Mechanisms of Avian Egg Recognition: Possible Learned and Innate Factors

MECHANISMS OF AVIAN EGG RECOGNITION: POSSIBLE LEARNED AND INNATE FACTORS

STEPHEN I. ROTI-ISTEIN

THE belief that at least some passerinebirds reject nonmimetic eggs placedin their nestswas confirmedlong ago by the experimentsof Swyn- nerto.n (1916, 1918) and Rensch (1924). The latter worker (Rensch 1925) went on to questionwhether such birds actually recognizetheir own eggs(rejection by true egg recognition)or whetherthey simply reject any eggthat differs from the majority (rejectionby discordancy).Rensch was interestedin egg recognitionbecause he believedit to be vital to the evolutionaryinteractions between brood parasitesand their hosts. Whether birds rejected eggson the basis of true recognitionor discordancy,the behaviorwould still function as an efficient antiparasiteadaptation because broodparasites generally deposit only one eggin eachhost nest. Although Rensch's(1925) experimentshave been widely interpretedas demonstrat- ing rejection by discordancy(e.g. Welty 1963), the bulk of his results actually indicate true egg recognition(Rothstein 1970). Numerous recent experimentsand a literature reviewsuggest that most or all passefines that reject foreign eggspractice true egg recognition (Rothstein 1974). Nearly all these recent experiments,though, were conductedon birds that had completedtheir clutch. The fact that birds that reject foreign eggspractice true egg recognitionafter completingtheir clutch prompts two significant questions: (1) Is this recognitionas highly developedat earlier stagesof the breedingcycle? (2) Which componentsof rejection by true egg recognitionare primarily learned and which are primarily innate? This paper reports on experimentsthat were designedto deal with these two questions. The new experimentsreported here were done on naturally breeding Gray Catbirds (Dumetella carolinensis). Previous experimentsshowed that catbirds are extremely intolerant of foreign eggs placed in their nests. Singleartificial or real cowbirdeggs experimentally added to 30 catbird nests in eastern North America (Connecticut, Maryland, and Michigan) were all removedby the catbirds. Catbirdsin westernNorth America (Manitoba and Nebraska) may be slightly more tolerant, with 22 of 25 nestsyielding ejectionsof singlecowbird eggs. In 17 additional catbird nests (from Connecticutand Maryland), where experimentsre- sulted in clutchesconsisting of only cowbirdeggs or of only one catbird egg and two or more cowbird or other type of foreign eggs, the catbirds ejectedthe foreigneggs in everyinstance (see Rothstein 1974 for deta/ls).

796 The Auk 91: 796-807. October 1974 October 1974] .4vian Egg Recognition 797

Friedmann (1963) has stated that while suchintolerance of foreign eggs servesas an efficient host defenseit is probably not evolvedin response to broodparasitism. I suggestthis intolerancecan be explainedonly in terms of an adaptation that evolved becauseit protects birds from brood parasites. This is the most parsimoniousexplanation, as rejectingforeign eggsdoes not seemto have any adaptive value in most birds, other than in the contextof broodparasitism (Rothstein 1970, MS). Althoughcatbird and cowbirdeggs differ little in size (averaging23.3 x 17.5 mm and 21.45 x 16.42 mm, respectively,according to Bent 1948, 1958), they are strikingly different in colorationand thus providea valuable pair for experimentation.Catbird eggsare immaculatewith a blue- green ground color whereascowbird eggsusually have a whitish ground colorand are heavily mottled with brownand gray spots. Previouswork by Tschanz (1959) has shownthat in a nonpasserine, the CommonMurre (Uria aalge), egg recognitionis realized througha learning process. In the case of a passerine,the Village Weaverbird (Ploceus cucullatus), it has been suggestedthat egg recognitionis also learned (Victoria 1972). Given the variable nature of murre and weaverbird eggsthese findings might not be unexpected.The eggsof most song- birds, the catbird included, show little variation and egg recognition through largely innate means might not be difficult to evolve. Never- thelessthe hypothesisof egg recognitionby learning will be supported by a demonstrationof greater tolerancetoward a foreign egg type in the early stagesof the breedingcycle than in later stages. If egg recognition has a learning component,greater tolerancein the early stagesof the nestingcycle would be expectedwhether the birds learn the appearance of their eggsanew with each breedingattempt, or whetherthe learning occursonly in completelynaive individualsduring the first nesting attempt of their lives. In the latter casethough, increased acceptance early in the cycle would occur only at those nests tended by naive birds. Un- fortunately it is impossibleto determine whether the catbirds tested in the experimentsreported here were naive or experienced;but given the high mortality of passerinesit is reasonableto assumethat within any seriesof nestsexperimented upon in the field somewill be tendedby naive and others by experiencedindividuals. Much of what follows is relevant only to the catbird and to other speciesthat I have termed "rejecters." Experimentswith cowbird eggs have shown little intraspecificvariation in responseto artificial cowbird parasitism. A minority of North American speciesreject cowbird eggs at nearly 100% rates. These are the rejecters. Most speciesaccept the eggs at nearly 100% rates and are termed "accepters." Rejecter and 798 STEPH• I. ROTHST•n• [Auk, Vol. 91 accepter specieshave presumably respondedand not responded,respectively, in a major way to the evolutionarypressures of brood parasites (Rothstein 1970). As accepter speciesdemonstrate little or no egg recognition (except under special circumstances(Rothstein 1970, MS)), questionson their acquisitionof this behavior have reduced relevancy.

