Behavioural Responses of Potential Hosts Towards Artificial Cuckoo Eggs and Dummies

Reprinted from: BEHAVIOUR 1161/21991

E.J. Brill — P.O.B. 9000 — 2300 PA Leiden The Netherlands

Behaviour 116 (1-2) 1990, E.J. Brill, Leiden

BEHAVIOURAL RESPONSES OF POTENTIAL HOSTS TOWARDS ARTIFICIAL CUCK00 EGGS AND DUMMIES

by

ARNE MOKSNES'), EIVIN RØSKAFT'), ANDERS T. BRAA'), LARS KORSNES1), HELENE M. LAMPE') and HANS CHR. PEDERSEN2) 3)

(Department of Zoology, University of Trondheim, N-7055 DragvolP , and Norwegian Institute of Nature Research, Tungasletta 2, N-7004 Trondheim2, Norway)

(With 1 Figure)

(Acc. 10-VII-1990)

Introduction

About one percent of all bird species are brood parasites, i. e. they lay

their eggs in the nest of another species, which then incubates the eggs

and broods the young of the parasite (LACK, 1968). The cuckoo Cuculuscanorus, is probably the most famous among the 80 or so known

interspecific brood parasites. In Europe, only a few species are

frequently-used cuckoo hosts. According to WYLLIE (1981), 11 host

species are parasitized frequently, and about the same number occa-

sionally. In spite of this, cuckoo eggs have been found in the nests of

more than 100 different host species, (WYLLIE, 1981). In the present

study these are the species that are defined as "potential hosts" for the

cuckoo. In Fennoscandia, the cuckoos normally start laying in late

May—early June. They lay their eggs at two day intervals, eventually

laying a distributed "clutch" of 10-15 eggs (HAARTMAN, 1981). Each

time a female cuckoo parasitizes a nest she removes one or more of the

host's eggs. Every female cuckoo lays eggs of constant type, hence her

3 ) We are indebted to E. ALSTADHEIM, T. BOLLINGMO, Y. ESPMARK, F. FALKENBERG,P. FISKE, D. KARLSEN, J. A. and V. KRØKE, H.E. LERKELUND, C. and M. MELAND, A.and Y. MOKSNES, P. OLSEN, A.C. OTHMAN, C. PEDERSEN, T.H. RINGSBY, S. SVARTAASand 0. VIE for their assistance in the field, to A. and P. OLSEN and K. SOMMERVOLD fortheir outstanding work in making the artificial cuckoo eggs, to J. SAND, who stuffed thecuckoo dummies, to M. de L. BROOKE, S.I. ROTHSTEIN and an anonymous referee forconstructive comments on an earlier draft of this paper, to P. TALLANTIRE for improvingthe English and to M. BRUMMERMANN for translating the summary into German. Thisproject was supported by the Trondheim Electricity Board and the Nedal and NansenFoundations.

RESPONSESTOWARDSARTIFICIAL CUCK00 EGGS AND DUMMIES 65

mimicry is normally only effective in regard to either a single host species

(BROOKE & DAVIES, 1988) or to a group of species that lay similarly col-

oured eggs (MOKSNEs & RØSKAFT, 1987). Groups of females that lay

similar eggs are termed "gentes" (e.g. JOURDAIN, 1925; BAKER, 1942;

LACK, 1968), and such "gentes" may show geographical patterns in their

distributions. As soon as the cuckoo egg hatches, the nestling ejects the

remaining host's eggs and any hatchlings. It is an extremely rare event

for any of the host's young to be reared in a nest containing a young

CliCk00 (WYLLIE, 198 1) .

The aim of the present study was to make a survey of the evolutionary

status achieved between the cuckoo and its hosts, with special emphasis

on the strategies adopted by different host species. Host reactions

towards cuckoo parasitism were studied by observing host species' nests

m which artificial cuckoo eggs had been placed (a method also used by

DAVIES & BROOKE, 1989a,b), and the host parents' reactions towards a

stuffed cuckoo dummy placed near the nest.

Host strategies

Because successful cuckoo parasitism reduces the host's fitness to a very

low level, evolution will favour host defence mechanisms which reduce

the probability of being parasitized. One of these mechanisms may be to

behave aggressively towards the cuckoo. Many potential host species

may be capable of preventing the parasite from laying its egg in their

nest, by behaving very aggressively towards any parasitic bird that

approach their nest, but so far there are few data available which could

support this general idea (see MOLNAR 1944; ROBERTSON & NORMAN

1976; SLACK, 1976).

The most successful stage of the breeding cycle for rejecting the

parasite seems to be at the egg stage. Many hosts of the brown-headed

cowbird Molothrus ater, for example, are capable of rejecting any cowbird

eggs laid in their nests (ROTHSTEIN , 1975, 1982). Some potential cuckoo

hosts are also known to be capable of recognizing a cuckoo egg and then

ejecting it from the nest SWYNNERTON, 1918; RENSCH 1924; ALT, 1931;

BROOKE & DAVIES, 1988; DAVIES & BROOKE 1988, 1989a; MOKSNES &

RØSKAFT, 1988; HIGUCHI , 1989). Species which are physically incapable

of ejecting the cuckoo egg may instead reject it by either deserting the

nest, or by burying the old nest and building a new one above it (WYLLIE,

1981; DAVIES &BROOKE, 1988). We have used the term rejectors for those

host species which are capable of recognizing and rejecting cuckoo eggs.

