Anita. Behav., 1989, 38, 510-519

Responses of yellow warblers to the threat of cowbird parasitism

K E I T H A. HOBSON & S P EN CER G. SEALY Department of Zoology, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada

Abstract. Responses of yellow warblers, Dendroica petech&, to a model of a female brown-headed cowbird, Molothrus ater, and a fox sparrow, Passerella iliaca, control were tested during the nest-building, egg-laying, incubation and nestling stages of the nesting cycle. Testing pairs only once avoided the risk of habituation to models. Females rarely responded aggressively to models or showed distraction displays. Instead, a nest-protection behaviour involving 'sect' calling and a rush to sit in the nest was observed, primarily in response to the cowbird model. Yearlings did not show this behaviour as frequently as older or previously parasitized birds. Females gave fewer seet calls when they defended cryptic compared with exposed nests. They gave more seet calls and fewer 'chip' calls in response to the cowbird model than the control. The frequency of seet calling by females was highest during egg laying when they were most susceptible to cowbird parasitism. Males responded infrequently to all models and were first to arrive in only 5% of trials.

The yellow warbler, Dendroica petechia, is parasit- ized frequently by the brown-headed cowbird, Molothrus ater (Schrantz 1943; McGeen 1972; Clark & Robertson 1981; Lowther 1984). Once a cowbird has laid an egg in a yellow warbler nest, the female warbler responds in one of three ways. She may accept the egg or reject it, either by deserting the entire nest or burying the cowbird egg and any eggs of its own present at the time by adding more nesting material. All of these responses have costs associated with them. Acceptance results in cow- bird nestlings that outcompete the warbler nest- lings (Goossen 1978; Clark & Robertson 1981). Egg burial and renesting necessitate delays that can lower the reproductive success of those individuals that reject cowbird eggs (Clark & Robertson 1981). Clearly, brood parasitism is a selection pressure that favours the evolution of antiparasite defences by this and other potential hosts. The most adapt- ive defences should be ones that reduce the chances that cowbirds will lay any eggs in hosts' nests.

Aggression by potential hosts toward cowbirds when they are near their nests may effectively deter cowbirds, and thus avoid parasitism (Robertson & Norman 1976; Slack 1976; Scott 1977). However, particularly amongst smaller passerines like the yellow warbler, aggression may not effectively drive them away (Hann 1937; Prescott 1947; Scott 1977). In fact, it may even be used by the parasite as a cue to find a host's nest (see Smith et al. 1984). Several workers using live cowbirds or models have shown that yellow warblers apparently recognize

the threat that female cowbirds pose and are often 'aggressive' toward them (Robertson & Norman 1977; Folkers 1982; Burgham 1985; Folkers & Lowther 1985). However, these previous studies suffered from several methodological problems that complicated the interpretation of the role of aggression per se as an anti-brood parasite defence in this species. In all cases only 8-12 pairs of birds were tested and thus the extent of variability of response within populations remains poorly under- stood. All studies used the subjective aggressive score index of Robertson & Norman (1977) that combined motor pattern and proximity measures in a single response value. Thus it remains unclear to what extent hosts used aggression, distraction, vocalizations or other behaviour to defend their nests (see Moran et al. 1981; Smith et al. 1984). The studies that investigated the patterns &response by yellow warblers to cowbirds over the breeding season tested pairs more than once, and thus introduced the possible bias of habituation (see Knight & Temple 1986a, b).

In this paper we investigated the nature of responses of yellow warblers to models of female brown-headed cowbirds placed near their nests throughout the breeding season. We tested large sample sizes from a single parasitized population, tested pairs with the model only once, and did not use a subjective score index. This allowed us to analyse the nature and timing of this host's re- sponses more rigorously. We hypothesized that yellow warblers should respond to the cowbird

0003-3472/89/090510+10 $03.00/0 �9 1989 The Association for the Study of Animal Behaviour 510

Hobson &Sealy: Warbler responses to cowbirds 511

model most strongly during the egg-laying and early incubation periods when they are most susceptible to cowbird parasitism, but made no a priori predictions about the nature of that re- sponse. We also investigated whether the response was influenced by the host's age or previous experience with the brood parasite.