METItODS AND CONTROLS FOR ARTIFICIAL EGGS

The artificial eggs used in most experiments were cast in plaster of paris and painted with artist's paints of the acrylic polymer type. Artificial cowbird and catbird eggs were also shellacked. I have elsewhere (Rothstein 1970, 1974) described the production and properties of these eggs in greater detail. Suitable controls for artificiality of the eggs have been performed. For example, at four nests all four of the catbirds' own eggs were replaced with one artificial catbird egg plus three artificial cowbird eggs. In all four cases the cowbird eggs were ejected while the artificial catbird egg was left in the nest. At another five nests a single artificial catbird egg added to a nest with two or more real catbird eggswas accepted,where- as a single real or artificial cowbird egg was rejected under similar conditions at 52 of 55 nests from five localities in North America. These different acceptance rates (5-o vs. 3-52) are significant at P < 0.005 (Fisher Exact Probability Test, Siegel 1956). Throughout this paper data on which statistical tests have been performed will be reportedas in the precedingsentence. The entire two-by-two con- tingency table can be constructedfrom the information given (e.g. 5-0 vs. 3-52). To determinewhether catbirds possesstrue egg recognitionat an early stage in their breeding cycle and whether any recognitionthat occursis learned, the fol- lowing manipulation (experimentI) was performed: The first egg laid in 11 catbird nests was replaced with an artificial cowbird egg. The time interval between egg laying and initiation of the experimentis unknown, but it could have ranged from a few minutes to 4• h. The nestswere checkedlater the same day and then the next morning. In some casesadditional egg manipulations were conducted. Of the 11 nestsstudied 10 were in New Haven County, Connecticutduring May and June 1969 and 1970; the 11th nest, number 72-215, was in Anne Arundel County, Mary- land in May 1972.

R•su•.Ts FROM PRt•A•¾ EX2•R•TS Resultsof experimentI are summarizedin Table 1. At three nests, the cowbirdegg was missingby the sameafternoon of the day it had beeninserted. At anotherthree, it wasmissing and a secondcatbird egg was in its place the next morning. The catbirdsat thesesix nestsclearly recognizedtheir own egg type even at the earlieststages of clutch initiation. At the threenests where the cowbirdegg was ejected by the same afternoon,it was ejectedin the absenceof any cuesor informationthat one or more catbird eggsmight have supplied. It cannot be determined whetherthe cowbirdeggs in the other three nestswere ejectedbefore or after the secondcatbird egg was laid. But it is of coursecertain that they werenot the minoritytype eggat the time of their ejection. It could be arguedthat the missingcowbird eggs in thesesix nestswere removed October 1974] Avian ,Egg Recognition 799