66 ARNE MOKSNES ET AL.

At the present time they are ahead of the cuckoo in the evolutionary arms

race.

An important factor in the evolution of rejection behaviour is the

"rejection costs" involved (cf. SPAW & ROHWER, 1987; DAVIES &

BROOKE, 1988; ROHWER & SPAW, 1988). Such costs may arise from

mistaken recognition of a parasite's egg. In species where the cuckoo has

evolved a mimetic egg, rejection of an "unusual" egg may result in

rejection of own eggs, because of the normal variation in egg colour

found within any clutch (DAvIEs & BROOKE, 1988). This is costly if such

mistakes lead to rejection of unparasitized clutches. In theory, considera-

tion of such rejection costs may be helpful in explaining why some host

species seem to accept the parasitic egg. At low rates of parasitism, for

example about 6% (MoKsNEs & RØSKAFT, 1987; DAVIES & BROOKE,

1988), it is perhaps not much more expensive to accept a rare case of

parasitism than to be faced with the costs of rejection (DAvIEs & BROOKE,

1989b) (especially if there is a risk for deserting unparasitized nests).

Furthermore, the selection pressure on hosts to discover the occurrence

of parasitism is probably negligible compared to the selection pressure on

the cuckoo to deceive the hosts (DAWKINs & KREBS, 1979). At these

observed low rates of parasitism, most individuals of potential hosts will

never be faced with cuckoo parasitism, and those which do may still be

capable of successfully rearing a brood in the subsequent breeding

season. The cuckoo, however, has to be successful for survival.

Among these species which accept the cuckoo's egg are the true cuckoo

hosts, i.e. species which at the present-day have fallen behind the cuckoo

in the coevolutionary arms race, although this process is still in progress.

However, most of the species in whose nests cuckoo eggs have been

found, are probably not true cuckoo hosts. This because, for many such

potential hosts, there are "physical" or "ecological" barriers which

either prevent, or counteract, such parasitism, viz. 1) a large size of nest,

eggs or nestlings of the host may prevent their successful ejection by the

young cuckoo. 2) When the cuckoo parasitises hole-nesting species, both

the actual egg-laying, the subsequent ejection of the host's eggs or young,

and of fledging by the young cuckoo is difficult. 3) The food which a

potential host brings to its young may not be suitable for rearing the

cuckoo chick. In such cases, egg-laying may be considered as a mistaken

act by the cuckoo. However, when there is shortage of host nests, the

cuckoo may find it better to take a chance with an unsuitable host than

simply to drop the egg on the ground and lose it (see also GÄRTNER,

1987). Thus, no or a negligible coevolutionary process is in progress

RESPONSES TOWARDS ARTIFICIAL CUCK00 EGGS AND DUMMIES 67

between the cuckoo and such species which we in accordance with DAVIES

& BROOKE (1989a,b) have termed unsuitable hosts. Excepting these

species, we assume that, for most of the potential host species, a coevolu-

tionary process is in progress and enough time has elapsed in which

counter-adaptations may have evolved. When the cuckoo starts parasitiz-

ing a new species, its egg is most probably a poor copy of the egg coloura-

tion of the host species. Our intention in making this study was to copy

this situation experimentally in nature. If a potential host species accepts

poor mimicry, it should also obviously be expected to accept good

mimicry and has therefore evolved no counter-adaptations towards a

cuckoo's egg. Such acceptors may either be true cuckoo hosts or are pro-

tected from parasitism by physical barriers (i.e. unsuitable hosts). In

species which reject non-mimetic eggs, further experiments are necessary

to find out if they are deceived by more sophisticated counter-adaptation

on the part of the cuckoo (e.g. better egg mimicry). These results are

presented in subsequent papers (BRAA et al., subm.; MOKSNES &

RØSKAFT, unpubl. obs.).

Bird species which have been involved in such evolutionary arms race

with the cuckoo, should also be able to recognize the potential brood

parasite as an enemy. We therefore tested the reactions of both

unsuitable hosts and rejectors/true cuckoo hosts towards a cuckoo

dummy placed near the host's nest.

Material and methods

Potential hosts and predictions.

On the basis of a general literature survey, we have assigned the potential host speciesthat were studied to one of four groups (Table 1). Groups A and B comprise the mostcommon hosts and the frequently used hosts, respectively. Group C and D are the rarelyused and the unsuitable hosts, respectively (see later). These categories are very similarto those used by DAVIES & BROOKE (1989a,b).

The meadow pipit Anthuspratensis is one of the most common hosts in Europe (CHANCE,1922; BAKER, 1942; WYLLIE, 1981). In a mountain area in Central Norway, we havefound a parasitism rate of 6.4% for this numerous breeding species (MoKsNEs &RØSKAFT, 1987).

