand brooding,is the an- lis lost male care following an increasein fe- cestral condition for calidridine sandpipers. male care in ancestor2. One of the optimiza- This result mirrors Sz6kely and Reynolds' tions on the maximum-parsimonytree also (1995) conclusionsthat biparentalcare is an- producesthis pattern,although it pushesthe cestral for the shorebird infraorder Charadri- origin of an increasein femalecare back to an- idesand doesnot supportvan Rhijn'ssugges- cestor1 (Fig. 3) and, as a consequence,requires tion that male-onlycare is the precursorto all that a subsequentdecrease in femalecare oc- other forms of parental care in birds (Charad- curredin the ancestorof the C. alpina+ C. mar- riiformesor otherwise).Our resultsalso indi- itima + C. ptilocnemisclade. It is equallyparsi- cate that asymmetricbiparental care forms a monious on the maximum-parsimonytree, strongancestral backbone within theclade: 7 to however,to suggestthat the increasein female 10 of 22 speciesretain the symplesiomorphic October1999] ParentalCare in Sandpipers 1111

MaleincubatesFemale0nly and incubates caresforyoung[] [] I F•c. 4. Deltran optimizationof parental-carestates on the maximum-parsimonyphylogenetic tree for calidridinesandpipers. See Figure 2 for explanationof symbols.

increasefemalecare [increasefemalecare

N N•4increasefemalecare ]increase femalecare••?• ]] increase femalec• ' F•c. 5. Fourequally parsimoniousalternatives for the evolutionof parentalcare in the Philornachuspugnax + Limicolafalcinellus + C. acuminataclade. White box = decreasein female care,black box = lossof male care. 1112 BOROWIKAND MCLENNAN [Auk, Vol. 116

5 extant spp + 8 ancestors femaleincubates//•equally biparentalI• 11ext'ntIm•e s•"'incu--bates+brøødsl+•3ancestørs •3• le•Ytr•it• •3• •l•xø-•a•-•s•l•ppf•m•!cestørs 0 extant spp + 0 ancestors FIG.6. Evolutionarypathways of parental-careevolution within calidridinesandpipers. condition(Figs. 2 to 4). Many biologistshave lomachuspugnax + Limicolafalcinellus + C. ac- tended to focus their attention on differences uminataclade (Fig. 5, lowerright), do the pat- amongspecies in a group.We believethat it is ternssuggest that it is possibleto reducepa- also important to (1) formulatetestable hy- rental carebelow the amountprovided by the pothesesabout the proportionsof a behavioral symplesiomorphicasymmetric biparental con- systemthat do not changeacross long periods dition.The hypothetical loss of malecare in the of time, and (2) documentthe frequenciesof ancestorof that cladewould haveproduced a stasisversus divergence in order to determine populationin whichonly females incubated the whethersuch frequencies are character-specif-eggs and neitherparent provided any carefor ic, clade-specific,or a combinationof the two. the hatchlings.This ancestoris no longeravail- From the perspectiveof macroevolutionary able for examination,so we can never fully re- patterns,the term "stasis"is usedto indicatea solvethis situation.However, given that none lack of changein a particularcharacter across of the other calidridinesandpipers, including two or more speciationevents. The macroevo- the extantmembers of the P.pugnax + L. falci- lutionary patternsallow us to recognizea pu- nellus+ C. acuminataclade, displays such a de- tativecase of stasiswithout implying anything creasein parentalcare, the sequencedepicted aboutthe underlyingmechanisms, which must in the lower right of Figure 5 probablyrepre- be soughton genetic,selective, functional, and sentsa situationin whichmethodological pos- developmental levels (Carrier 1991, Arnold sibilitycan be discountedon biologicalgrounds. 1992, McKitrick 1993, Bj6rklund 1996). Recog- Although ambiguitiesexist concerningthe nition of stasisis important,however, because exact number of times that female care was in- it highlightsareas for future research.For ex- creased and male care was lost in calidridines, ample, do similaritiesoccur in ecologicalcon- a consistentpattern emerges within this group ditions,life-history parameters, and/or social of birds. In all cases,the increasein female care structureof the speciesretaining the symple- to includeboth incubationof eggsand brood- siomorphicparental care system that couldbe ing of youngeither co-occurredwith, or pre- operating as stabilizing selectionon parental ceded,the loss of male care. Thesepatterns carein thesebirds? Alternatively, is a portion highlight three possibleareas for future re- of the observedstasis an artifactof missingin- search.First, all optimizationssuggest that one formation,or incorrectcharacter coding? Only increasein female parental investmentis bur- by collectingthese data can we begin to for- ied deepwithin the evolutionaryhistory of the mulatemore complete hypotheses of behavior- calidridine sandpipers;i.e. at least as far back al evolution,hypotheses that canexplain both asancestor 2 (Figs.2 and 4) and possiblyearlier the origin, maintenance(stasis), and diver- (Fig. 3). This increasein femaleparental care, genceof behavioralsystems. to matchthat alreadydisplayed by males,was Parental care diverges from this ancestral maintainedin the majority of descendantsof asymmetric biparental backbonein two dis- eitherancestor 1 or ancestor2 (yetmore stasis). tinct ways, involving (1) an increasein female This suggeststhat somethingis differentabout parentalinvestment indicated by the origin of thesedescendant species that favored the main- female brooding behavior,and (2) a loss of tenanceof an increasein overall parental in- male parentalinvestment. In no case,with the vestmentonce it originated.The mostobvious exceptionof one optimizationwithin the Phi- placesto look for derivedchanges that might October1999] ParentalCare in Sandpipers 1113