TABLE 1 RESPONSES OF CATBIRDS TO ARTItlCIAL COWBIRD EGGS PLACED IN TIllER NESTS'

Status of cowbird egg Status of cowbird egg after 1 day after 2 days Experimental procedure and location Accepted Ejected Accepted Ejected

I First catbird egg laid replaced with an artificial cowbird egg (experiment done within 4• h 5 6 4 7 after the first egg was laid); Connecticut, Maryland II One artificial cowbird egg added to clutch when there were at least two catbird eggs present; 4 25 2 27 Connecticut, Maryland, Michigan x A catbird egg was removed at the time the cowbird egg was added in 23 of the 29 experiment II nests. Whether or not a catbird egg is removed at the time of experimentation has no effect on response (Rothstein 1970). At one experiment II nest a real cowbird egg was used rather than an artificial one. It was ejected within a day. by predatorsrather than by the catbirds,but 20 other catbird nestssub- jected to different experimentalprocedures during the same years and in the samestudy areas as the experimentI nestscan serveas a control for nest predation. Only one of thesenests suffered nest predation (all the eggswere missing) within 1 day after the experimentwas initiated, and this is significantly(P •< 0.01) lessthan the proportionof experiment I nestsat which the cowbird egg disappearedwithin 1 day (19-1 vs. 5-6). Events at the remainingfive nestswere variable. The cowbird egg in nest 69-228 was ejected after 2-2Y2 days. At nest 69-222 the cowbird egg remained in the nest for 2-2• days while laying proceededand the nest was then predated. The cowbird egg in nest 69-251 was accepted alongwith the three catbird eggssubsequently deposited. At nest 72-215 the cowbirdegg and the secondcatbird eggwere presentthe next morning. This secondcatbird egg was replacedby a cowbirdegg but both cowbird eggswere missing that afternoon. The two catbirdeggs were then returned to the nest and three catbird eggs were there the next morning. The complicatedevents at the last nest (69-264) are worth reporting in detail: 28 May, first egg laid replacedwith an artificial cowbirdegg; 29 May, onecatbird q- one artificial cowbirdegg, replaced the former with secondartificial cowbird egg; 30 May, one catbird egg q- one real (naturally deposited) cowbird egg q- two artifical cowbird eggs,removed the catbird eggand addeda third artificial cowbirdegg; 31 May, one catbird egg q- three artificial cowbirdeggs, real cowbirdegg is gone,replaced the catbirdegg with a fourth artificial cowbirdegg; 1, 2, 3, and 5 June,nest active, contentsfour artificial cowbirdeggs; 7 June, same, added a real 800 Sz•vvrz•r I. Rozvrszznv [Auk, Vol. 91 catbirdegg; 8 June,four artificialcowbird eggs q- real catbirdegg; 9 June,same; I 1 June,four artificialcowbird eggs, real catbirdegg is gone, addedan artificial catbirdegg; 13 June, four artificial cowbirdeggs q- oneartificial catbird egg; 14 June,same; 15 June,last nestvisit, same, neststill active. This historyshows that the catbirdsat nest 69-264 ap- parentlyaccepted a clutchconsisting only of artificial cowbirdeggs. I suspectthe catbirdsremoved both the real catbird egg,which I addedon 7 June, and the real cowbirdegg, which appeared on 30 May. Thus while the experimentI seriesshows that somecatbirds recognize their own eggseven in the initial stagesof egg-laying,the situationis rather complexfor other individuals.By contrastnone of the 29 pairs of catbirdsin easternNorth Americawhose nests received experimental cowbirdeggs when at least two catbirdeggs were present (experiment II), showedcomparable complexities. All ejectedthe cowbirdegg within 3 days,although as shownin Table 1, two had not yet doneso by the end of the first 2 days.

