Removal of Yellow Warbler Eggs in Association with Cowbird Parasitism’

The Condor94~40-54 0 The Cooper Ornithological Society 1992

REMOVAL OF YELLOW WARBLER EGGS IN ASSOCIATION WITH COWBIRD PARASITISM’

SPENCER G. SEALY Department of Zoology, Universityof Manitoba, Winnipeg, Manitoba R3T 2N2, Canada

Abstract. In this study, I quantified the removal of eggsby the Brown-headed Cowbird (Molothrus ater) from parasitized Yellow Warbler (Dendroicapetechia) nests. Laying cowbirds removed one warbler egg from about one in three parasitized nests. Assuming the same individual was involved in both acts, cowbirds removed host eggson a day before or the same day they laid their own eggs(33.3%, n = 8 nests), on the same day (20.8%, n = 5) but after they laid, or on the same or subsequentdays (46%, n = 11). As almost half (4 1%) of the parasitizednests received cowbird eggsbefore host eggsappeared, many cowbirds that removed eggshad to return to the nest to do so, although burial precludedthat at some nests. Return trips increasedthe chancesthat a cowbird might mistakenly remove its own egg, especially if it was the only egg in the nest, and that interactions might occur between host and parasite. Explanations for the removal of eggsat the time of parasitism are sum- marized and two hypothesesare tested. The likelihood of warblers acceptinga cowbird egg experimentally introduced into their nests was not influenced by the removal of a host egg at the time of parasitism, as predicted by the “host deception” hypothesis.Yellow Warblers tolerated five- and four-eggclutches being reducedto three eggs(36/37 nests),but abandoned nearly one-third of clutchesreduced to two eggs(13/42) and most clutchesreduced to one egg (20122). Only one control nest was deserted (n = 41 and 59 clutches of five and four eggs,respectively). Only four of 13 (3 1%) clutchesreduced to one eggof each of the warbler and cowbird were abandoned, but 11 of 14 (79%) clutchesreduced to onlv one cowbird egg were deserted. None of the 10 clutches reduced’to two cowbird eggswas deserted. These results suggestthat cowbirds can remove at least two eggswithout risking desertion by the warblers. It is not clear why only one eggis removed, when removal occursin the first place. Cowbirds that manage to ingest eggsthey remove undoubtedly gain nourishment. Key words: Broodparasitism: egg laying; egg removal;clutch reduction;nest desertion; Brown-headedCowbird; Yellow Warbler.

INTRODUCTION the nesting cycle of the hosts, while others take Avian brood parasites manipulate the clutches place much later. Ejection of host young and and broods of their hosts. Parasitic eggs increase unhatched eggsclearly eliminates any competi- the volume of host clutches unless the parasites tive advantage host nestlings might have, max- remove one or more host eggswhen they para- imizing the survival of the parasitic young to sitize nests (e.g., Lombard0 et al. 1989) or if the fledging (e.g., Blankespoor et al. 1982, Carey hosts respond to the parasitic egg(s) by laying 1986). However, it is not obvious why many fewer eggs (e.g., Kendra et al. 1988). Parasitic brood parasites steal eggsfrom nests they para- nestlings of some parasites may kill their host sitize. Few studies have quantified the extent of “siblings” (e.g., Friedmann 1955, Morton and removal or identified the circumstances under Farabaugh 1979) physically oust them or the which it occurs(but seeDavies and Brooke 1988, unhatched host eggsfrom the nest (e.g., Jensen Lombard0 et al. 1989). Some speciesof parasitic and Jensen 1969, Wyllie 1975, Gill 1983) or cuckoosalmost always remove one or more eggs outcompetehost young by monopolizing the food from host nests (e.g., Jensen and Jensen 1969, brought by the foster parents, eventually crowd- Wyllie 1975, Brooker et al. 1988) while other ing their undernourished nest mates until they speciesusually do not remove any (e.g., Liver- starve and are removed by the hosts or fall from sidge 197 1, Gaston 1976). Among the parasitic the nests(e.g., Gaston 1976, Carter 1986, Briskie cowbirds, females remove or damage host eggs and Sealy 1987, Marvil and Cruz 1989). with considerable variability, possibly depend- Some of these manipulations occur early in ing upon the particular host speciesparasitized (e.g., Friedmann 1963, Post and Wiley 1977, Smith 1981, Zimmerman 1983, Carter 1986). ’ ’ ReceivedApril 1 1991. Accepted9 October199 1. The Brown-headed Cowbird’s (Molothrus ater)