be coupledwith this increasein parentalcare progenyproduced. The fact that paternal in- are in the ecologyof the parents(e.g. availabil- vestmenthas been lost in at leastthree lineages ity of food,length of breedingseason, preda- indicates that there must have been a concom- tion pressure)and/or the developmentof the itant increasein someother aspectof overall young (increasein the lengthof development male fitnessto balancethe negativeeffect of from the ancestralprecocial state; Emlen and male desertionon offspringsurvivorship. For Oring 1977, Temrin and Sil16n-Tullberg1995). example,freeing males from the bondsof pa- Second,all optimizationssuggest that the in- rentalcare may have been coupled with an increasein female care was secondarilylost in creasein the ability of malesto pursuealter- Calidrispusilla, creating a changefrom sym- native reproductiveoptions (Maynard Smith metric to asymmetricbiparental care.Demon- 1977). Tryngitessubruficollis is a lekking spe- stratingthat a changein ecologyand/or de- cies,C. fuscicollisis polygynous,and C. melan- velopmentof theyoung was correlated with the otoshas been described as promiscuous. We are increasein femalecare ancestrally, and thatthe currentlyinvestigating the patternsof mating- derived ecology and/or developmentsubse- systemevolution in this clade to determine quentlyunderwent a reversalcorrelated with whetherthe patternsshown by thesethree spe- the decreasein femalecare in C. pusilla,would ciesare derived from monogamy. If so,then we providestrong macroevolutionary evidence for will have demonstrated that the ancestral in- a causalrelationship among the variables. Once crease in female care created the conditions detected, such macroevolutionaryevidence within whichmales could be releasedfrom pa- formsthe basisfor experimentalinvestigations rental duties. The creation of such conditions, of the hypothesizedrelationship (McLennan however,does not explainwhy malesin these 1996).These patterns also indicate that "asym- particularspecies were ableto exercisethat op- metricbiparental care" in C. pusillais not ho- tion,nor doesit explainwhy malesfrom many mologouswith the samestate in othercalidri- of their close relatives remain bound to their dine sandpipers.The origin of the asymmetric offspring.To disentanglethese two issues,we biparentalcare system predates the origin of need to collectinformation about a variety of the calidridinesandpipers and thus is buried factors,including the effectsof male care on deep within the phylogenetichistory of birds. offspring survival, the effect of female-only Thereare only two waysin whichwe canre- careon female fecundity, offspring growth pat- constructthe forcesthat shapedthe original terns,and the availabilityof fertilefemales for successof suchold systems:(1) examineall of additionalmating attempts by males(Maynard the factorsinfluencing the maintenanceof the Smith 1977, Kettersonand Nolan 1994). plesiomorphictrait in extantspecies, optimize In summary,the resultsfrom our analysis those results onto the tree, and extrapolate providestrong support for the suggestionthat backwardto the point of origin;or (2) investi- biparental care forms a bridge between pre- gatethe forcesshaping the evolutionof the an- dominantly male and predominantly female cestralsystem if it reappearsas a reversal(au- care.In approximatelyhalf of the casesnoted, tapomorphy)in an extantspecies (Brooks and the biparentalstage persistedevolutionarily McLennan 1991, McLennan 1996). throughseveral speciation events before the Third, both treessuggest that male parental transitionto female-onlycare occurred (cf. Fig. carehas beenindependently lost in Tryngites 1A). In the otherhalf of the cases,the increase subruficollis,Calidris melanotos and C.fuscicollis. in femalecare and subsequentloss in male care Althoughstudies attempting to documentthe were coupledphylogenetically, indicating that fitnessconsequences of removingmales from a the transitionleading to a