EVIDENCE THAT EGG RECOGNITION IS LEARNED The results(Table 1) suggestthat the catbirdlearns to recognizeits eggsthrough an imprinting-likeprocess on the first egg or eggsthat a bird sees.The evidenceis derivedfrom severalaspects. First, catbirds wererelatively tolerant of cowbirdeggs that replacedtheir first egg. The cowbirdegg in four of the ! 1 nestsin the experimentI serieswas still acceptedafter 2 days. This is opposedto only two of 29 for other ex- perimentsin easternNorth Americain whicha cowbirdegg was added whenthere were at leasttwo hosteggs in the nest (seeexperiment II, Table 1). The differencein 2-dayacceptance rates (4-7 rs. 2-27) is significantat P = 0.039. If the criterionof a 1-dayacceptance rate is ap- plied,the diffference (now 5-6 rs. 4-25) is alsosignificant (at P: 0.047). It is possiblethat the longeracceptance time in the experimentI nests occurredbecause some of the birdsin questionhad not yet fully learned their egg type when I removedtheir first egg. The presenceof the cowbird eggalone, where previously only a catbirdegg had beenpresent, may have interferedwith the egg recognitionof somebirds and either caused themto delay their rejectionor to acceptboth eggtypes. In contrastto learnedegg recognition,two alternativeinterpretations canbe offeredto explainthe differencesbetween the resultsof experiments I and II. Birds at experimentI nests could have shown increasedac- ceptancebecause their motivationalstate, as regardsrejection, was lower than that of birds at experimentII nests. A number of recordsindicate that rejecterspecies show slightly greater tolerance towards foreign eggs October 1974] Avian Egg Recognition 801 as their nestingcycle progresses(Rothstein 1970). This increasedtoler- ance may occur becausethe later a cowbird egg appearsin the host's nestingcycle the lesschance it has of hatching and of resultingin harm to the host'sown young. On this basis,experiment II rather than experiment I shouldhave had the higher acceptancerate. Secondly,it could be arguedthat birds at experimentI nestsshowed greater acceptance than those at experimentII nests becausethey visited their nests less frequently. While catbirds were usually in close attendanceto their nests on the first day of egg laying, my observationsindicate that birds at experiment II nests were in more frequent contact with their nests, so the possibleconfounding factor of differential contactwith the nest cannot be completelydiscounted. However, frequentnest inspectionsafter egg-layinghas begunare to be expected,as this would permit early de- tection of predation. In addition, while they have greater contact with their nest,incubating birds may seetheir eggsless frequently than do birds early in the egg-layingstage becausethey keep the eggscovered. Lastly, evidencepresented below supportslearned egg recognition,nearly all of it independentof the problem of differential contact with the nest. At severalnests events occurringmore than 2 days after experimentI was initiated also support the hypothesisof learned egg recognition. At nest 69-251 the cowbird egg was acceptedfor at least 8 days before the nest was destroyed. No other catbirds tested in eastern North America accepteda single cowbird egg for more than 3 days. Nest 69-228 is also relevant; here the cowbirdegg placed in the nest on the first day of laying was acceptedfor 2-21• days, after which the birds continuedto incubate two eggsof their own. Nine days after laying was completedI removed both catbird eggsand added two artificial cowbird eggs,which the birds ejectedwithin 6 h, indicatingthat they were then able to detect this egg type as foreignquickly whereasearlier they neededat least 2 days. Learned egg recognitionis most strongly supportedby the results from nest 69-264. At this nest, the catbirdsaccepted a clutch containingonly artificial cowbird eggswhen these were depositedin such a manner that each cowbird egg replaced a catbird egg soon after the latter was laid. The best explanation for the results from this nest is that the catbird eggswere not in the nest long enoughto allow the birds (or just the female) to learn this egg type as their own and that they learned the artificial cowbirdegg as "their own type." That they still retainedrejection behavioris indicatedby the disappearanceof both the naturally deposited cowbirdegg and the real catbird egg that were added to the nest on days 2 and 10, respectively.It seemslikely that both theseeggs were removed becausethey were detectablydifferent from the artificial cowbird eggs. 802 STE•'m;• I. ROTttSTE1N [Auk, Vol. 91