[401 EGG REMOVAL BY COWBIRDS 4 1 habit of removing eggsfrom parasitized nestshas with the act of parasitism. Below, I summarize been suspected for over 100 years (e.g., Bur- explanations for this behavior. I exclude from roughs 1887, Savage 1897). Since then, anecdotal consideration behavior of many other brood par- observations and studiesof closelywatched nests asites, which may also remove eggswhen they of a few host specieshave revealed that if a fe- parasitize nests, but are known also to destroy male cowbird removes an eggat all, she may do host or potential host clutches or broods at other so either a day before, later on the same day, or stagesof the breeding cycle, possibly to create a day after she laid her own egg (assuming the new opportunities for parasitism (e.g., Payne same female is involved in both acts). Because 1977), to prevent other females from gaining ac- eggremoval by female Brown-headed Cowbirds cess to nests to parasitize (Wyllie 1975) or to apparently requires extra visits to host nests, op- revisit parasitized nestsafter hatching and, if the portunities increase for interactions to occur be- parasite chick is not in the nest, prey upon host tween cowbirds and hosts. As Yellow Warblers nestlings to force them to renest (Zahavi 1979). (Dendroica petechia) recognize female cowbirds Lastly, I do not consider the destruction of host as a threat (e.g., Hobson and Sealy 1989) they eggs in nests parasitized by some of the other may reject parasitized clutchesafter intercepting speciesof cowbirds (e.g., Post and Wiley 1977, a cowbird at their nests. Indeed, cowbirds and Carter 1986). other brood parasites lay their eggswithin sec- Host deception.Egg removal may dupe a host onds (e.g., See1 1973, Nolan 1978:371, Brooker that counts eggsinto acceptinga parasite egg(e.g., et al. 1988), presumably to avoid being detected Hamilton and Orians 1965, Moksnes and Ros- by hosts.Davies and Brooke (1988) and Moksnes kaft 1987). This hypothesis predicts that para- and Roskaft (1989) demonstrated experimental- sitic eggslaid in nests where a host egg is not ly that some hosts of the Common Cuckoo (CU- removed are more likely to be rejectedthan those culus canorus) presented at their nests with a laid in nests where a host egg is removed. model of the cuckoo plus its egg,were more likely Food for the parasite. Typically, brood para- to reject the egg than hosts in whose nests only sites remove a single egg from each host nest, if a cuckoo egg had been introduced. they remove any at all (e.g., Jensen and Jensen Several hypotheseshave been proposed to ex- 1969, Gill 1983, Wyllie 1975, Brooker et al. 1988, plain the function of host-eggstealing. Few have Lombard0 et al. 1989). Although early workers been tested (see Payne 1977, Davies and Brooke debated whether female Common Cuckoos ate 1988, Rothstein 1990). This behavior has re- the eggsthey removed from host nests(e.g., Gur- ceived relatively little attention in the literature, ney 1897) this behavior has since been con- despite its likely importance in the dynamics of firmed for this and many other speciesof para- parasite-host interactions. In the present study, sitic cuckoo(e.g., Livesey 1936, Friedmann 1968, I examined the removal of Yellow Warbler eggs Jensen and Jensen 1969, Wyllie 1975, Brooker by Brown-headed Cowbirds (hereafter cow- and Brooker 1989) and other brood parasites, birds). My objectives were (1) to measure the including cowbirds (see below). Lijhrl(l979) es- rate at which cowbirds removed warbler eggsin tablished from observations of captive Common relation to laying by the cowbird and warbler, Cuckoos that only females remove eggsand that (2) to quantify the frequency of removal over they swallow them whole. Becauseparasites un- several breeding seasons,and (3) to summarize doubtedly gain nourishment from this behavior explanations for why laying brood parasites re- (seePayne 1974, Becking 1979, Liihrl1979) Da- move (usually one) host egg. In addition, I de- vies and Brooke (1988) wondered why they do scribe two experiments designed (1) to ascertain not remove more eggsand suggestedthat hosts whether Yellow Warblers are more likely to ac- are prone to desert greatly reduced clutches. cept cowbird eggsexperimentally introduced into Do Brown-headed Cowbirds eat eggsthey re- their nests, if switched with a host egg, and (2) move from host nests? Females have been re- to reduce warbler clutchesto ascertain the extent ported carrying eggs away from nests in flight to which warblers tolerate lowered clutch sizes. (Nice 1937, Mitchell 1956, Earley 1991), drop- ping them while flying from nests(Roberts 1932) EXPLANATIONS FOR HOST-EGG REMOVAL and carrying eggsto the ground where, in cases In my treatment of egg removal, I address only where females were not immediately flushed, ate the removal of eggsby parasites in association them piecemeal, sometimes shell and all (Nice 42 SPENCER G. SEALY

1929; Blincoe 1935; Hann 1937, 1941; Olson (e.g., Scott 1977, Blankespoor et al. 1982). Gas- 1943; Norris 1944; Nolan 1978:371). On our ton (1976) detected egg removal in populations study area, we have thrice observed females eat- of the Pied Crested Cuckoo (Clamator jacobi- ing eggson the ground and once observed a cow- nus), which normally does not remove host eggs bird carrying an egg away from a nest (Sealy, when laying. In these populations, multiple lay- unpubl. observ.). Benson (1939: 122) watched a ings by the parasite were common and Gaston female cowbird remove one of two cowbird eggs (1976) suggestedthat it is imperative under these (the only eggs in the nest) from an American circumstances that some eggs are removed to Redstart (Setophuguruticillu) nest and eat it, shell ensure the brood does not become too large. and all, on the ground a few meters away. Captive Enhancement ofhost incubationeficiency. Da- females noted by Ring (1979: 13) either ate or vies and Brooke (1988) pointed out that in some “disregarded” eggsthey removed from artificial specieslarger clutches have a higher frequency nests. Thus, ingestion of eggsremoved by cow- of unhatched eggs (e.g., Yom-Tov 1980, Wik- birds from naturally parasitized nests appearsto lund 1985). Thus, it might benefit a brood par- be a regular behavior associatedwith the act of asite to remove a host egg if the addition of its parasitism. If cowbirds remove eggs to obtain own eggto the host clutch results in less efficient food, but are limited by the risk of host desertion incubation, becausethe parasitic egg also would if too many eggsare stolen, I would predict that be less likely to hatch. The incubation limit hy- clutches reduced more than those induced nat- pothesispredicts that the incidence of unhatched urally (seebelow) should lead to more desertions eggsin nests from which a host egg is removed by hosts and should be selectedagainst. to make room for the parasitic egg will be less Ankney and Scott (1980) demonstrated that than that in nests where no host eggis removed. egg-laying female cowbirds, which lay an esti- Parasitism of smaller hosts. This explanation mated 40 eggsin an eight-week breeding season involves two quite different behaviors-the evic- in southern Ontario (Scott and Ankney 1980) tion of host nestlings by newly hatched parasites, rely on exogenousnutrients for egg production. and the removal of host eggsat laying. Gaston Cowbirds obtained these nutrients by increasing (1976) suggestedthat eviction of eggsand nest- their intake of protein. Stomachsof females they lings may be an adaptation for parasitizing hosts examined often contained piecesof mollusc shell, that are much smaller than the parasite, where which are sourcesof calcium. Although leg-bone the rearing of a single nestling is the equivalent calcium reserveswere also used by female cow- to rearing a whole brood of host offspring. In the birds for eggproduction (Ankney and Scott 1980) genus Clamator, most species parasitize hosts eggshellsmay supplement their calcium uptake. similar to, or larger than themselves in size, and This would be another benefit to ingesting eggs hence eviction is not necessary if the female removed from host nests. Lijhrl(l979) reported cuckoo removes or destroysone ofthe host’s eggs that one captive female Common Cuckoo swal- while laying (see also Lack 1954). Supportive of lowed 65 passerine eggsin one breeding season. this hypothesis is Friedmann’s (1960) observa- Wyllie (1975) reported a wild female cuckoo par- tion that viduines, which parasitize estrildine asitizing Reed Warblers (Acrocephalus scirpa- hosts similar to themselves in size and mass, ceus) that took at least 19 fresh eggs and two frequently remove a host egg at laying. Fried- nestlings in one season. mann noted, however, that other parasites that Test incubation status of hosts.Livesey (1936) are hardly larger than their usual hosts, such as suggestedthat cuckoos might remove an egg to honeyguides and the Didric Cuckoo (Cu. ca- determine whether host clutches are fresh or in- prius), usually replace the entire host brood with cubated, thus ascertaining whether or not they a single individual of their own. are suitable for parasitism. Predicted here is that brood parasites should eat, or at least break, a METHODS host eggbefore they commit their own eggto the nest. STUDY AREA Reduction of crowding and competition. For Natural parasitism on the Yellow Warbler by the parasitessuch as cowbirds, whose newly hatched Brown-headed Cowbird was studied from 1974- young do not eject host eggs or nestlings, egg 1987 (except 1977) on the forested dune ridge removal probably reduces nestling competition that separatesLake Manitoba and Delta Marsh, EGG REMOVAL BY COWBIRDS 43