Many species show a great variation in their importance as cuckoo hosts in differentparts of Europe. The redstart Phoenicurus phoenicurus is the most common host species inFinland (HAARTMAN, 1976, 1981; JÄRVINEN, 1984) and is also one of the most commonin the European part of the Soviet Union (MALCHEVSKY, 1960). However, this speciesseems only rarely to be parasitized in the more western parts of Europe. (e.g. GLUE &MURRAY, 1984). The dunnock Prunella modularis, in contrast, is a common host inWestern Europe, but a rare one in the eastern part (WYLLIE, 1981; GLUE & MURRAY,1984; MALCHEVSKY, 1960). The white wagtail Motacilla alba seems to be a common hostin most parts of Europe.

68 ARNE MOKSNES ET AL .

We would expect the most common hosts to show a higher degree of acceptance of non-mimetic cuckoo eggs than frequently used hosts, but the latter group should also acceptthe model eggs at a high rate. Both groups should be capable of recognizing the cuckooas a potential enemy.

We have put the rarely used and unsuitable hosts into groups C and D, respectively.Species which should be well suited as hosts, but despite this are rarely used, are put intogroup C, on the assumption that they are ahead of the cuckoo in the coevolutionary armsrace. We would expect them to reject a non-mimetic, dummy cuckoo egg and to be ableto recognize a dummy cuckoo as a potential enemy.

The species in group D are assumed to be unsuitable hosts, because their breedingbiology probably either prevents, or at least counteracts, cuckoo parasitism (see under"Host strategies"). Cuckoo eggs, for example, are very seldom found in the nests of holenesting species such as the swift Apus apus, starling Sturnus vulgaris, blue tit Parus caeruleus,great tit Parus major, marsh tit Parus palustris, pied flycatcher Ficedula hypoleuca, wheatearOenanthe oenanthe, and house sparrow Passer domesticus. Reports of parasitism in the nestsof thrushes, or of passerine species larger than thrushes, are also very rare (see Hoststrategies), although MALCHEVSKY (1960) has reported some cases of parasitism in thesong thrush Turdus philomelos in the European part of the Soviet Union (see alsoYAMAGISHI & FUJIOKA, 1986). Observations made in Norway (MOKSNES & RØSKAFT,unpubl.), indicate that it is either difficult or impossible for a young cuckoo to eject thehost's eggs from fieldfare Turdus pilaris nests. In spite of the fact that the fieldfare is verynumerous in Scandinavia, and that cuckoo eggs might now and then be expected to befound in fieldfare nests, no observations exist, to our knowledge, of a young cuckoo beingreared by this species. The redpoll Acanthis flammea and the greenfmch Chloris chloris fre-quently feed their young with seeds (PEIPONEN, 1962; NEWTON 1967, 1972), which maybe an unsuitable diet for a young cuckoo. We would expect the unsuitable hosts to accepta non-mimetic, dummy cuckoo egg and that they will not recognize a dummy cuckooas a potential enemy.

Egg experiments.

The fieldwork for this study was carried out in both mountain areas and lowlands in Cen-tral Norway (MoxsNEs & RØSKAFT, 1987, 1988, 1989). To collect information about thestage reached in the evolutionary struggle between the cuckoo and its potential hosts, wemade experiments in the nests of these species. The experimental procedure was anattempt to copy the behaviour of the cuckoo. We removed one of the host's eggs andadded an artificial cuckoo egg. This egg was made of hard plastic and painted to resemblethe cuckoo eggs found in meadow pipit nests in the study area (as being the most commoncuckoo host in Norway). The resemblance between the dummy and real cuckoo egg wasso good that, by visual inspection alone, an observer could not distinguish between anartificial egg and a genuine cuckoo egg. The artificial eggs were of about the same weightas the genuine ones, but were considerably more resistant to destruction because they hada thicker shell than the natural eggs. A more detailed description of these eggs is givenin MOKSNES & RØSKAFT (1988, 1989). Several authors (e.g. ROTHSTEIN, 1975, 1976;ORTEGA & CRUZ, 1988; DAVIES & BROOKE, 1989a; HfoucHI 1989) have discussed the useof model eggs in experiments from a methodological point of view. The general con-census is that the birds treat the model eggs as if they were real eggs.

In our experiments, as an example of poor mimicry, we used the kind of egg laid bythe cuckoo in meadow pipit nests for all trials with host species except the meadow pipititself. We used red-spotted white eggs (willow warbler Phylloscopus trochilus type) in thenest of that species so that there would be a contrast with the host's eggs.

The subsequent course of events in the nests was observed by making several visits,over a period of at least six days, after the experimental egg had been placed in the host


nest. If no rejection behaviour had been recorded by the sixth day, the artificial parasiticegg was considered to have been accepted. If the bird had abandoned its nest, but withoutattempting any destruction or ejection of the dummy egg, the event was defined as adesertion. If the bird had ejected, or damaged, either the artificial egg or some of its owneggs, then the event was defined as an ejection, regardless of whether it subsequentlydeserted its nest or not. Many of these birds were unsuccessful in removing the artificialcuckoo egg and subsequently deserted the nest because they had, in the progress,destroyed most of their own eggs. However, in this study we have only classified theresult of the experiments as "acceptance" or "rejection". The different types of rejectionis described in another paper (MoicsNEs et al., subm).