S T U D Y AREA A N D M E T H O D S

From 25 May to 8 July 1986 and 19 May to 8 July 1987, we studied nest-defence behaviour of yellow warblers toward cowbirds in the forested dune ridge that separates Delta Marsh and Lake Mani- toba, Manitoba (see Scaly 1980 and MacKenzie 1982 for descriptions of the study site). In both years, yellow warbler pairs were chosen for testing with models with usually at least one member of the pair uniquely colour banded. Only the first nests of the season were tested. We presented models of a female brown-headed cowbird and fox sparow, Passerella iliaea, at approximately 0-5 m from each warbler nest. The fox sparrow was used as a control. It does not occur on the study site when yellow warblers are breeding, thus, any confound- ing influence of differences in prior experience with this species were eliminated. In addition, fox sparrows are approximately the same size and shape of female cowbirds. Thus, any differential response of a yellow warbler to cowbird and control due to body size were removed.

Models were freeze-dried specimens mounted in perching positions that were attached to branches or foliage with clips to mimic an intrusion. Models were placed within 1.0 cm of nest height and faced the nest bowl. Prior to testing, a portable blind was set up 3-10 m from the nest. If the pair being tested was building, egg laying or rearing young, we waited until nest visits resumed and after the parents left the vicinity of the nest before the first model was presented. In five trials, an incubating bird was disturbed but we allowed it to incubate again for 15 min before presenting a model. We presented models and returned to the blind within about 10 s (range 8-15 s).

As part of another study, we also presented a model of a grey catbird, Dumetella carolinensis, at some nests. Models were tested for 5 min, begin- ning from the time one of the parents returned unless an individual left the nest area during the trial. Timing started only after we returned to the

: Z

v

o

g 8

a)

b/

0 0 0.5

Time (s)

Figure 1. Sonograms of yellow warbler (a) chip and (b) sect calls.

blind. After a model was removed, we waited at least 20 min before presenting the next one. At most, three models were presented at each nest, all between 1000 and 1930 hours. Behaviour was recorded directly into a portable cassette tape- recorder and later transcribed.

As in Smith et al. (1984), we scored the proximity and behaviour of yellow warblers to the model for each 10-s period within a trial as follows: (1) the distance of focal birds from the model in one of the three distance classes, less than 2 m, 2-5 m, and greater than 5 m; (2) alarm calling ('seet' or 'chip' calls, see Fig. 1); (3) perch changes; (4) in view and perched; (5) close pass or hover over model; (6) contacted model; (7) distraction display; (8) sitting in nest (female only); (9) preening; (10) feather

512 Animal Behaviour, 38, 3

ruffling or head scratching; (11) bill wipe; (12) foraging (including searching); and (13) out of sight or leaves area. Several chip and sect calls were recorded in 1987 on the study area with a Dan Gibson parabolic microphone and a Uher Report L tape-recorder. One representative example of each call, readily distinguished by ear, was sona- graphed with a Kay Elemetrics 6061B sonograph.

Distracton displays involved adults 'hunching' while they fluttered their wings rapidly or quivered them above their bodies, This behaviour was performed as they moved along branches or dropped to the ground. Preening, foraging, ruffling feathers or head scratching, and bill wiping were included because they may be displacement activi- ties that were elicited by the model stimulus (see Robertson & Norman 1976). The categories in view and perched, distraction display, sitting in nest, and out of sight or leaves area were mutually exclusive and, together with distance categories, were analysed as the number of 10-s periods within trials that the bird was observed engaged in these behaviours. All other categories were quantified by counting the actual number of behaviours observed in a 5-rain trial.

If a second bird arrived during a trial, we continued to record the behaviour of the focal bird. Only obvious behaviours such as contacts and distraction displays were recorded for the second bird. For most of the nests tested, the per cent exposure of the nest on four sides and from above were estimated from an arbitrarily chosen distance of 1 m from the nest. This value was then scored 1-5 based on 20% exposure increments with 1 corres- ponding to 80-100% exposure.