Manitoba (seeMacKenzie 1982). The study area did not distinguish between nests that lost one (5O”l l’N, 98”19’W) is a 3-km portion ofthe ridge egg or more than one egg. forest that averages 80 m in width as it runs Cowbird eggsdisappeared from some parasit- westward from the Portage Diversion to Cram ized nests, but in all cases host clutches were Creek (see map in Sealy 1980), on the adjoining completed and otherwise remained active. War- properties of the University of Manitoba Field blers might have ejected them (see Weatherhead Station and Portage Country Club. 1989), although other authors either did not re- cord the disappearanceof cowbird eggsor stated EGG LAYING BY HOST AND PARASITE explicitly that Yellow Warblers cannot eject them Nests at all heights over the entire ridge forest (e.g.,Rothstein 1975a, Clark and Robertson 198 1, were checked before 12:00 (Central Daylight Graham 1988, Rohwer and Spaw 1988). On the Time) each day before and throughout egglaying, other hand, cowbirds or predators might have and intermittently during incubation. Nests were removed them (see Rothstein 1975b). Cowbirds numbered with flagging tape placed nearby and have been suspected of occasionally removing individual eggs, including cowbird eggs, were cowbird eggsfrom nests, usually those parasit- markedin 1974-1976,and 1987withwaterproof ized more than once or where host eggs were markers in the order they were laid. Unparasit- larger or similar in appearance to cowbird eggs ized and parasitized clutches were considered (e.g., Hann 1937, Benson 1939:122, Klaas 1975, complete when the number of eggsremained the Elliott 1977, Scott 1977). same for at least two consecutive days. CLUTCH MANIPULATIONS REMOVAL OF YELLOW WARBLER EGGS Experimental parasitism. I experimentally par- Daily visits to warbler nests in which each egg asitized Yellow Warbler nests in 1988, 1989 and was marked on the day it was laid showed that 1990 using real cowbird eggscollected from nests one egg,rarely more, sometimesdisappeared with of several host species, including the Yellow the nestsremaining active. Becausepredators and Warbler, in and near the Delta Marsh. I para- strong winds could account for these losses sitized most nests between 07:OO and lO:OO, so (Goossen and Sealy 1982), the relative effectsof as not to interfere with normal laying by the these influences were estimated by comparing warblers (see below). I experimentally parasit- egg-loss rates in parasitized and unparasitized ized two groupsof nestswith single cowbird eggs nests. Data for this analysis were from nests ex- on LDl (= Laying Day 1, i.e., day on which the amined in 1974-1976 and 1987. I determined A-egg was laid) or LD2, without removing a host the proportion of nests that lost at least one egg egg from nests in one group, and switching the without the nest being abandoned, in the five cowbird eggand one host eggin the other group. days following laying of the first host egg and I consideredcowbird eggsaccepted when egglay- also during the incubation period. I used only ing was not interrupted and clutches were com- neststhat were visited daily from at least the day pleted, or incubation continued for at least six before the first host eggswere laid. A nest that days. I considered desertion to have occurred lost eggswithout being abandoned was counted when all activity at the nest ceased after para- as having a loss. One that survived to the morn- sitism and the eggswere cold to the touch, or, if ing of Day 6 without egg-losswas scoredas a no- the female laid after the interference, but never loss. incubated. The timing of egg removal relative to stageof Clutch reduction.I reduced clutch size in three the host’s reproductive cycle was determined to groupsof neststo determine the tolerance of Yel- the nearest day in some nests,to within two days low Warblers to lowered clutch volumes. In the in others. Thus, a warbler egg that disappeared first group, I removed the first-laid eggs, i.e., between inspections could have been removed A-eggs,within l-2 hours of their being laid, leav- either later that day or before I checked the nest ing the nests empty. B-eggsfollowed by C-, D-, the next morning. As a typical example of the and E-eggs (when laid) were removed as they latter kind of data, eggB sometimes disappeared were laid in the second group, leaving only the between mid-morning inspections on the second A-egg in nests. In the third group, nestswith four and third days of laying. I subdivided the data or five eggs,the most common clutch sizesin the according to their two degreesof precision but population (Goossen and Sealy 1982) were as- 44 SPENCER G. SEALY signed to one of six treatments, plus a control their eggson successivedays (Ankney and John- group, i.e., nests with eggsnumbered but only son 1985). In these cases,cowbirds that stole an visited each day. Seven or eight days after the eggfrom nestsalmost certainly had to distinguish A-egg was laid, clutches in four treatments were between host eggsand their own egg. reduced to one, two, three, or four warbler eggs. Time of day of laying. Cowbirds usually lay Nests in two other treatments were reduced to shortly before sunrise (Scott 199 1). Time of day one cowbird egg only, and one egg each of the of laying by 10 Yellow Warblers, determined be- warbler and cowbird. All nestswere checkeddai- tween 2 and 10 June 1989 (sunrise times 05:23 ly for at least six days, or until they were aban- and 05: 19, respectively) using Muma’s (1986) doned, i.e., not incubated for three consecutive observational procedure, ranged from 05: 15 to nights, or depredated. Ten nests were also re- 06: 15, with a mean time of 05:52. duced to two cowbird eggs,three by experimental Laying by individual cowbirdsrelative to laying reduction and seven as a result of parasitism by by host warblers.In 255 cases,I knew the day on cowbirds. which a cowbird laid in a warbler nest and the day on which the host female laid its first egg, MEASUREMENTS OF COWBIRD AND WARBLER EGGS i.e., LDl. I assumed that when a cowbird and a warbler laid on the same day, the cowbird laid Cowbird eggsare fairly consistent in appearance earlier (see above). All nests were observed be- and do not mimic eggsof host species(see Roth- fore any eggswere deposited, but some cowbirds stein 1974). Nevertheless, Yellow Warbler eggs may have removed warbler eggsfrom nests they (see photo in Harrison 1975: 183) and cowbird parasitized before I recorded them. If egg A had eggsare similar in appearance,although the latter been removed before my inspection on the day averages 47.2% larger in volume and is 45.5% it was laid, I might have thought laying began heavier. The mean length and breadth (measured the following day. However, because cowbirds with dial calipers) of 77 cowbird eggslaid in 73 generally removed host eggsafter mid-morning warbler nests was 21.07 (SE = 0.12 mm) and (see later), after I had checked most nests, I am 16.36 (SE = 0.09 mm), respectively. Mean mass confident that this bias was small. Of the 255 (measured on an electronic balance) was 3.14 (SE cowbird eggs in the sample, 105 (41.2%) were = 0.04 g) and volume (calculated using the for- laid before the day on which warblers laid their mula V = 0.498LBZ, where V is interior volume, first eggs,i.e., during the pre-laying period (Fig. L is length, and B is breadth; from Spaw and 1). Most of these cowbird eggs(62.9%) were bur- Rohwer 1987 ) was 2.82 (SE = 0.33 ml). The ied or the nests were deserted. The remaining mean length and breadth of 85 Yellow Warbler 150 eggs(58.8%) were laid during the laying pe- eggs(irrespective of laying order) was 16.80 (SE riod and in some casesafter host clutches were = 0.08 mm) and 12.60 (SE = 0.04 mm). Mean complete (Fig. 1). mass was 1.43 (SE = 0.01 g) and volume was 1.33 (SE = 0.11 ml). REMOVAL OF YELLOW WARBLER EGGS RESULTS Number of eggs removed. Totals of 1,005 and 2 16 unparasitized and parasitized nests con- EGG LAYING BY HOST AND PARASITE tained means of 4.47 (SE = 0.0006) and 4.15 (SE Frequency of parasitism. Of the 1,885 Yellow = 0.003) warbler eggs, respectively (Table l), Warbler nests studied, 396 (21%) were parasit- which differed significantly (Kruskal-Wallis test, ized by cowbirds. Of the 396 parasitized nests, adjusted for ties, H = 50.5 16, df = 1, P < 0.001). 354 (89.4%) were parasitizedonce, 38 (9.6%) were Thus, the number of Yellow Warbler eggsin nat- parasitized twice, and 4 (1 .O%) were parasitized urally parasitized nests was 0.32 eggsless than three times. The following intervals were ob- in unparasitized ones, which indicates that fe- served between successivecowbird eggslaid in male cowbirds typically removed an egg from the same nest: 0 day (n = l), 1 day (n = 34), 2 about one-third of the warbler nests parasitized. days (n = 3), 3 days (n = I), and 4,5, and 8 days I assumed this difference was due to cowbirds (n = 1 each). The preponderance of l-day, over stealing host eggsfrom neststhey parasitized (see O-day intervals, at multiply parasitized nestssug- Rothstein 1975b for discussionof the legitimacy geststhat the same females were usually involved of this assumption). The following analysis sup- (see Gaston 1976), as cowbirds are known to lay ports this assumption, as does the summary be- EGG REMOVAL BY COWBIRDS 4.5