The experiments were made during the egglaying and incubation periods in the years1986 to 1990. During the egglaying period, the egg exchange was carried out after thebird had laid its fourth egg. However, the nests of many species (e.g. the meadow pipit)proved so difficult to find during the laying period that the experimental parasitism oftenhad to be done during the incubation period (see MOKSNES & RØSKAFT, 1989 for furtherdiscussion). The breeding period was divided into three stages: I: Laying and the firstthree days of incubation, II: Incubation from the fourth to the eighth day, III; Incubationfrom the ninth day to hatching.

When nests were first visited, the number of host eggs present was recorded. The eggswere floated (HAYs & LECROY, 1971) to determine whether they were freshly laid, or hadalready been partially incubated. By floating the eggs, or by examining the embryos thatwere collected, we were able to estimate the laying dates for most of the nests in oursample.

Cuckoo dummy experiments.

Host aggression towards the cuckoo was tested by using a stuffed cuckoo dummy placedpointing towards the nest and within 0.5 m of it. In 1986, however, the dummy wasplaced on the ground below the nest in the case of ten fieldfare nests (MOKSNEs &RØSKAFT, 1988). Simultaneously, we also played female cuckoo calls from a tape-recorder (see MOKSNES & RØSKAFT, 1989 for further descriptions). Each experimentlasted until we were sure that the parent bird(s) had become aware of the dummycuckoo's presence for at least 5 min. The behaviour of the birds during this period wasnoted from a hide some distance away. According to their reaction towards the dummy,the birds were classified as: a) showing no aggression, i.e. the host had obviously observedthe dummy, but showed no aggressive behaviour towards it, b) mobbing, i.e. the hostmobbed the dummy, usually from a distance of about 0.5-1.5 m., c) attack, i.e. the hostmade physical contact with the dummy, often pecking its back and head. Each nest wastested only once. Cuckoo dummy and egg experiments were not done in the same nestsexcept for a few cases where cuckoo dummy experiments were carried out after the resultfrom the egg experiment was clear (i.e. at least six days after the egg exchange).

Statistics.

All the statistical analyses of the data are two-tailed, except where stated otherwise.

Results

Reactions towards the dummy egg.

Most of the meadow pipits (92%) accepted the non-mimetic cuckoo egg

(Table 1). The dummy eggs were accepted by all the dunnocks, and in


TABLE 1 . Frequencies at which potential hosts accepted non-mimetic cuckoo eggs.

Acceptance Stage in breeding periodSpecies

A. Most common hosts:*Meadow pipit 22/24 92 9/10

8/9 5/5*White wagtail 0/3 0 0/3

0/0 0/0*Dunnock 15/15 100 10/10

3/3 2/2*Redstart 2) 4/5 80 2/2

0/1 1/1Total 41/47

21/25

11/13 8/8

B. Frequently used hosts:

*Tree pipit 0/1 0 0/0

0/1 0/0Yellow wagtail 1/5 20 0/4

1/1 0/0*Garden warbler 1/3 33 1/2

0/1 0/0*Spotted flycatcher 5/9 56 4/7

0/1 1/1Lapland bunting 2/2 100 2/2

0/0 0/0Total 9/20

7/15

1/4 1/1

C. Rare hosts:

*Blackcap 3/13 23 3/9

0/4 0/0*Willow warbler 1/10 10 1/8

0/2 0/0*Chiffchaff 0/6 0 0/5

0/1 0/0*Icterine warbler 2/6 33 0/4

2/2 0/0*Bluehthroat 8/17 47 1/6

1/4 6/7*Chaffinch 5/16 31 5/14

0/2 0/0*Brambling 2) 3/31 10 2/21

1/8 0/1*Yellowhammer 0/8 0 0/5

0/3 0/0*Reed bunting 1/11 9 1/5

0/5 0/1Total 23/118

13/77

4/32 6/8

D. Unsuitable hosts:

Swift 4/4 100 0/0

3/3 1/1*Swallow 2/2 100 1/1

1/1 0/0Starling 13/14 93 13/13

0/1 0/0Blue tit 12/12 100 11/11

1/1 0/0Marsh tit 3/3 100 3/3

0/0 0/0*Great tit 17/17 100 15/15

2/2 0/0Pied flycatcher 13/13 100 13/13

0/0 0/0Wheatear 4/4 100 1/1

3/3 0/0Fieldfare 30/33 91 12/15

15/15 3/3*Blackbird 0/2 0 0/1

0/0 0/1*Redwing 2) 28/43 65 21/32

3/4 4/6*Song thrush 2/10 20 1/6

0/3 1/1*Greenfinch 10/17 59 5/11

4/5 1/1*Redpoll 8/8 100 8/8

0/0 0/0House sparrow 5/5 100 5/5

0/0 0/0Total 151/187

109/135

32/38 10/13

1) DoD, 1892; MONTELL, 1917; COLLETT, 1921; ROSENIUS, 1929; OWEN, 1933;WASENIUS, 1936; BAKER, 1942; DIESSELHORST, 1955; MAKATSCH, 1955; MALCHEVSKY, 1960; LACK, 1963; BLAISE, 1965; HENNINGS, 1966; HARRISON, 1968; HAFTORN, 1971;

RESPONSESTOWARDS ARTIFICIAL CUCK00 EGGS AND DUMMIES 71

80% of the cases by the redstart. However, none of the white wagtails

accepted the dummy egg. The median acceptance rate for the most com-

mon hosts was 86% .