Pairs of yellow warblers tested with the cowbird and control were grouped into three categories: (1) pairs with females 2 years of age or older for which there was no evidence of brood parasitism by cowbirds during that breeding attempt; (2) pairs with females of various ages that had been parasit- ized as evidenced by cowbird eggs present or buried; and (3) pairs in which the female was 1 year old (and thus would not have been exposed to cowbird parasitism in previous nesting attempts) and was not parasitized at the time of testing.

Sealy and co-workers have uniquely banded yellow warblers every year from 1974 through l987 on a 3-kin portion of the dune-ridge forest. Each warbler captured in mist nets was banded with a standard U.S. Fish and Wildlife Service aluminum band in combination with coloured celluloid

hands. In subsequent years, any of these indi- viduals seen or recaptured were known to be 2 or more years old. Beginning in 1981, nestlings were banded with an aluminum band plus a year-specific celluloid band; free-flying fledglings netted in late July and August were banded with an aluminum band and a different year-specific celluloid band. The ages of these individuals encountered in later years were known precisely.

The data were analysed using non-parametric statistical tests (Conover 1980). Changes in nest- defence variables over the four stages of the nesting cycle were analysed using Kruskal-Wallis tests. Wilcoxon two-sample tests were used to test for differences between periods. Wilcoxon signed- ranks tests were used to compare responses to different models. Chi-squared contingency analy- ses were used when proportions between trials or periods were compared. Unless otherwise stated statistical tests are two-tailed. The chosen level of significance was P < 0-05.

RESULTS

Response by Females Nest-protection behaviour

Females arrived first in 95% of the trials and so our data were based primarily on female responses. Females responded strongly to the cowbird model, particularly during the egg-laying stage (Table I). The response often involved a burst of seet calling after the model was discovered and a 'rush' to sit in the nest bowl, often for the duration of the trial. This nest-protection behaviour was in response primarily to the cowbird rather than the sparrow model and was observed throughout the breeding season (Table II). We also heard female yellow warblers responding with the sect call during seven natural encounters with female cowbirds and three times saw them sitting in their nests during these encounters. In these observations cowbirds were usually at least 3 m from the warblers' nests. Several times our attention was drawn to the presence of a female cowbird after we first heard seet calling.

Vocalizations The frequency of seet calling changed signifi-

cantly over the season in response to the cowbird model (Table I) and was highest during the egg- laying stage (Kruskal-Wallis test, Zz=19.24,

Hobson &Sealy: Warbler responses to cowbirds

Table I. Summary of female yellow warbler responses to female brown-headed cowbird and fox sparrow mounts presented near the nest (2_+ SE)

513

Stage

Nest building Egg laying Incubation Nestling Response variable (19, 18)$ (36, 20) (47, 31) (21, 24)

Seets 50.8_ 16-5"* 108.5+24.4"* 26-8_+5-9** 24.4-1-6-2"* 14.8___6.1 35.9_+ 1 8 . 4 11.5+4.3 6.0+4.5

Chips 0.8-1-0.4" 13.6___6.1 10.9___3.3" 6.5__+3.4* 4.9 + 3.5 10.6_+ 5.5 20.6 + 5.8 22-3 + 7-5

Less than 2 m 18-9 ___ 2-8 22-3 ___ 1.9* 19-8 + 1.7 20.4_+ 2.8 12.1 _+2.7 13.2_+2.7 1 8 - 6 _ + 2 . 2 12.0_+2.4

2 5 m 7.1+2.4 6.3_+1.7 6.6_+1.3 8-1_+2-6 11.4_+2.6 12.8-+2.7 7-6__+ 1.9 13.8_+2.5

Greater than 5 m 0.6+0.5 0.7___0.4 2.6_+ 1.0 0.1 _+0.1 6.4_+2.0 4.1 _+ 1.5 3.8_+ 1.4 4.3 _+ 1.7

Perch changes 8.6_+ 2.8 8.1 _+ 1.4 9.6_+ 1.8 7.3 • 1-7 12-4___ 1.9 7.9__+ 1-5 13.1 ___2.0 12.1 __+2.7