N = 255 COWBIRD EGGS N = 236 NESTS 66

u-n PRE- EARLY LATE INCU- LAYING LAYING LAYING LAYING BATION FIGURE 1. Frequency of cowbird laying in relation to laying stage of the Yellow Warbler. PRE-LAYING STAGE: cowbird eggslaid before LD 1. EARLY LAYING STAGE: cowbird eggslaid on LD 1 and LD2. LATE LAYING STAGE: cowbird eggslaid on LD3-LD5. INCUBATION STAGE: cowbird eggslaid after LD5. The values on top of the bars are the number of cowbird eggslaid. low of observations of cowbirds removing and parasitized clutches for the same week. A Krus- eating host eggs, including those of the Yellow kal-Wallis ANOVA showed a significant differ- Warbler. ence in egg removal among weeks (T = 24.91, Thirty-eight of 23 1 unparasitized warbler nests df = 5, P < 0.001). Multiple comparisons fol- lost eggsduring the laying period, a rate signifi- lowing this test suggestthat egg removal was cantly lower than for parasitized nests (38:193 greater in weeks two, four, and six than in week vs.29:33;G=11.419,df=1,P<0.001).Losses three, and greater in week two than in week one. during incubation in unparasitized and parasit- Hour of removal. On the study area, female ized nests, however, did not differ (23: 117 vs. 5: cowbirds were twice observed eating Yellow 18, G = 0.052, df = 1, P > 0.20). The results Warbler eggsaway from nests,at 1O:OOand 10:47, confirm that cowbirds removed most of the eggs and an American Robin (Turdus migratorius) lost from parasitized nestsduring laying, but not egg near the nest, at 16:07. At 09:47 on 2 June during incubation. 199 1, I watched a female cowbird carrying an Although the number of warbler eggslaid in egg from a warbler nest. Elsewhere, female cow- unparasitized and parasitized nestsvaried among birds have been observed removing eggs from years (Kruskal-Wallis ANOVAS, adjusted for just before sunrisethrough the evening (e.g., Hann ties, H = 19.392, df = 9, 0.05 > P > 0.02 (un- 1937, Nice 1937, Olson 1943, Nolan 1978:374- parasitized); H = 19.49, df = 9,0.05 > P > 0.02 378, Wolf 1987, Earley 1991). (parasitized)), there was no correlation between Stage of host nesting effort. At leist 80% (24/ the number of host eggs in unparasitized and 30) of all laying-interval removals were on LD 1 parasitized nests between years (Spearman rank or LD2 of the warbler laying cycle. Three re- correlation coefficient,p = 0.258, P > 0.05). Over movals were known for sure to have left the nests the breeding season,egg removal was estimated empty (Table 2). by calculating the percentagedifference between Removal relative to cowbird laying. Treating each parasitized clutch and the mean for all un- each removal separately, I determined the inter- 46 SPENCERG. SEALY