Among the frequently used hosts the median rate of acceptance was

33% . Interestingly enough, one garden warbler Sylvia borin and also one

spotted flycatcher Muscicapa striata, which were classified as acceptors

according to the egg experiments, both rejected the cuckoo egg following

their later presentation with the cuckoo dummy near the nest (see also

DAVIES & BROOKE, 1988; MOKSNES & RØSKAFT, 1989). The difference in

acceptance rate between the frequently used hosts (33%) and the most

common hosts (86%) was not statistically significant (Mann-Whitney U-

test, NS).

The median acceptance rate for the rare hosts was 10% , which is not

statistically significant lower than for the most common or frequently-

used hosts (Mann-Whitney U-tests, NS). However, the difference

between the most common hosts and the rare hosts was almost significant

(U = 28, p < 0.12). Among the rare hosts, the blackcap Sylvia atricapilla,willow warbler, chiff chaff Phylloscopuscollybita, chaffinch, Fringilla coelebs,brambling F. montifringilla, yellowhammer Emberiza citrinella and reed

bunting Emberiza schoeniclusshowed strong egg rejection behaviour, with

acceptance frequencies ranging from zero to 31% . However, the

bluethroat Luscinia svecicaaccepted about half of the non-mimetic cuckoo

eggs. Most instances of the acceptance of the artificial egg by the

bluethroat were found in the experiments carried out at the later stage

III in the incubation period (see below).

The median acceptance rate for the unsuitable hosts was 100% , a

value not far from that for the most common hosts (Mann-Whitney U-

test, NS). This acceptance rate was significantly different from that for

the rare hosts (Mann-Whitney U-test, U = 133, p <0.001), but not from

that for the frequently used hosts (Mann-Whitney U-test, NS). The

KVÆRNE, 1971; GLUE & MORGAN, 1972; HEATH, 1973; YOUNG, 1974; HAARTMAN, 1976,1981; SEEL & DAVIS, 1981; WYLLIE, 1981; GLUE & MURRAY, 1984; CRAMP, 1985; BROOKE& DAVIES, 1987; MOKSNES & RØSKAFT, 1987.2) Stage in breeding period not known for all nests.

The meadow pipit were given red-spotted white eggs of the willow warbler type, whileall the other species were parasitized with artificial eggs of the meadow pipit type. Thespecies are grouped according to the parasitism rates given in the literature 1). *: Speciesfor which rearing of a young cuckoo has been observed in Europe. N: Number of nests(accepted/total). Stage in the breeding period at which the experiment was carried out:I: Egg-laying period and the first three days of incubation. II: Incubation from the fourthto the eighth day. III: Incubation from the ninth day to hatching.

72 ARNE MOKSNESET AL.

TABLE 2. Host reactions towards cuckoo dummies placed near the nest.

Species

A. il/lost common hosts:

AGAT

Number of nests

M NA %AG

Meadow pipit 28 (22) 7 (2) 23 (1) 60Dunnock 0 0 7 (0) 0Redstart 0 1 (1) 1 (0) 50Total 28 (22) 8 (3) 31 (1)

B. Frequently used hosts:

Garden warbler 0 1 (1) 0 100Spotted flycatcher 4 (4) 0 2 (0) 67Lapland bunting 0 1 (1) 0 100Total 4 (4) 2 (2) 2 (0)

C. Rare hosts:

Blackcap 4 (4) 0 0 100Willow warbler 7 (4) 0 0 100Chiffchaff 2 (2) 2 0 100Icterine warbler 2 (2) 0 0 100Bluethroat 4 (2) 0 3 (0) 57Chaffinch 9 (9) 1 (1) 1 (0) 91Brambling 11 (10) 2 (2) 4 (2) 76Reed bunting 5 (2) 1 (1) 0 100Total 44 (35) 6 (4) 8 (2)

D. Unsuitable hosts:

Starling 0 0 6 (0) 0Blue tit 0 0 4 (3) 0Great tit 0 0 5 (0) 0Pied flycatcher 0 0 3 (0) 0Wheatear 1 (1) 1 (1) 1 (1) 67Fieldfare 0 0 12 (3) 0Redwing 1 1 (1) 19 (6) 10Greenfinch 0 3 (2) 3 (0) 50Total 2 (1) 5 (4) 53 (13)

AG: Aggression (AT: Attack or M: Mobbing), NA: No aggression. The number of nests where both parents were present during the experiment is shown in parentheses.

acceptance frequency for most of the species among the unsuitable hostswas 100% , or almost so. However, the non-mimetic artificial egg wasaccepted in 65% of the nests of the redwing Turdus iliacus, in 59% of thegreenfinch nests and in only 20% of the song thrush nests. The artificialegg was also rejected in the two blackbird Turdus merula nests that weretested.

The rejection rate by the bluethroat was significantly greater duringthe egg-laying period and the first three days of incubation (stage I:


TABLE 3. Reactions of the meadow pipits towards cuckoo dummies

placed near the nest

Number of adults I II III Totalat the nest AG NA AG NA AG NA AG NA

1 7 9 4 10 0 3 11 222* 15 1 5 0 4 0 24 1

Total 22 10 9 10 4 3 35 23

*: Includes 6 cases in which more than two adults were present.