Silent watching 10.4_+2.4 10.8_+ 1.9 12.8_+ 1.8 13.3_+2.6 8.4+2.2 8.5_+2.0 9.3_+ 1.8 7.7_+2.3

In nest 11.8_+3.0" 1 4 . 3 _ + 2 . 2 " 1 3 - 3 _ + 1 . 9 " I5.4_+2.8" 2-8__+ 1.9 4.6__+ 1.9 7.5__ 1.9 5.1 _+2.1

Distraction displays 1.5 _+ 0.4 2-1 _+ 0.8 1.6 _+ 0.5 0.8 _+ 0.4 0.7_+0.7 0.4_+0.2 1.8_+0.7 1.5_+0.6

Contacts 0.3 _+ 0.3 0.4 _+ 0.2 0-5 + 0-4 0.1 _+ 0.1 0 0 0 0

Close passes 0.1 _+0.1 0.2+0.1 0.1 +__0.1 0.2_+0.2 0 0'1_+0.1 0.1_+0.1 0

Head scratch or 0 0.3_+0-1 0.2+0-1 0.1 -+0.1 feather ruffle 0 0 0 0

Bill wipes 0"9__+ 1.6 0.5___0-2 0.5-+0.2 0.1 _0.1 0.2+0.2 0.6+0.2 0.5__+0.2 0.2-+0.1

Preens 0.2-+0.1 0.2_+0.2 0.1 _+0.1 0 2.8-1-1.5 0.9-+0.6 0 0

Forages 0.2 _+ 0.1 * 0-03 _+ 0.03 0.1 __+ 0-04 0.1 _ 0.1 3.6-+ 1.1 0.9-1-0.4 0.2+__0.1 0.3+0.1

Departures or not seen 0.9 _+ 0.6 0.4 +_ 0.3* 0.9 _ 0.5 0.2 _+ 0.1" 2.2_+0.1 3.0-+ 1-4 1.1 _+0.5 4.7_+ 1.6

? Categories of distance, silent watching, sitting in nest, distraction displays, and time spent out of sight (departures) are given as the mean number of ! 0-s periods within trials that the bird was engaged in these behaviours. All other categories are given as the mean number recorded in the 5-min trial.

$ Number of trials for cowbird and control given in parentheses. Results of Wilcoxon signed-ranks test between models are indicated by ** P < 0.01, * P < 0.05.

P<0.001) . The frequency of this response de- creased significantly between the egg-laying and both the incubation (Wilcoxon two-sample test, Z = 3.87, P < 0.0005) and nestling (Wilcoxon two- sample test, Z=2 .77 , P < 0.001) stages. A similar pat tern was observed for responses to the sparrow model (Table I) but here changes over the season were not significant (Kruskal-Wall is test, t: 2 = 6.66,

P > 0-05). Females gave more seet calls in response to the cowbird model than to the sparrow model in all stages (Wilcoxon signed-ranks test, T>2.37, P < 0.01 for all comparisons). Females gave fewer seet calls when they defended cryptic (exposure i n d ex =5 ) compared with exposed (exposure i ndex= 1) nests (Wilcoxon two-sample test, Z = 1'97, P<0 .05) .

514 Animal Behaviour, 38, 3

Table !I. Proportion of trials where female yellow warblers responded to the female cowbird and sparrow models with the 'nest-defence' behaviour and the results of chi-squared tests for diferences between models

Model Test

Stage Cowbird Sparrow Z2 p

}qest building 0.47 0.11 2.08 > 0.1 (19)* (18)

Egg laying 0.50 0.20 4.85 < 0.05 (35) (20)

Incubation 0.62 0.19 12.86 <0.001 (47) (3 I)

Nestling 0.67 0.13 13.99 <0.001 (21) (24)

* Number of trials given in parentheses.

