Foam Produced by Male Coturnix Quail: What Is Its Function?
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The Auk 116(1):184-193, 1999 FOAM PRODUCED BY MALE COTURNIX QUAIL: WHAT IS ITS FUNCTION? ELIZABETH ADKINS-REGAN • Departmentof Psychologyand Section of Neurobiologyand Behavior, Cornell University, Ithaca, New York 14853, USA ABSTRACT.--Malesof the Old Worldquail genusCoturnix are unique among birds in pos- sessinga well-developedproctodeal gland. The gland and associatedcloacal musculature are sexuallydimorphic, androgen dependent, and producea foamy substancethat is intro- ducedinto the femalealong with semenduring copulation, suggesting that the foamplays somerole in increasingmale reproductive success. I experimentally tested three hypotheses aboutthe functionof this foam in JapaneseQuail (Coturnixjaponica): (1) foam functionsin spermcompetition, (2) foamreduces the female'sreceptivity to a secondmale, and (3) foam increasesthe probabilityof fertilizationwhen a hard-shelledegg is presentin the uterus (hypothesis3 was originallyproposed by Chenget al. 1989a).Insemination shortly before ovipositionfertilized fewer eggs than inseminations earlier in theday, but only if maleshad a reducedfoam complement,supporting the third hypothesis.The othertwo hypotheses were not supported.Copulation reduced female receptivity, but this effect was not due to the male'sfoam. Received 2 February 1998, accepted 22 June1998. IN MOSTAVIAN SPECIES,males either have no "whipped" into foam by the action of the phallus or have a rudimentarynon-intromit- sphinctercloacae (Ikeda and Tajii 1954,Fujii tent phallus (Briskieand Montgomerie1997). and Tamura 1967, Seiwert and Adkins-Regan Thus,mating is accomplishedwithout the elab- 1998).The foam gland complexis markedly orate genitalia characteristicof many mam- sexuallydimorphic (large in malesbut rudi- mals, reptiles,and insects.Recent interest has mentaryin females),is well developedin males developedregarding the possibilitythat birds onlyduring the breeding season, and is highly have evolvedspecial anatomical and physio- androgendependent (Nagra et al. 1959,Beach logicalmechanisms to manipulatefertilization, and Inman 1965, Sachs1967, Adkins and Adler specificallysperm competition or femalesperm 1972, Siopesand Wilson 1975). manipulation(Birkhead and Moller 1992). During copulation,the male introducesnot Malesof the Old World quail genusCoturnix only semenbut also a large quantity of foam are unique among birds in possessinga well- into thefemale. The rhythmic movements of the developedproctodeal gland (McFarlandet al. sphinctercloacae that areknown to "whip up" 1968, Klemm et al. 1973, Slopes and Wilson the foam increasegreatly in frequencyas soon 1975, Bakst and Cecil 1985). In domesticated as the male detectsthe female, in advanceof ac- JapaneseQuail (Coturnixjaponica), a large,red tual mountingand cloacalcontact (Seiwert and protuberanceis presentimmediately dorsal to Adkins-Regan1998). These observations sug- the cloacalopening (Fig. 1). Thisprotuberance, gest that the foam functionsto increasethe the foam gland complex,is distinctlydifferent from the cloacalprotuberances of somepasser- male'sreproductive success by promotingfer- ines (it does not contain the coiled vas defer- tilization(Ogawa et al. 1974,Fujihara 1992). ens) and is not a sperm-storageorgan. It con- Female JapaneseQuail are unusual in that sistsof an enlargementof the dorsalportion of they lay eggsin the late afternoon(Wilson and the sphinctercloacae muscle plus the procto- Huang 1962)rather than in the morningas in deal glandproper, the unitsof whichare inter- manyother bird species(Skutch 1952). Females digitatedwith sphinctercloacae muscle fibers also are more sexuallyreceptive behaviorally (Klemm et al. 1973).The proctodealgland se- in the afternoon(Delville et al. 1986).Cheng et cretes a viscous mucoprotein that is then al. (1989a, b) proposedthat foam enabled a male to fertilize a female even when a hard- shelledegg was in the uterusduring mating, E-mail: [email protected] whichwould often be the casefor matingsoc- 184 January1999] QuailFoam and Fertilization 185 FIc. 1. Externalview of the foamgland complex (feathers removed) of a reproductivelyactive male Jap- aneseQuail. Arrow indicatesthe cloacalopening. Photograph by Marie Read. curringin the afternoonduring the female's Cauterizationis a potentially confounding peak of receptivity.In supportof this hypoth- manipulation,however, because the interdigi- esis,Cheng et al. (1989a,b) reportedthat foam tation betweenthe proctodealgland and the prolongedsperm rnotility in vitroand thatmale sphinctercloacae muscle makes it impossible JapaneseQuail whosefoam glandshad been to destroythe gland without damagingthis destroyedby cauterizationfertilized few or no muscle.Because the sphinctercloacae is essen- eggs. tial