I, II and III: Stages in the breeding period at which the experiments were carried out(see Table 1). AG: Aggression (attack and mobbing). NA: No aggression.

artificial egg rejected in 5 of the 6 nests) than later on in the incubation

period (stage III: rejection in only 1 of 7 nests, Fisher's exact pro-

babilities test, p <0.05). For other single species such a relationship

between stage I and later stages was not found, but this might be due to

very few observations in stage III.

Reactions towards the cuckoo dummy.

The most common hosts showed aggressive behaviour (attack or mobb-

ing) towards the dummy in about a half of all the experiments (Table 2).

However, aggression was never observed by the dunnock and only once

by the redstart, so nearly all the observations of aggressive behaviour

derive from the experiments with the meadow pipits. Meadow pipits

were more aggressive towards the cuckoo dummy early on in the

breeding cycle than later (Table 3). Aggressive behaviour was more fre-

quent during stage I (22/32) than during either stage II (9/19) or stage III

(4/7) (Table 3). This is partly due to the fact that aggression appears to

depend on whether one or both parents were present at the nest when the

cuckoo dummy was exposed. During stage I, the pipits were significantly

more aggressive when both parents were present than when only one was

at the nest (15/16 and 7/16, respectively, X2= 9.31, p <0.01). This was

also observed for stage II (both parents: 5/5, 1 parent: 4/14, Fisher's

exact probabilities test, p = 0.01) and stage III (2 parents: 4/4, 1 parent:

0/3, Fisher's exact probabilities test, p <0.05). Both parents were present

in 50% of all cases in stage I, 26% in stage II and 57% in stage III.

In the meadow pipit there was also a small tendency for greater aggres-

sion to be shown towards the dummy cuckoo early on than later even

when only one parent was present at the nest. During stage I, aggression


was shown by 7 of 16 compared to 4 of 14 during stage II (Fisher's exact

probabilities test, NS). During stage III the value was 0 for the 3

instances (I and III: Fisher's exact probabilities test, NS). When both

parents were present, the birds were in all but one case aggressive

throughout the breeding cycle.

Compared to the observations made for the most common hosts

(median aggression rate 50%), the frequently-used and the rare hosts

behaved considerably more aggressively towards the dummy, both

groupes with median values of 100% (Table 2). The difference between

the values for the most common and the rare hosts was statistically

significant (Mann-Whitney U-test, U = 23, p <0.05), while the dif-

ference between the most common and the frequently-used hosts was not

significant (Mann-Whitney U-test, U = 9, p <0.10), nor was the dif-

ference between the frequently-used and the rare hosts (Mann-Whitney

U-test, NS).Since the results of the aggression experiments were similar for the

frequently-used and the rare hosts, they were pooled in the subsequent

analyses. The rate of aggression for this combined group of hosts was

higher when both parents were present than when only one was present

at the nest during the experiment. For stages I-III of the breeding period

aggression was recorded in 45 of 47 cases when both parents were pres-

ent, compared to 11 of 19 cases when one parent was present (Table 4).

The respective separate values were 21/22 and 4/8 for stage I, 13/13 and

6/8 for stage II and 11/12 and 1/2 for stage III. The distribution of data,

however, did not allow any statistical test. We found no decrease in the

aggression rate during the breeding period.

In some of the instances when both parents behaved aggressively

towards the dummy cuckoo, one of them was seen to be more aggressive

than the other e.g. in 7 of the experiments with meadow pipits, in one

with the spotted flycatcher and in one with the chiff chaff. For those

species where sex identification was possible, the male turned out to be

the more aggressive parent (Sign-test, p <0.05, Table 5). In some of

these instances, one of the parents did not take part in the attack at all,

as was the case with one female and one male bluethroat, two female

chaffinches, one female brambling and one female reed bunting. We

noted two instances in which female bramblings were non-aggressive

until their mates appeared, whereafter both parents proceeded to attack

the dummy cuckoo.

Most of the species in the group of unsuitable hosts showed little or no

aggression towards the dummy cuckoo (Table 2). The median aggression


TABLE 4. Reactions of the frequently-used and the rarely-used hosts (pooled data) towards cuckoo dummies placed near the nest

Number of adults

Total

at the nest AG NA AG NA AG NA AG NA

1 4 4 6 2 1 1 11 8')2* 21 1 13 0 11 1 45 2

Total 25 5 19 2 12 2 56 101)

*: Includes 1 case in which more than two adults were present.1 ) Including 1 case with stage unknown.

I, II and III: Stages in the breeding cycle at which the experiments were carried out (seeTable 1). AG: Aggression (attack and mobbing). NA: No aggression.