(Real cowbirdeggs show great variation, whereasthe artificial oneswere identical mimicsof an averagecowbird egg.) A catbird nest at Delta, Manitoba in June 1970 yielded similar data. An artificial cowbird egg was addedto the nest on the day the catbird laid its third or fourth egg. This cowbird egg was one of the few (three of 55) anywherein North America that was acceptedwhen added to a nest already containingmore than one catbird egg; but a naturally depositedcowbird egg appearing 7 days later was ejected while the artificial cowbirdegg was left in the nest. In this case the catbirds may have learned both the artificial cowbird egg and the catbird egg patternsas their own and rejectedthe real cowbirdegg because it wassufficiently different from both theseegg types. The most reasonableinterpretation of these results is that the tendency to reject eggsother than their own is largely innate in catbirds but that individualsnormally learn the egg type respondedto as their own from the first eggs that appear in their nest. Once the individual learns its egg type, it presumablyejects all other eggsthat depart from this type to a sufficient degree (catbirds will accept some types of nonmimetic eggs (Rothstein 1970)). Possiblya geneticcomponent in this learning processprevents catbirds learning any eggs whose features lie beyond a certain rangeof variablesas their own. An important questionregarding the learningprocess is whether it occurs only onceor with each nestingattempt. If the former is the casethe variation in responseto experimentI could be due to some of the birds being naive and someexperienced. If the latter is the case the variation couldbe due to the lengthof time the birdswere in contactwith their first egg beforeI replacedit with a cowbirdegg. Since naive and experienced birds could not be differentiated,my data do not permit resolvingthis questiondefinitely. I tested the hypothesisthat learning occursonly in naive birds by determining whether nests in experiment I that yielded acceptanceshad smallereggs, smaller clutches, or were started later than those that resultedin rejections. Birds breedingfor the first time often have smallereggs (Romanoff and Romanoff 1949, Coulsonet al. 1969) and often have smallerclutches and breedlater (Klomp 1970) than older birds. These analysesfailed to demonstratea correlation between egg or clutch size or date of laying and responseto experimentI, suggesting that the factor responsiblefor the variation in responseto the experiment was relatedto how long the birdswere in contactwith their first egg before I started the experiment and not to whether the birds were naive or experienced.But as I foundno correlationbetween response to experiment I and time of day I started the experiment,the length of time the birds werein contactwith the first eggwas alsoapparently unimportant. None October 1974] Avian Egg Recognition 803 of theseanalyses provides a definite explanationfor the variation in re- sponsesto experimentI, but I believelearning probably occursprimarily in naive birds, and each breedingattempt may further refine it. If egg recognitionis learned, an individual of a rejecter speciesmight accepta naturally depositedcowbird egg if this egg replacesits own first eggor is depositedbefore any of its own eggs. Probablythis is a rare oc- currence,but it seemsto have taken place at a catbird nest in the same study area (New Haven County, Connecticut) and at the same time that I conductedmost of the experimentsreported here. On 21 May 1969 I found an unlined catbird nest. When next visited on 24 May, the com- pleted nest containedone naturally depositedcowbird egg that a catbird was incubating. The bird behavednormally in that it scoldedme while I was at the nest. I checkedthe nest once or twice daily until the morning of 31 May when it was empty. Until this last visit, the nest con- tained only the cowbird egg. On all nine visits from 25 May until 30 May (my penultimatevisit) the cowbirdegg showedsigns of being incubated (it was warm), and a catbird scoldedme. It is unlikely that incubation behavior by the catbird would have occurred in the absence of egg-laying,so the most likely interpretationof the eventsat this nest is that the cowbird egg appeared shortly before any catbird eggs or quickly replacedthe first catbird egg (female cowbirdsoften remove a host egg (Friedmann 1963)). In either case, the catbird could have learned the cowbird egg as its own egg type. Then, shortly after laying each of its own eggs,it may have ejected them sincethey were unlike the eggit had learnedas its own. The catbird continuedto incubatethe cowbird egguntil it was removed,perhaps by a predator,between 30 and 31 May. This explanationaccounts for the unique featuresof this nest--a cowbirdegg was acceptedand incubated,and only a cowbird egg, never a catbirdegg, was seenin the nest. Experimentswith another egg type also suggestthat egg recognition is learned. As indicatedabove, rejecter speciesgenerally show slightly greater tolerance towards foreign eggs as their nesting cycle progresses, but catbirdsshow the reversetendency when parasitized with an egg that differs only slightly from their own. This egg, type Va, measures23.32 X 17.91 mm and has a blue-white ground color with 16 symmetrically placed brown dots (each dot being 0.5 to 1 mm in diameter). Real catbird eggsdiffer little in size but are blue-greenand unspotted. All four catbirds parasitized with egg type Va after they had completedtheir clutch rejectedthe egg whereasall five parasitizedduring the egg-laying periodaccepted it. This difference(0-4 vs. 5-0) is significantat P •< 0.025 and is what one might expectif, as the nestingcycle progresses,learning 804 SrEm{•N I. ROTItSTEIN [Auk, Vol. 91 continuesto refine an individual'srecognition behavior so that it becomes easierfor it to detect slight differences.Even if egg recognitionis ac- quiredprimarily at a bird's first nest, the recognitionmay be sharpened temporarilyduring each successive nesting attempt through prolonged contact with the eggs. Thus, two conflictingtendencies may developthe longera bird has contactwith its eggs: The drive to reject foreigneggs decreases,but the ability to detect their presenceincreases. Althoughseveral independent lines of evidencebased on field studies are all easilyexplained by the singlehypothesis that catbirdslearn their own egg type, this shouldbe confirmedwith experimentson breeding birds of known ages. This could be done most easily in captivity, but unfortunatelynone of the North Americanspecies that have been found to reject nonmimeticeggs breed readily in captivity.