TABLE 1. Number of hosteggs in unparasitizedand parasitizedYellow Warbler nests.

No. of rlvtches Unparasitized Parasitized Total Total 2 eggs 3 eggs 4 eggs 5 eggs nests X k SE 3 eggs 4 eggs 5 eggs nests R + SE

1974 1 15 17 33 4.5 + 0.02 0 11 6 17 4.4 * 0.03 1975 0 27 25 52 4.5 * 0.009 3 7 6 16 4.2 & 0.05 1976 4 25 30 59 4.4 * 0.01 1 9 9 19 4.4 * 0.03 1980 1 20 49 4.6 & 0.01 0 5 0 5 4.0 * 0.00 1981 4 34 ;; 71 4.5 * 0.008 3 11 10 24 4.3 * 0.03 1982 5 52 45 102 4.4 * 0.006 4 20 4 28 4.0 * 0.02 1983 I 67 63 137 4.4 & 0.004 7 7 2 16 3.7 + 0.05 1984 1 12 67 103 183 4.5 + 0.004 2 18 8 28 4.2 + 0.02 1985 10 59 56 12.5 4.4 * 0.005 5 27 7 39 4.1 + 0.01 1986 57 122 188 4.6 f 0.003 1 17 6 24 4.2 f 0.02 Totals : 5: 423 528 1,005 4.5 + 0.0006 26 132 58 216 4.1 f 0.003

val between a cowbird’s laying and removal to host eggswere removed. In one case, a cowbird within one to two days (Table 3). I assumedthat egg was removed, possibly the only egg present, the cowbird that laid in the nest was the same from a nest that otherwise remained active. Fi- one that removed the egg.Between 2 1% and 54% nally, in three cases,Yellow Warbler eggswere of24 removals were on the day the parasite laid. taken, but I did not know whether a choice had At least 33% (8/24) of the host eggswere taken to be made. Thus, most warbler eggsremoved one or more days after the cowbird laid (Table were from among the first three eggsin the laying 3). Finally, about 13% (3/24) of the warbler eggs order. Cowbird eggsdisappeared from one other were removed on a day before the cowbird egg nest that otherwise remained active. was laid. Burial of cowbird eggsby Yellow War- blers precluded subsequent host-egg removal, CLUTCH MANIPULATIONS which may bias the data in favor of early records Experimental parasitism. The introduced cow- of removal. bird eggwas buried at only one of 47 nests(2.1%) Warbler eggswere sometimes removed from parasitized on LDl or LD2, from which one host “new” clutches initiated after the cowbird egg egg was removed. In 54 nests similarly parasit- had been buried. At 28 such superimposednests, ized but with no host eggsremoved, two cowbird host clutches were initiated 24 hr (1 nest, 3.6%) eggswere buried (3.7%) and five were deserted 48 hr (2, 7.1%), 72 hr (5, 17.9%), 96 hr (11, (9.3%). Combining burials and desertionsin these 39.3%) and 120 hr (9, 32.1%) after parasitism experimental groups, the results are not signifi- occurred. “New” clutches averaged 4.2 eggs(SE cantly different (x2 = 2.3 1, df = 1, ns). Thus, = 0.02, II = 25) compared with an average of Yellow Warblers were no more likely to reject 4.7 eggs(SE = 0.05, 12= 144) per unparasitized an experimentally introduced cowbird egg, nest (Mann-Whitney U-test, z = 2.059, P < 0.02). whether or not a host egg was removed. Cowbird discrimination between cowbird and Clutch reduction.Females at all nine nestsfrom warbler eggs.Because cowbirds lay so early, they which I removed first-laid eggsas they were laid must rarely have removed an egg in the brief continued to lay. Seven females completed their daylight interval before laying, although Nolan clutches(four of four eggs,three of five eggs)and (1978:37 1) observed this once, within a few sec- one nest was depredated after egg C was laid. A onds of laying. For this reason, when a cowbird cowbird removed egg B later the day it was laid laid and a host eggdisappeared on the same day, in the ninth nest after having parasitized the nest I assumed laying preceded removal. This sce- earlier in the day. Egg C was laid the next day, nario required the cowbird to return to the nest but the nest was eventually deserted. and to choose whether to remove a cowbird or All six females tolerated the reduction of their warbler egg. Of the 30 nests in Table 2, at least clutches to one egg, when egg B and all subse- seven contained only warbler egg(s)at the time quent eggswere quickly removed as they were of removal. In at least 19 parasitized nests, only laid, which always left only egg A in the nest.