TABLE 5. Comparison of male and female aggression towards the cuckoo dummy, as shown by the number of experiments for which observations

were made where both parents were present at the nest

The more aggressive sexSpecies Male Female

Icterine warbler 1 0Wheatear 1 0Redstart 1 0Bluethroat 1 1Chaffinch 2 0Brambling 3 0Greenfinch 1 1Reed bunting 1 0

Total 11 2

rate for this group (0%) was less than that for the most common hosts(50%) (Mann-Whitney U-test, NS) and significantly less than that forthe frequently-used hosts (100%) (Mann-Whitney U-test, U = 23.5,p <0.05), and the rare hosts (100%) (Mann-Whitney U-test, U = 63,p <0.001). However, in four experiments with the great tit, one of theparents gave alarm calls when it returned to the nest, as was alsoobserved at two of the blue tit nests when both parents were present. Thisbehaviour pattern obviously differed from all the other types of aggres-sion that we observed. It was difficult to interpret, because the reaction


c o jo 70ow

a) 50LT,0

-, Ca) 300a.)o_

0 Most Common hosts

Frequently used hosts

A Rare hosts

Unsuitable hosts

A

A AA

A a

90

10

A

• • • 0

0

10 30 50 70 90

Percentage Aggression

Fig. 1. The relationship between the values for median percentage aggression shown towards the dummy cuckoo and median percentage rejection of dummy cuckoo eggs for

each particular host species tested. (rsp = 0.72, N = 22, p <0.001).

did not seem to be directed towards the dummy cuckoo, but seemedrather to be a general state of excitement, due to the disturbance, or

perhaps to some kind of predator warning. This behaviour was thereforenot recorded as aggression towards the dummy cuckoo. At two of the titnests, this warning calls attracted several other birds, mostly chaffinches,bramblings, greenfinches and chiff chaffs.

For those species where both egg experiments and dummy cuckooexperiments were carried out, a positive correlation was found between

the degree of egg discrimination and the rate of aggression (rsp = 0.72,p <0.001, N = 22, Fig. 1). Excluding the unsuitable hosts from thisanalyses, there is still a positive correlation (rsp = 0.53, p = 0.056,N = 14). Finally, when using medians for each genus, the positive cor-relation is still significant (rsp = 0.63, p <0.05, N = 17).

Discussion

Reactions towards the dummy egg.

As predicted, the most common hosts showed a higher (but not signifi-cant) rate of acceptance of the non-mimetic cuckoo egg than thefrequently-used and the rare hosts. The meadow pipits accepted most ofthe white model eggs and rejected only 8% (2/24), which is about the


same rate as they rejected the mimetic model eggs; 5% (1/19, MOKSNES

RØSKAFT, 1989). This may seem surprising and one may ask why the

cuckoo has evolved a mimetic egg of the meadow pipit type (MoxsNEsRØSKAFT, 1989) when the meadow pipits are obviously prepared to

accept a non-mimetic egg (see also HAARTMAN, 1981). However, in

experiments where meadow pipits in addition to egg exchange were faced

with a cuckoo dummy, we have found higher rejection rates for non-mimetic than for mimetic eggs (KoRsNEs et al. unpubl.). Besides of this,

since few hosts experience a cuckoo, but every cuckoo encounters a host,

there is a stronger selection pressure on the cuckoo to deceive the host

than on the host to reveal the parasitism (DAWRINs & KREBS 1979).

Therefore one may expect to find an evolutionary stage where the cuckoo

lay a mimetic egg even if a proportion of the host population accepts non-

mimetic eggs (see KELLY, 1987). On the other hand, a selection from

other reasons than host rejection behaviour could also lead to a mimetic

egg (see HARRISON, 1968; BROOKER & BROOKER, 1989). However, the

existing data do not permit any further discussion of this problem.

The rate of rejection in Central Norway is statistically significantly

lower than that found in Britain, where 48% (28/58) of the non-mimetic

eggs were rejected (X2 = 11.7, p < 0.001) (DAvIEs & BROOKE, 1989a).

Even in Iceland, where the cuckoo is absent and the meadow pipits not

have been subject to any coevolutionary pressure, the rejection rate of

non-mimetic eggs, 19% (5/27) was greater than that found for Central

Norway (X2 = 1.11, NS) (DAVIEs & BROOKE, 1989a). In both Britain and

Iceland, the non-mimetic model eggs used were of redstart, pied wagtail

Motacilla alba yarrellii and reed warbler Acrocephalus scirpaceus types, of

which the redstart type was the one most frequently rejected in both

countries. In our study, all the non-mimetic eggs were of the white,

willow warbler type; a colour in striking contrast to that of the meadow

pipit eggs. However, it seems unlikely that usage of different types of

model eggs is responsible for the different rejection rates observed. This

conclusion is supported by the tendency that in Britain meadow pipits

also rejected mimetic model eggs at a higher rate, 22 % (6/27), than that

found in Norway, 5% (1/19) (X2 = 2.49, NS) (MoRsNEs & RØSKAFT,

1989; DAVIES & BROOKE, 1989a). However, one cannot at present

speculate about the reasons for such a difference.

The rejection rate of non-mimetic dummy eggs in the white wagtail

(3/3) was not statistically significant different from that found for the pied

wagtail in Britain (27/38) (Fisher's exact probabilities test, NS) (DAvIEs

BROOKE, 1989a).

78 ARNE MOKSNESET AL .

The dunnock accepted all the non-mimetic eggs, a result in accordance

with that for experiments made with British dunnocks (DAvIEs &

BROOKE, 1989a). The dunnock' s reactions towards the dummy egg and

also towards the dummy cuckoo are similar to those of most of the species

in the group of unsuitable hosts. It seems therefore reasonable to suggest

that in the past some ecological barrier may have prevented a coevolu-

tionary arms race between the dunnock and the cuckoo. Since DAVIES &

BROOKE (1989b) have already speculated about this, we will therefore not

pursue the problem further.