for copulation(i.e. for cloacalcontact and 186 ELIZABETHADKINS-REGAN [Auk,Vol. 116 ejaculation;King 1981,Seiwert and Adkins-Re- few seconds.If the male is lesscompetent or the fe- gan 1998),it is likely that cauterizedmales are male is unreceptive,repeated chasing, mounting, defectivein componentsof copulationcritical and attemptedcloacal contact occur, which some- for fertilizationsuccess other than foam pro- timesbut not alwaysresults in successfulejaculation duction. Also, neither in vitro observationsnor and insemination.Foam is depositedin the female's proctodeum(Cheng et al. 1989a),and spermare not cauterizationexperiments provide a direct test foundin the femaleunless foam is alsopresent (Ad- of the hypothesisthat foam increasesfertiliza- kins 1974).Thus, inseminationcan be confirmedby tion successmainly when a hard-shelledegg is examinationof the female(the foam is clearlyvisible present. in the proctodeum)or, if tactilecontact with the fe- The experimentsreported here use a lessin- male'scloaca might introduce an experimentalcon- vasivemanipulation to test the abovehypoth- found, by closeobservation of the male'sbehavior esisand alsotest two additionalhypotheses for (cloacalcontact followed by suddencessation of the the function of foam. One is that foam enables copulatoryattempt followed by featherfluffing and/ a male to reducethe abilityof a secondmale to or strutting).For data validating the use of themale's fertilize the female; that is, that it functions in behaviorto judge successfulinsemination, see Ad- kins-Regan(1995). sperm competition.Foam could function as a Dependingon the experiment,females were al- mechanical device analogousto the sperm lowedto copulatewith a male eitherin their home plugsof someother vertebrates, or it couldact cages(21 x 18 x 15 cm hardwarecloth), a smalltest- chemically,for example,by enabling a male's ing cage (38 x 24 x 18 cm), or a large testing cage spermto remainmotile longerthan a compet- (183 x 91 x 77 cm). Cage size has no effect on the ing male'ssperm. The secondhypothesis is that likelihoodthat an inseminationwill fertilize eggsor the foam reduces the female's receptivity on the number of eggs fertilized (Adkins-Regan (again decreasingthe likelihoodthat a second 1995).If the male did not begincopulating immedi- male would be able to fertilize the eggs),but ately,he was replacedwith anothermale. The male was removed after insemination,and except when througha differentmechanism, the female'sbe- measuringfemale receptivity,only resultsfrom mat- havior.Both of thesehypotheses assume that ing trials in which the male achievedinsemination femalesmight mate with multiple males. Al- were analyzed.Unless stated otherwise, mating tri- thoughlittle is knownabout the matingsystem als were conducted between 1130 and 1500 EST, a of wild JapaneseQuail, extrapair copulations time when femalesare likely to be receptive. havebeen observed in feral JapaneseQuail in a Most eggswere laid between 1600 and 2000. Eggs seminaturalenvironment (Nichols 1991), and were collecteddaily in the morning (beginningthe field observationsof the closelyrelated Com- morningafter mating)for 11 days,which is the max- mon Quail (Coturnixcoturnix) suggest that sit- imum sperm-storageinterval in this speciesand in uations in which females switch mates, or in birds in this laboratory (Sittman and Abplanalp 1965, Adkins-Regan 1995). Eggs were stored at 13øC whichmore than one male attempts to copulate for a maximumof two weeksprior to incubationat with a female,occur rather frequently (Rodri- 38øCand 60% relative humidity. Eggs were broken go-Ruedaet al. 1997). open after one week of incubationand recordedas fertile if any embryonicdevelopment had begun.It METHODS is possiblefor eggsto be fertilized,in the sensethat spermare attachedto the outer perivitellinelayer, Birds,mating trials, and fertilization measures.--The without any embryonicdevelopment being initiated quailused in thisstudy were hatched from eggspur- (Birkheadet al. 1994).Such outcomes do not, how- chasedfrom Truslow Farms, Chestertown,Mary- ever, contribute to a male's reproductive success. land, and were housedindividually after the age of Therefore,because my experimentstest hypotheses four weeks(sexual maturity beginsat ca. five to six abouthow foam influencesmale reproductivesuc- weeks).All birds were at leasteight weeksold and cess,all eggswith no embryonicdevelopment were not more than eight monthsold during the experi- categorizedas infertile, and "successfullyfertilized" mentsand werehoused on a 16:8light: dark cycle.A shouldbe takento mean fertilized suchthat embry- new set of birdswas used for eachexperiment, and onic developmenttakes place. Early embryonic maleswere sexuallyexperienced prior to use. deathsoccurred at a low rate (in eachexperiment In this species,ejaculation