48 SPENCERG. SEALY

377) revealed that if female cowbirds remove other hand, do not remove host eggs, possibly an egg at all, they may do so either on a day becausethey cannot lift them (see Soler 1990). before, later on the day they laid their own eggs, or on a subsequent day (see Table 3). Host-egg REMOVAL OF COWBIRD EGGS removal by cowbirds at the moment of parasit- Cowbirds should be expectedto remove cowbird ism has been reported only twice (e.g., Prescott eggsat already-parasitized nests, as long as they 1965, Nolan 1978:371), and the (same?)females are not their own, becausethis would maximize returned to lay within secondsof removing the the care their own young would receive from the egg. Cuckoos, on the other hand, seem to mon- foster parents. Brooker and Brooker (1989) ar- itor potential host nests more closely and para- gued that single-egg parasitism among cuckoos sitize them when they contain one or two eggs, allows a parasite to remove a host egg at laying removing the egg when the nest is parasitized. without inadvertently removing one of its own In the present study, cowbirds removed an egg eggs.This behavior is adaptive because cuckoo from about one in three Yellow Warbler nests eggsoften mimic those of the host eggs. In the parasitized, over the entire breeding season.Al- Brown-headed Cowbird, Elliott (1977) suggested though the percentageof eggremovals from nests that the first cowbird eggslaid in multiply par- differed statistically over the season,this appar- asitized nests were deliberately placed in certain ently resulted from differences among the first nests,while subsequenteggs were placed lessdis- four weeks of the season, rather than a decline criminately. He reasoned that this distribution in the number of eggsremoved per nest, as Zim- should result from females avoiding nests they merman (1983) reported for the Dickcissel (Spi- had already parasitized, and should reduce the za americana). Also, the number of warbler eggs possibility of a female cowbird mistakenly represent in parasitized and unparasitized nests moving one of her own eggs,when attempting varied discordantly among the years, which sug- to remove a host egg. Elliott (1978) interpreted gests that there were annual differences in the the high frequency of mistaken removals of cow- rate of egg removal. Why such variation in egg- bird eggsin his study as evidence in support of removal rates exists is not known. Perhaps some this contention. This explanation, however, is females always remove eggs,while others do not. not entirely consistent with what is known about As cowbirds do not remove eggsat the same time the laying and egg-removal patterns of cowbirds. they parasitize nests,they may not always be able Becausecowbirds usually do not lay their own to return to remove an egg,or nest defense(Hob- eggs and remove host eggs at the same time, son and Sealy 1989) sometimes may be effective. females that return to steal a host eggmust often In populations of the Yellow Warbler in On- choosebetween it and their own egg. tario, Clark and Robertson (198 1) estimated that host eggswere removed from about one-half of COWBIRD NEST VISITS AND all parasitized nests, whereas Burgham and Pic- TIME OF DAY man (1989) recorded egg removal from only Cowbirds that parasitize nests before they con- two of the 15 (13.3%) parasitized neststhey stud- tain host eggsmust return to the nest to remove ied. In Michigan, more than one egg was re- an egg.This not only forcesthe cowbird to choose moved from each parasitized Yellow Warbler between its own egg and the host’s, but the nest nest (DellaSala 1985). It is not known whether must be visited at least once more, which in- the geographic differences in egg-removal rates creasesthe chances of encountering hosts. Even are real, or whether they reflect year-to-year dif- cowbirds that remove host eggsbefore they par- ferenceswithin the populations. asitize nests must make additional trips to the Estimates of eggremoval from nests of several nest (see also Mayfield 196 1). Again, this behav- other cowbird host specieshave ranged from 46% ior seemsparadoxical becausecowbirds lay ear- to 85% of parasitized nests (e.g., Hann 1937, lier in the day than their hosts (Scott 1991) and Nice 1937, Smith 198 1). Interestingly, cowbirds lay within only a few seconds(e.g., Nolan 1978: almost always remove one eggfrom Red-winged 371), which suggestscowbirds attempt to mini- Blackbird nests, a larger host (Blankespoor et al. mize the chances they will be detected by hosts 1982, Roskaft et al. 1990). Cuckoos that para- at their nests. The undetermined odds that a fe- sitize hosts much larger than themselves, on the male cowbird will find a Yellow Warbler nest EGG REMOVAL BY COWBIRDS 49 unattended again are probably small. This may she had laid. She did not lay in the nest that day, be another reason why cowbirds do not remove although she resumed laying the next morning an eggfrom every Yellow Warbler nest they par- and eventually completed her clutch. Common asitize. Interactions between other hostsand par- Cuckoos, on the other hand, may have evolved asiteshave been shown to increasethe likelihood away from morning laying (Davies and Brooke of rejection by hosts (e.g., Davies and Brooke 1988). Results of theseauthors ’ experiments sug- 1988), hence cowbirds may limit egg stealing to gest that this speciesparasitizes Reed Warblers situations where the benefits accrued through in the afternoon, when they are likely inattentive, consumption of the egg(s) outweigh the risk of because to do so in the morning would lead to encountering the host. rejection of the cuckoo’s egg. Chance and Hann (1942) regarded the early- morning laying of the Brown-headed Cowbird as ADAPTIVE VALUE OF EGG REMOVAL a specialization for brood parasitism, which im- Above, I have discussedrisks that cowbirdsmight plies that this behavior evolved in the context of take when they steal eggs from host nests, i.e., parasitism. These authors suggestedthat cow- mobbing by hosts, rejection of parasitism, and birds lay around sunrise so as not to disturb mistakenly removing their own eggs.However, host females, which they believed would be away parasites,and perhaps even hosts in some cases, foraging before laying their own eggs,and hence presumably benefit from this behavior. Never- inattentive. However, Scott (199 1) compared the theless, results of experiments conducted in the time of day of laying of the Brown-headed Cow- present study did not support two hypotheses bird and several non-parasitic icterines, and con- proposed to explain this behavior. Firstly, ex- cluded that the cowbird’s early laying time may perimentally parasitized Yellow Warblers were simply be a primitive icterine trait, which prob- no more likely to reject a