dramaticshift in pa- biparentalsituation have producedequivocal rental care systemcan occurrelatively rapidly results,those results tentatively indicate that (cf. Fig. lB). Theseresults do not support van males may be essentialfor successfulrepro- Rhijn's(1990) prediction that biparentalcare is ductionwhen they share the incubationduties unlikelyto evolveinto eithertype of uniparen- (Erckmann 1983, Dunn and Hannon 1989, Ket- tal careif both parentsshare incubation duties. tersonand Nolan 1994).In otherwords, reduc- They do, however,support van Rhijn's(1990) tion in malecare may have a negativeeffect on predictionthat female-onlycare is extremely malefitness by decreasingthe number of viable unlikely to evolveinto anotherparental-care 1114 BOROWIKAND MCLENNAN [Auk, Vol. 116 pattern.No evidencefor the transition"female- associations. Annals of the Missouri Botanical only careto male-onlycare" was uncovered for Garden 72:660-680. theshorebirds (Sz•kely and Reynolds 1995, this BROOKS,D. R., ANDD. g. MCLENNAN.1991. Phylog- study),and the transition"female-only care to eny,ecology and behavior:A researchprogram biparentalcare" was eitherabsent (this study) in comparativebiology. University of Chicago Press,Chicago. or rare (Sz•kelyand Reynolds1995), indicating BROOKS,D. R., AND D. g. MCLENNAN. 1994. Histor- that male care, once lost, is difficult to evolve ical ecologyas a researchprogram: Scope, lim- again.The overallpattern of symplesiomorphy itationsand the future.Pages 1-27 in Phyloge- depictedin Figures 2 to 4 indicatesthat pre- netic approachesto ecology(R. I. Vane-Wright dominantmale care, in the formof asymmetric and P. Eggleton,Eds.). Academic Press, London. biparentalcare, has been very stablethrough- CARRIER,D. R. 1991.Conflict in the hypaxialmus- out the evolutionaryhistory of calidridines. culo-skeletalsystem: Documenting an evolu- Overall, these patterns are consistentwith tionary constraint.American Zoologist31:644- Maynard Smith's(1977) fundamentalinsight 654. that forcesoperating on malesand femalesare CARTAR,R. V., ANDB. E. LYON.1988. The matingsys- evolutionarilyinterdependent throughout the tem of the Buff-breastedSandpiper: Lekking and resourcedefence polygyny. Ornis Scandi- evolutionof parental-caresystems and that, navica 19:74-76. within birds, someform of biparentalcare gen- CARTAR,R. V., AND R. D. MONTGOMERIE.1985. The erally shouldprevail over mate desertion. influenceof weatheron incubationscheduling of theWhite-rumped Sandpiper: A uniparentalin- ACKNOWLEDGMENTS cubator in a cold environment. Behaviour 95: 261-290. We thankD. R. Brooks,B. Moore,and two anony- CARTAR,R. V., ANDR. D. MONTGOMERIE.1987. Day- mous reviewers for their comments on the manu- to-dayvariation in nestattentiveness of White- script.We are particularlygrateful to P. Chu for his rumped Sandpipers.Condor 89:252-260. thoughtfulreview. This researchwas funded in part CLUTTON-BROCK,T. H. 1991.The evolutionof paren- by NSERC operatinggrants to A. J. Baker and D. A. McLennan. tal care. PrincetonUniversity Press,Princeton, New Jersey. COOPER,J. M. 1994.Least Sandpiper (Calidris minu- LITERATURE CITED tilla). In The birds of North America, no. 115 (A. Pooleand E Gill, Eds.).Academy of Natural Sci- ANDREEV,A. V. 1980.A nestingbiology study of the ences,Philadelphia, and American Ornitholo- Great Knot (Calidristenuirostris) in the River Ko- gists'Union, Washington, D.C. lyma basin. Ornitologiya 15:207-208 [in Rus- COOPER,J. M., AND E. H. MILLER. 1992. Brood amal- sian]. ARNOLD,S. J. 1992.Constraints on phenotypicevo- gamation and alloparental care in Least Sand- lution. 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and other charadriiformspecies. Ardea 73:25- WANNTORP, H.-E. 1983. Historical constraints in ad- 37. aptationtheory: Traits and non-traits.Oikos 41: VAN RHIJN,J. G. 1990.Unidirectionality in the phy- 157-160. logeny of socialorganization, with specialref- erence to birds. Behaviour 115:151-173. Associate Editor: R. M. Zink