Females generally 'chipped' more in response to the sparrow model than to the cowbird model and these differences were significant for all stages (Wilcoxon signed-ranks test, T> 1.46, P < 0-05 for all comparisons) except during egg laying (Wil- coxon signed-ranks test, T= 11.26, P>0 ' I ) . How- ever, the frequency of chipping in response to either cowbird or control models did not change signifi- cantly over the breeding season (Table I).

Distance of approach Females spent more time closer to the cowbird

model than to the sparrow model during egg laying (Wilcoxon signed-ranks test, T=2-35, P<0.01) but no other significant differences in distance of approach between models was found for all stages (Wilcoxon signed-ranks test, T< 1-07, P>0.1 for all comparisons). Females sat in their nests more frequently when they responded to the cowbird model than to the sparrow model for all stages (Wilcoxon signed-ranks test, T> 1.87, P < 0-05 for all comparisons). This reflects the greater fre- quency of nest-protection behaviour in response to the cowbird model. Females also sat in their nests less frequently when defending cryptic compared with exposed nests (Wilcoxon two-sample test, Z=2.02, P < 0.05).

Aggressive responses and displacement behaviours Aggressive responses involving contacts or close

passes were observed rarely in response to cowbird and sparrow models. Distraction displays were rare during trials with any of these models. Displace- ment behaviours occurred in low frequencies for all

models during all periods with the possible excep- tion of foraging during the nest-building stage (Table 1). Here the frequency of foraging was higher for trials with the sparrow model than for trials with the cowbird model (Wilcoxon signed- ranks test, T=2.44, P<0-01). Female yellow warblers were recorded as 'left area or out of sight' more frequently during sparrow trials than during cowbird trials. Differences were significant for the egg-laying (Wilcoxon signed-ranks test, T= 1.40, one-tailed, P<0"05) and the nestling (Wilcoxon signed-ranks test, T= 1.75, P < 0.05) stages.

Effects of age and experience Responses to the cowbird model by female

yellow warblers based on age and experience categories are summarized in Table III. Using the a priori assumption that yearling birds with little or no experience should respond more weakly than older or more experienced birds, we used one-tailed statistical tests to compare age and experience categories. Yearlings gave fewer seet calls than older birds (Wilcoxon two-sample test, Z = 1.98, one-tailed P<0.05) but there was no difference between yearlings and birds of various ages that had been parasitized (Wilcoxon two-sample test, Z = 0.37, P > 0-7). Yearlings gave more chips than both older birds (Wilcoxon two-sample test, Z = 2.61, P < 0-01) and birds that had been parasit- ized (Wilcoxon two-sample test, Z = 2'56, P<0-01). Also, yearlings did not approach to within 2 m of the model as frequently as birds in other categories, but these differences were not significant (Table III).

Yearlings did not show the nest-protection beha- viour as frequently as older ()~2=8.52, df=l, P < 0"005) or more experienced 0 ( = 5.54, dr= 1, P<0-05) birds. Consequently, they changed perches about the model more frequently than did older (Wilcoxon two-sample test, Z = 1-99, P < 0.05) or parasitized (Wilcoxon two-sample test, Z = 2-07, P < 0-05) birds. Yearlings also sat in the nest less than older or parasitized females but these differences were not significant (Table III). Unlike older birds yearlings were also never observed to contact or swoop at the cowbird model.

Male response Males responded infrequently to the cowbird

model; thus, observations were restricted to conspi- cuous behaviours and the time spent in the vicinity of the model (Table IV). Males rarely behaved

Hobson & Scaly: Warbler responses to cowbirds

Table II1. Summary of yearling, older and parasitized female yellow warbler responses to a female brown-headed cowbird mount presented near the nest (l?-+ SE), and results ofKruskal Wallis tests for differences between categories