cowbird egg, whether ably did not arise as an adaptation for parasitism. or not a warbler eggwas removed at the time of Nevertheless, Scott (199 1) believed that laying parasitism. This result, and those of other studies very early allowed female cowbirds to parasitize that have tested the host deception hypothesis, nests before the hosts arrived to lay. That cow- involving both cowbird and cuckoo hosts(Roth- birds do not parasitize nests on a particular day stein 1975a, Davies and Brooke 1978, Moksnes of the host’s laying cycle frees them to parasitize and Roskaft 1989) demonstrates that host-egg nests earlier in the morning. removal does not deceive hosts into accepting Laying earlier in the day, however, may not parasitic eggs.Secondly, the removal of only one necessarilyallow cowbirds to sneak into Yellow eggfrom some Yellow Warbler nests, when they Warbler nests unseen, even though the warblers apparently can safely remove more than one have not yet laid. This is because some females without causing nests to be deserted, suggests roost overnight in their nests, starting in some that cowbirds remove one eggfor a reason other casesbefore they have laid their first eggs,with than nourishment, and simply take advantage of the frequency increasing through egglaying (Sea- a free meal. This behavior may enhance the cow- ly et al., unpubl. data). Becauseroosting females birds’ own egg production over the season (see usually do not leave their nestsuntil after sunrise, Payne 1974; Lohrl 1979). presumably they would be confronted by the The responsesto experimentally reduced Yel- cowbird when it arrives to lay. Yellow Warblers low Warbler clutches revealed that nest aban- are known to respond to the threat of cowbird donment was not simply a result of disturbance parasitism by rushing to their nests and sitting by potential predators or parasites(cf. Hamilton tightly in them (Hobson and Sealy 1989) but I and Orians 1965) becauseonly one control nest do not know whether warblers can actually deter was deserted despite control nests being dis- cowbirdsbent on parasitizing their nests.At nests turbed repeatedly. Nor was nest desertion simply in which female warblers did not roost, laying a responseto partial clutch lossesbecause war- early may allow cowbirds to avoid flushing ovi- blers abandoned one- and two-egg clutches only positing females, although it is not likely that when eggswere removed from complete clutches females flushed under such circumstanceswould but not during laying (see also Rothstein 1986, desert their nests. Once I inadvertently flushed Armstrong and Robertson 1988). The results, a female Yellow Warbler from her nest before however, may relate to the magnitude of eggloss 50 SPENCER G. SEALY in the two situations, rather than to nesting stage. in new nests if all, or all but one, of their eggs During laying, one-egg clutches were tolerated, were removed. Experiments on accepter species but the initial clutch size was never more than (Common Grackle, Quiscalusquiscula, and East- two, and one of these eggswas removed quickly. em Phoebe, Sayornisphoebe)revealed that birds Three- and four-egg clutches (still in the laying do not count their eggsbut instead “assess” their stage)might be abandoned if they were suddenly volume collectively (Rothstein 1982, 1986; see reduced to one egg, as resulted from manipula- also Holcomb 1970). Interestingly, this assess- tions during incubation. Warblers possibly do ment producesthe paradoxical finding that phoe- not assessthe overall value of their clutchesuntil bes are less likely to desert their four- to six-egg after they are complete. clutches if they are reduced to two cowbird eggs If cowbirds removed eggsprimarily for nour- than to two of their own eggs.This may be be- ishment, they should be expectedto remove more cause the two cowbird eggs represent a larger of them, possibly returning each day to remove proportion of the original clutch volume (Roth- the next-laid egg. However, this behavior would stein 1982, 1986). Similarly, Yellow Warblers in increase the chances of female cowbirds being the present study tended to desert clutches re- intercepted at host nests, although waiting until duced to only one of their own eggs or to one the clutch is complete before returning to take cowbird egg, but incubated most clutches re- the eggsall at once may not be an option. This duced to one warbler plus one cowbird egg and is because cowbirds cannot carry off more than all clutchesreduced to two cowbird eggs.Perhaps one egg at a time because they impale them on parental investment and its payoffs are impor- the tips of their mandibles. Either way several tant for hosts such as the Yellow Warbler. That trips would be necessaryto remove more eggs. Reed Warblers abandon a single egg but not a Such disturbances at the nests might causehosts single chick strongly suggeststhat the schedule to desert, although observations in the present of parental investment is an important consid- study suggestthat abandonment was a response eration in the “decision” to abandon nests. to something other than, or in addition to, dis- Hann (194 1) argued that if cowbirds removed turbance, assumingthat warblersview in the same eggsto obtain extra nourishment, unrelated to way visits to their nestsby humans and cowbirds. egg laying, we should expect both males and fe- Perhaps egg-remoying cowbirds show restraint males to remove eggsfrom parasitized and un- becausethey apparently could remove more eggs parasitized nests. This has not been observed without causing hosts to desert. However, it is (e.g., Scott 1977, this study). If the extra meal not known whether cowbirds have the time and was tied to the need for calcium, we might expect ability to remove more eggsbut do not do so. only females to remove eggs. Indeed, evidence Davies and Brooke (1988) concluded that the that free-ranging male cowbirds eat eggsis scarce pattern of removal, and replacement, accurately and equivocal (e.g., Friedmann 1963:26; Sealy, predicted the observed behavior of the Common unpubl. data), although experiments on captive Cuckoo, which is usually to remove one host egg cowbirds revealed males do have egg-pecking from each parasitized nest. These authors noted tendencies (Burgham and Picman 1989). that Reed Warblers nearly always deserted Despite the advantagesgained from eating host clutches reduced to one egg, but never deserted eggs,we must still reconcile why usually only one a singlewarbler chick in naturally reducedbroods. egg is removed from a host nest. Livesey (1936) Thus, while the adult cuckoo is limited by the suggestedthat cuckoos remove an egg to test number of eggs it can remove, later when the whether the clutch is fresh or incubated, thus cuckoo chick hatches it can eject all host eggs