APPENDIX.Sources of informationon parentalcare in calidridinesandpipers. Ruddy Turnstone is the outgroup.

Species Source Surfbird(Aphriza virgata) Jehl 1968; Strauch1976; Miller et al. 1987 Sharp-tailedSandpiper (Calidris acurninata) Britton 1980 Sanderling(C. alba) Parmelee1970; Parmelee and Payne1973; Hild•n 1975;Pienkowski and Green1976; Myers et al. 1980 Dunlin (C. alpina) Holmes 1966; Soikelli 1967; Norton 1972; Jehl 1973; Miller 1983b; Jonsson1987 Baird'sSandpiper (C. bairdii) Drury 1961;Parmelee et al. 1967;Norton 1972;Myers et al. 1982;Reid and Montgomerie1985 Red Knot (C. canutus) Hobson1972; Prater 1972; Nettleship 1974; Dorogoy 1982 Curlew Sandpiper(C. ferruginea) Holmes and Pitelka 1964 White-rumpedSandpiper (C. fuscicollis) Drury 1961;Holmes and Pitelka 1962;Parmelee et al. 1968;McCaffery 1983; Cartar and Montgomeri 1985, 1987; Parmelee 1992 Stilt Sandpiper(C. hirnantopus) Flint 1973;Jehl 1973; Miller 1983b Purple Sandpiper(C. rnaritirna) Bengston1970, 1975 WesternSandpiper ( C. rnauri) Holmes 1971, 1972, 1973; Tomkovich and Morozov 1980;Myers et al. 1982 PectoralSandpiper ( C. rnelanotos) Pitelka 1959;Norton 1972;Myers 1982 Little Stint (C. rninuta) Hild•n 1978; Cramp and Simmons1983 LeastSandpiper (C. rninutilla) Jehl1973; Miller 1979,1983a, b, 1985,1986; Cooper and Miller 1992;Cooper 1994 Rock Sandpiper (C. ptilocnernis) Myers et al. 1982 SemipalmatedSandpiper (C. pusilla) Norton 1972; Ashkenazie and Safriel 1979; Gratto et al. 1983, 1985; Miller 1983b; Gratto-Trevor 1991, 1992 Red-neckedStint (C. ruficollis) Flint 1980;Myers et al. 1982 Long-toedStint (C. subrninuta) Tomkovich1980; Myers et al. 1982 Great Knot (C. tenuirostris) Andreev 1980;Flint 1980;Myers et al. 1982;Tomkov- ich 1995 Broad-billedSandpiper (Lirnicolafalcinellus) Flint 1973 Ruff (Philornachuspugnax) Hogan-Warburg1966; Van Rhijn 1985,1990; H6glund and Alatalo 1995 Buff-breastedSandpiper (Tryngites subruficollis ) Hogan-Warburg1966; Prevett and Barr 1976;Myers 1979, 1980;Cartar and Lyon 1988;Pruett-Jones 1988; Lanctot and Laredo 1994; Lanctot 1995 Ruddy Turnstone(Arenaria interpres) Parmeleeet al. 1967;Nettleship 1973