Female age or experience

Yearling Older Parasitized Response variable* (19)1" (19) (15) P:~

Seets 26-1+8.4 78.1_+24-9 24.2_+7.1 ys Chips 36.8+__12.4 5.3___3.8 6.5___5-9 <0.01 Less than 2 m 16.5_+2.8 23.4+__2.1 24.4-t-2-7 Ms 2-5 m 11.9_+2.8 5-4-+ 1.9 2.9__+2.0 <0.05 Greater than 5 m 1.6_+ 1.6 1.2+ 1-2 2.7_+2.0 Ms Perch changes I5.8-+3.2 8.1-+1.9 6.7-+l-9 <0-05 Silent watching 9-9-t-2.6 11-6+0.8 17.7-+2.9 NS In nest 9.3+2.8 15.7_+2.9 15.5___3.5 MS Distraction displays 0.5-+0.3 0 . 9 _ + 0 . 4 0.9+0.6 NS Contacts 0 0"6_+0"4 l ' l_+l ' l NS Close passes 0 0.3 -+ 0.2 0 NS Head scratch or 0-3 _+ 0,2 0.4_+ 0.2 0 NS

feather ruffle Bill wipes 0.6_+0.3 0.4-+0.2 0.4_+0.3 NS Preens 0.1 -+0 .1 0.2_+0-1 0 NS Forages 0-1 +0-1 0.I _+0-1 0 NS Departures or not seen 0.2 _+ 0.1 0.8 _+ 0.4 2.0 _+ 1.4 MS

* Categories as in Table I. t Number of trials given in parentheses. :~ NS indicates P>0.05.

515

Table IV. Summary of male yellow warbler responses to the female brown-headed cowbird model presented near the nest (J?_+SE), and results of Kruskal-Wallis tests for differences between stages

Stage Test

Nest building Egg laying Incubation Nestling Response variable* (6)I" (16) (29) (15) ;(2 p:~

Contacts 0-7+0-3 0 .3_+0 -2 0 .4_+0.2 0.8-+0.3 2.67 MS Close passes 0.7-+0.7 1 .0_+0-5 0 .9_+0 .4 0.5--+0.2 0.97 ys Distraction displays 0 0 0.1 +0.1 0.2-+0.2 3.71 ys Time in vicinity (s) 1 1 6 _ + 3 6 217-+19 243-+12 230-+25 8.23 <0.05

* Categories as in Table I. t Number of trials given in parentheses. :~ MS indicates P > 0.05.

aggressively but responded occasionally with sect calls and distraction displays. Because males were rarely the focal birds, their sect calls were not quantified. The time males spent in the vicinity of the model increased significantly after the nest-

building stage (Wilcoxon two-sample test, Z = 2 . 0 9 , P<0-05) . This reflects changes in the male 's time budget over the breeding season (e.g. incubation and nestling feeding). Males did not respond aggressively to the sparrow model and no

516 Animal Behaviour, 38, 3

change in time in the vicinity of this model occurred over the breeding season (Kruskal Wallis test, X2=4-01, P > 0-2).

D I S C U S S I O N

Female Nest-protection Behaviour Female yellow warblers reacted most strongly to

the cowbird model during egg laying when they were most susceptible to parasitism. These results support earlier suggestions by Robertson & Nor- man (1977), Folkers (1982), Folkers & Lowther (1985) and Burgham (1985) that female yellow warblers recognize female brown-headed cowbirds as brood parasites and hence a threat. Further comparison with these studies is not warranted, however, because these authors used aggressive index scores that mixed a variety of behaviours. For example, alarm calling and distraction displays are not aggressive behaviours per se and using them in a generalized score confuses the nature and possible evolutionary consequences of this host's re- sponse to threats of interspecific brood parasitism.

Female yellow warblers generally were not aggressive toward the model and rarely showed distraction displays. Small passerines such as the yellow warbler (about 10 g) are not likely to prevent cowbird parasitism effectively through aggressive attacks. However, small body size does not neces- sarily preclude effective defence against this brood parasite. Briskie & Sealy (1987) found that despite their small size (about 10 g), least flycatchers, Ernpidonax rninimus, were extremely aggressive toward a female cowbird model and noted that this species was rarely parasitized in the dune-ridge forest. In contrast, we noted that when the cowbird model was discovered, yellow warbler females responded vocally with a seet call and a rush to sit in the nest. To our knowledge, the seet call has not been described previously in this species. Burgham (1985) observed yellow warblers sitting in the nest, apparently in response to live cowbirds introduced prior to egg laying, but he subsequently referred to the behaviour, we believe incorrectly, as 'prema- ture incubation'. Our study showed that this nest- protection behaviour is common and occurred before, during and after egg laying. This response may prevent female cowbirds from gaining access to the nest and thus serve specifically as an anti- brood parasite defence, once the yellow warbler's nest has been located.