EVOLUTIONARY IMPLICATIONS oF LEARNED RECOGNITION The likelihoodthat rejecter specieslearn their egg type and do not recognizeit innatelyhas importantevolutionary implications for the interactionsbetween brood parasitesand their hosts. It is commonly acceptedthat broodparasites may evolve new egg types that mimicthose of the host becausethis reducesthe host'sability to distinguishbetween the parasiticeggs and its own. Someworkers have stated that this evo- lutionaryprocess will eventuallyend when the mimicryis perfect(Meise 1930 in Southern1954) and result in "perfect or complete"evolution (Baker 1942: 3), but the possibilityof selectivepressures on the host's eggshas not beengiven sufficient consideration. It is unlikelythat the egg-relatedaspects of the evolutionaryinteractions of a parasiteand its host cometo an end and are completedif the parasite'segg mimicsthe host'segg perfectly. Selection might favor changes in the host'seggs so that thesediverge in appearancefrom a highlymimetic parasitic egg. Evo- lution could take two differentpathways. The developmentof egg poly- morphismin the hostwould make it difficultfor the parasitesto match their eggsto thoseof the host even if they had egg typesidentical to one or all of the host'smorphs (Rothstein 1971, Victoria 1972). This matchingdifficulty would arise becausebrood parasitesapparently com- mit themselvesto hostnests before any eggsappear (Chance 1940, Hann 1941) and thus have no way of predictingwhat egg morpha givennest will contain. Another strategy would be for the hosts to. undergo.direc- tional selectionand evolvea singlenew eggtype as the parasite'smimicry of their old type becomesmore highly developed.Swynnerton (1918) alsosuggested that broodparasitism might be a selectivepressure that modifiedthe appearanceof host eggs. He stated (1918: 145) "that a October 1974] Avian Egg Recognition 805