ascertaining whether or not the nest is suitable and nestlings without penalty. Davies and for parasitizing. He noted that ingesting the eggs Brooke’s (1988) results, and those of the present may simply be a convenient way of disposing of study, may not prove that cuckoosand cowbirds, them. If the function of egg removal was to test respectively, remove host eggsto gain extra nour- the incubation status of host clutches, the para- ishment, but in the caseof the Common Cuckoo, site would be expectedto eat a host egg beforeit they nicely resolvethe dilemma ofwhy both adult commits its own egg to the nest. However, this and nestling cuckoos remove them. is not the normal sequenceof events in parasitic Rothstein (1982) found that most passerine cuckoos. Cuckoos usually parasitize nests when birds deserted their nests and laid new clutches they contain one or two host eggs,and normally EGG REMOVAL BY COWBIRDS 5 1 remove and hold the egg in their bill while they the original cause of the development of the egg lay their own egg (e.g., Wyllie 1975, Gartner removing habit, which merely seemsto have been 1981). Thus, the egg is not eaten, i.e., “tested,” favored by natural selection by virtue of the re- until after they have laid their own and left the sult.” host’s nest. In fact, cuckoosusually swallow host Enhanced incubation efficiency in parasitized eggswhole (Wyllie 1975). As cowbirds often par- clutches is the only explanation for host-eggre- asitize nests before the hosts have started to lay moval that has received support (seeDavies and (e.g.,Nolan 1978372, Clark and Robertson 198 1, Brooke 1988). This explanation indeed resolves this study), they appear not to be concerned with the dilemma of parasites removing an egg when the incubation statusof host clutches.If cowbirds they parasitize nests, and when they hatch still tested nests randomly, we should expect more evicting or outcompeting host eggsand young. well-incubated eggsto be removed without being In this context, without egg removal incubation replaced, but they seldom remove eggsfrom in- might be prolonged in enlarged clutches, thus cubatednests (e.g., Friedmann 1963, Nolan 1978: exposing nests to predation for a longer time, 377, this study). and possibly decreasingthe survival rates of the Although the results of the present study (see young (Zimmerman 1983). As many parasitized also Rothstein 1986, Davies and Brooke 1988) nests, from which no host eggswere removed, reveal that cowbirds can remove more than one have increased total clutch sizes and hence vol- host egg without penalty, removing extra host ume, incubation times could be increased be- eggsactually may be costly to the parasite. Da- cause of the female’s inability to maintain an vies and Brooke (1988) suggestedthat the more adequately high eggtemperature over all the eggs eggsthat remain in a host nest, the less likely a or the need for the female to be off her nest for secondcuckoo will remove the first cuckoo’s egg longer inattentive periods of feeding in response by chance. This is because cuckoo eggsusually to increasedenergy demands (Biebach 198 1). This mimic host eggs.But cowbird eggsdo not mimic hypothesis provides a fruitful avenue for future host eggs.Thus, they are “the odd ones out” in investigation into the adaptive value of host-egg many host clutchesand, as such, may be subject removal by brood parasites. to selective predation (see Verbeek 1990). Al- though such an outcome would be disadvanta- SUMMARY geousfor the cowbird, it might be advantageous Observations presented in this paper reveal that for hoststhat acceptcowbird eggs,especially spe- Brown-headed Cowbirds sometimes remove cies whose productivity is not severely reduced Yellow Warbler eggsin association with the act by raising parasitic young. This hypothesis has of parasitism, and although the stolen eggsare not been tested (but see Mason and Rothstein often eaten, the behavior seemsto be a breeding 1987). strategy rather than a form of predation. How- Lack (1954:42-43) argued that eggremoval by ever, whatever the function of host-eggstealing, laying female Great Spotted Cuckoos (Clumator present knowledge suggeststhat it is not a re- glandarius) is adaptive because it reduces nest- sponseto evolved host defenses,and hence does ling competition. However, Hamilton and Ori- not represent an example of coevolution (Roth- ans (1965) pointed out that this argument fails stein 1990). to explain why laying female parasites remove eggseven though their nestlings evict their nest- ACKNOWLEDGMENTS mates. These authors believed that because the I thank the staff of the University of Manitoba Field young of some parasitesresolve the competitive Station (Delta Marsh) for providing support and com- aspects of nest life by promptly evicting nest- fortable living conditions during the field work. Per- mates, the advantage of egg removal at the time sonnel of the Delta Waterfowl and Wetlands Research Station and Portage Country Club permitted me to of laying is not in reducing competition or crowd- conduct some of this work on their properties. I thank ing. Friedmann (1960:31) stated that “it is true G. Biermann, J. Briskie, C. Churchward, M. Gifford, that egg removal by the laying parasite some- P. Goossen. B. Grantham. P. Hebert. K. Hobson. D. times easesthe ensuing crowding and competi- Kinnear, W. Manchur, MI Peters, an’d D. Sutherland for assistancein the field. Paul Goossen and Percy tion, but only to the extent of obviating what Hebert allowed me to use some of their unpublished would otherwise be excessivecrowding. In this data. Gloria Biermann helped me with the statistical connection, we cannot assume such a ‘goal’ as analyses,and along with J. V. Briskie, L. S. Forbes, K. 52 SPENCER G. SEALY

A. Hobson, S. I. Rothstein, D. M. Scott, and two anon- CHANCE,E. P., AND H. W. HANN. 1942. The Euro- ymous reviewers read various drafts of the manu- pean Cuckoo and the Cowbird. Bird-Banding 13: script carefully and critically and offered many sug- 99-103. gestions that improved the paper. Financial support CLARK,K. L., AND R. J. ROBERTSON.198 1. Cowbird was provided by the Canadian National Sportsmen’s parasitismand evolution of anti-parasitestrategies Fund, Chapman Fund of the American Museum of in the Yellow Warbler. Wilson Bill. 93:249-258. Natural History, Manitoba Department ofNatural Re- DAVIES,N. B., ANDM. DEL. BROOKE.1988. Cuckoos sources (Wildlife Branch), Manitoba Naturalists So- versus Reed Warblers: adaptations and counter- ciety, Natural Sciences and Engineering Research adaptations. Anim. Behav. 361262-284. Council of Canada (arant no. A9556). and Research DELLASALA,D. A. 1985. The Yellow Warbler in Board of Senate of the University of’Manitoba. 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