To our knowledge there are no reports of

cowbirds physically attacking and ejecting poten- tial hosts from their nests, although Hann (1937) observed an incubating ovenbird, Seiurus novabor- acensis, leave its nest immediately after a female cowbird suddenly appeared beside it. The nest- protection behaviour would probably not be used in response to a nest predator and, indeed, it was never observed during nest-defence studies using a mounted grey squirrel, Sciurus carolinensis (Hob- son et al. 1988). Nice (1943) reported that song sparrows, Melospiza melodia, responded vocally when cowbirds of either sex entered their territor- ies, but the utterances, vigorous 'tchunks', were the same as those given toward other intruding species. Hickey (1940) reported that male American red- starts, Setophaga ruticilla, did not respond vocally toward female cowbirds, in contrast to females which did react vocally, accompanied by bill snapping and tail spreading.

In their investigation of behavioural defences to brood parasitism by potential hosts of the brown- headed cowbird, Robertson & Norman (1976) predicted that the greater the selection pressure for anti-parasite defences, the greater will be the host's aggressiveness. Yellow warblers are heavily par- asitized hosts and, by this reasoning, would be expected to be highly aggressive toward cowbirds. On our study site the average rate of parasitism is about 21% (Sealy, unpublished data). In sub- sequent investigations, Robertson & Norman (1977) found that populations of yellow warblers in Ontario and Manitoba were equally aggressive and suggested that yellow warblers in Ontario have evolved this level of aggression in about 150 years. They suggested that western populations may have evolved their aggressiveness to some upper limit. Our study indicates that such comparisons of aggression may not be appropriate when consider- ing the evolution of anti-brood parasite defences. The nest-protection behaviour shown by yellow warblers on our study site may represent an advanced level of host defence. It should be looked for in other populations of yellow warblers as well as in other heavily parasitized species.

It might be expected that the nest-protection behaviour, which involves a call apparently not used in any other context by yellow warblers, might facilitate group mobbing (see Clark & Robertson 1979). However, despite nesting at densities of up to 15 pairs/ha on the study area (Goossen & Sealy 1982), we never observed group mobbing of cow- birds or other predators by yellow warblers.

Hobson &Sealy: Warbler responses to cowbirds 517

The nest-protection behaviour probably pre- vents cowbird access to yellow warbler nests in cases where the host is able to intercept the brood parasite. On average, hosts exhibiting this beha- viour are more likely to prevent parasitism by effectively intercepting cowbirds near their nests more frequently than hosts that do not. A counter strategy by cowbirds may be to wait until nests are left unattended. In this way, cowbirds may oc- casionally still parasitize hosts that defend their nests (Robertson & Norman 1976; see also Roths- child & Clay 1952).

The occurrence, albeit infrequent, of nest-pro- tection behaviour during trials with the fox spar- row model probably represents cases of mistaken identity. Fox sparrows resemble cowbirds, espe- cially when viewed from behind. Yellow warblers approaching from this direction might make such ~. mistake. If the behaviour functions to prevent cowbirds gaining access to the nest then it would be in the best interest of female yellow warblers to err on the side of caution in such circumstances. Alternatively, this response may be an artefact of earlier trials with the cowbird model. Perhaps the duration between trials was not long enough to prevent such an effect.