race may in some caseshave taken place between the host's eggs and those of the overtaking Cuckoo"; of course,this race need never end. While theseevolutionary responses by the host to the egg-relatedadap- tations of the parasiteare a logical expectation,they would have little chanceof occurringif the hosts innately recognizedtheir own egg type. When new eggvariations appeared, the hostswould reject their own eggs, unlessthe geneticchange producing the new eggtype was accompaniedby another genetic change permitting the individual to recognizeinnately the new egg type as its own. But, if the egg recognitionis not rigidly determinedby innate meansand is learned, then the successfuldevelop- ment of new, more adaptivehost egg types would requireonly the genetic changethat affects the egg'sphenotype. Thus hostswith learned egg rec- ognitionshould be able to evolveadditional antiparasiteadaptations much more rapidly than hosts with innate egg recognition. Swynnerton (1918) and Victoria (1972) collecteddata that support the above arguments. Each worked on a different speciesof African weaver (Swynnertonprobably Hyphantornis jamesoni and Victoria Plo- ceus cucullatus). Both speciesare cuckoo hosts, have highly variable eggs, and reject nonmimetic eggs. Even the eggs of other members of their own speciesare rejected if such eggs are of a sufficiently different type. The two authorsthought it likely that the weaversevolved both rejection behavior and variable eggs in responseto cuckooparasitism. Certainly theseapparent adaptations of the weaverscould have evolved much more easily if their egg recognitionwas largely learned rather than innate. It shouldbe indicated though, that like learned egg recognition, rejectionof discordanteggs would facilitate evolutionarychanges in host eggs. The hostswould always reject only the minority type egg and in nearly all casesthe parasiticegg would be the minority type. But Swyn- nerton's evidence (1916: 559) suggests,and Victoria's (1972) proves, that the two weaver speciesinvolved actually recognizetheir own eggs. If egg recognitionvia a primarily learned route proves to be the general mechanismamong passerines,it is important from an evolutionary view- point to ask why it rather than a primarily innate mechanismevolved. As indicated above, learned recognitionwould provide advantagesin the future becauseof its evolutionaryflexibility, but it would be teleological to suggestthat thesefuture advantageswould enhancethe initial develop- ment of eggrecognition by learning. I suggestthat learnedegg recognition was simply evolved more easily than innate recognition. Birds are rela- tively flexible in their behaviorand perhapseven amongaccepter species older individuals become conditioned to the egg type they have seen in their many breeding attempts. If in some individuals this predilection 806 Sr•?ae• I. Roz•szenv [Auk, Vol. 91

to conditioningwere strengthenedby genetic determinants,the species might then evolveinto a rejecterspecies. Possibly even in the beginning of the evolution of rejection behavior, simultaneousselection for a new host egg type sometimesfacilitates the discriminationbetween host and parasitic eggs. Such simultaneousselective pressures might result in the developmentof both rejectionbehavior and learnedegg recognition.

ACKNOWLEDG1VIEN'TS

I thank N. Philip Ashmole, Richard S. Miller, and Charles G. Sibley who aided me with the thesis on which this paper is partially based. Adrian M. Wennet and Eugene S. Morton made valuable comments on the manuscript. Larry C. Holcomb graciously performed some of the experiments cited in this paper. This research has been suppo.rtedby the Frank M. Chapman Memo.rial Fund, Yale University, the SmithsonianInstitution, and the University of California.

SUMMARY

Another paper in this series demonstratedthat birds that reject foreign eggspractice true egg recognitionafter their own clutch is com- pleted and do not simply reject any egg type that is in the minority. This paper attempts to answer the questionsof whether this recognitionis as highly developedwhen egg-layingstarts and whether it has both learned and innate components.The first egg laid in 11 catbird nestswas replaced with an artificial cowbirdegg. At six neststhe cowbirdegg was rejected either beforeor shortly after the secondcatbird egg appeared. In the case of these nests the catbirds clearly knew their own egg type at the onset of laying. On an overall basis these 11 nests demonstratedsignificantly greater tolerancetowards cowbird eggs than nests experimentallypara- sitizedlater in the breedingcycle. This suggeststhat a learning component to egg recognitionexists. At one nest the catbirds' entire clutch was grad- ually replacedwith artificial cowbird eggs. These were accepted,but a real catbird eggwas then rejected,suggesting that the egg type responded to as the catbird's own is learned from the first eggsan individual sees in its nest and that the tendencyto reject other eggsis innate. Data from additional experimentaland nonexperimentalnests also support this hy- p.othesis,but none of the data allow a determinationof whetherthe learning occurs only once in an individual's lifetime at its first nest or re- peatedly with each nest. Egg recognitionby learning has significantim- plications as regards the long range evolutionary interactionsbetween broodparasites and their hosts. Hosts that learn their own egg type can evolve additional ant/parasite adaptations much more easily than hosts that innately recognizetheir own egg. October 1974] Arian Egg Recognition 807

LITERATURE CITED

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