Female yellow warblers elicited fewer seet calls and tended to sit in the nest less frequently when they defended cryptic compared with exposed nests. Even though models were placed within 0-5 m of all nests, cryptic nests were not usually visible from that distance. Thus, females may respond to threats of cowbird parasitism facultatively, with the strength of the response depending upon the extent of the perceived threat. This result was similar to that found during nest-defence tests using a mounted grey squirrel (Hobson et al. 1988). Here female yellow warblers gave fewer distraction displays when defending cryptic nests. Ricklefs (1977) found that among tropical passerines, the strength of the defending parent's response was also related directly to the conspicuousness of the nest. Although yellow warblers responded differ- ently to the cowbird model, depending on the exposure of their nests, this does not necessarily suggest that nest crypticity functions in any way to reduce the incidence of cowbird parasitism. Both Nice (1937) and Smith (1981) suggested that exposed nests of song sprrows may be parasitized more frequently than concealed nests. However, in their extensive study into factors affecting parasit-

ism of Kirtland's warblers, D. kirtlandii, Anderson & Storer (1976) found no such correlation.

Age and Experience

Yearling females nesting for the first time uttered fewer sect and more chip calls in response to the cowbird model than did older females, or those of unknown age but with cowbird experience. Year- lings were also less likely to show the nest-protec- tion behaviour noted in older or experienced birds. This suggests that learning or experience plays a role in yellow warbler responses to potential brood parasites. The chip call is a general alarm vocaliza- tion that is probably innate. It is elicited by a broad spectrum of stimuli including human intruders, conspecifics, predators and benign novel objects placed near the nest (Hobson et al. 1988). The seet call appears to be much more specialized and specific to the cowbird stimulus as does sitting in the nest. Such responses probably have a learned component. Smith et al. (1984) found that indi- vidual song sparrows nesting in their second year were more aggressive toward cowbird models than when they were yearlings. Likewise, Folkers & Lowther (1985) found different patterns of re- sponses for parasitized and non-parasitized red- winged blackbirds, Agelaius phoeniceus.

Male Response

Male response to the female cowbird model was constant, but at a low level, throughout the breeding season. Nevertheless, male response tended to be higher toward the cowbird model than the fox sparrow model which suggests that the male may also recognize the cowbird as a specific threat. In general male yellow warblers' participation in nest defence appears to be low (Hobson et al. 1988). This cannot be explained in terms of different activity budgets or reduced male parental care. Males watch and remain close to females during egg laying (Hobson 1988) and feed females while they incubate (Sutherland 1987). Males assume the larger proportion of feeding duties by feeding young more per trip and more often (Biermann & Sealy 1982). In addition, timing of model testing could not have produced this effect since we conducted trials randomly throughout the day, and Biermann &Sealy (1982) found in this population

518 Animal Behaviour, 38, 3

tha t t ime of day had no effect on the feeding rate of adul t yellow warblers t h r o u g h o u t the nesting cycle.

H o b s o n et al. (1988) suggested several possible explanat ions for low-level nest defence by male yellow warblers. These included the possibility tha t females have greater confidence of pa ren thood than their mates and are thus willing to take more risk in defending offspring. Alternatively, since the activities of females are based abou t the nest, their nest-defence behav iour may be more developed. This is expected part icular ly in the case of an anti- b rood parasi te defence that involves the use of an already well-developed behav iour such as sit t ing in the nest.

A C K N O W L E D G M E N T S

We t h a n k the s ta f fand s tudents of the Universi ty of M a n i t o b a Field Sta t ion (Delta Marsh) for assisting us in various aspects of our field work. The officers of the Por tage Coun t r y Club permit ted us to conduct some of this work on their property. M. Yurkowski of the Freshwater Insti tute, Envi ron- men t Canada , Winnipeg, permit ted us to use facilities under his care to produce the freeze-dried models used in our experiments. R. K. Baydack, R. M. Evans and J. H. Gee commented on an early draf t of the manuscr ip t . We thank L. C. Drick- amer, R. L. K n i g h t and J. P icman for critically reviewing the final manuscr ipt . This study was funded by a Na tu ra l Sciences and Engineer ing Research Counci l of C a n a d a grant (A9556) to S. G. S. and pos t -gradua te scholarships f rom N S E R C and the Univers i ty of M a n i t o b a to K.A.H. This paper is con t r ibu t ion n u m b e r 180 of the Universi ty of M a n i t o b a Field Sta t ion (Delta Marsh) .

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(Received 23 May 1988; revised 21 October 1988; MS. number: A5308)