As predicted, the majority of the redstarts (4/5) accepted the non-

mimetic cuckoo egg. This seems to be in accordance with the results of

HAARTMAN (1976, 1981) and JÄIWINEN (1984). However, our data are to

few to permit a closer discussion of the hypotheses which explain redstart

behaviour towards cuckoo eggs (HAARTMAN, 1981).

As predicted, the frequently used hosts showed a higher egg rejection

rate (median 67%) than did the common hosts (14%). However, this dif-

ference was not significant. The results for the spotted flycatcher yielded

a significantly lower rejection rate for non-mimetic eggs in Norway (4/9)

than in Britain (8/9, DAVIES & BROOKE, 1989a, Fisher's exact pro-

babilities test, p < 0.05), but in Britain the spotted flycatcher accepted

mimetic model eggs at a high rate (4/5, DAVIES & BROOKE, 1989a). This

indicates that the spotted flycatcher could be a true cuckoo host.

The rare hosts rejected the non-mimetic model eggs at a higher rate

than those found for any of the other groups. Two of the species in this

group, the chaffinch and the reed bunting, were also tested with non-

mimetic model eggs in Britain (DAvIEs & BROOKE, 1989a). The rejection

rates found for both species were similar in Norway and Britain (chaf-

finch: 11/16 and 9/15, respectively, reed bunting: 10/11 and 9/9,

respectively).As predicted, most of the species in the group of unsuitable hosts

accepted the model eggs. However, there were a few exceptions. The

redwing rejected 35% (15/43), the greenfinch 41% (7/17) and the song

thrush as much as 80% (8/10) of the non-mimetic model eggs. High rates

of rejection of such eggs by thrushes have also been found in Britain

(song thrush: 24/41, blackbird: 21/34), and DAVIES & BROOKE (1989a)

have classified these species as "suitable but rare" hosts, which have

evolved their rejection behaviour in a coevolutionary arms race with the

cuckoo. In contrast, we have placed the thrush species in the group of

unsuitable hosts, because of the very few reports of parasitism and

because field observations in Norway have indicated that the young


cuckoo has great difficulty in ejecting the host eggs and in surviving in

fieldfare nests (even when ejection of a fieldfare young was observed,

MOKSNES & RØSKAFT, unpubl.). As predicted, the fieldfare did accept

the non-mimetic egg in most cases (30/33, but see also MOKSNES &

RØSKAFT, 1988), so the situation may well be that the fieldfare, which

was the largest Turdus species tested, is an unsuitable host species,

whereas the other thrush species are rejectors. Furthermore, in Britain,

both the song thrush and the blackbird accepted mimetic model eggs at

a higher rate than non-mimetic eggs (mimetic eggs: song thrush 6/7,

blackbird 17/22, DAVIES & BROOKE, 1989a). There are thus two

possibilities, 1) these thrush species are instead true cuckoo hosts. This

is unlikely, nevertheless, because if the cuckoo has evolved eggs that

mimick those of these two species, there should have been more reports

of parasitism and acceptance of such eggs. 2) These species are perhaps

"rejectors" which are ahead of the cuckoo in the coevolutionary arms

race and should be classified therefore as rare hosts. This is not very

likely either, however, because many of the rejectors are also able to rec-

ognize and reject mimetic eggs to the same degree as they do with non-

mimetic eggs (DAvIEs & BROOKE, 1989a; MOKSNES & RØSKAFT,

unpubl.). More experiments on thrushes are therefore necessary; paying

especial attention to the fate of young cuckoos hatched in their nests, but

also to their behaviour towards dummy cuckoos. The redwings, for

example, did not behave towards the dummy cuckoo like the other rejec-tors did, i.e. they were not aggressive. Song thrushes were too shy for

dummy experiments to be made in our study area. According to ROTH-

STEIN(1975), the american robin Turdus migratorius is a rejector of eggs laid

in its nest by the brown-headed cowbird. Because there are certain

indications of intraspecific parasitism among fieldfares and redwings

(HÅLAND, 1987; MOKSNES & RØSKAFT, unpubl.), it will also be necessary

to find out whether the thrush species have developed their rejection

behaviour as a response towards the eggs of conspecifics.

In Britain, in contrast to Central Norway, the greenfinch accepted all

the non-mimetic model eggs (12/12). DAVIES & BROOKE (1989a) suggest

that the explanation for this is that the greenfinch never has been faced

with a coevolutionary arms race with the cuckoo, because the greenfinch

feeds its young largely on seeds, an unsuitable food for a young cuckoo.

However, at times in Britain young cuckoos are known to have been

reared in greenfinch nests (SEEL & DAVIS, 1981). This may perhaps be

due to local variation in the abundance of insects, possibly in areas near

to woodland (NEWTON, 1972) where the foster parents are able to find a


sufficient amount of animal food to rear their young cuckoo. The diet of

nestling greenfinches in Scandinavia is not known in detail, so one can

not exclude the possibility that an arms race between the greenfinch and

the cuckoo does occur in this part of Europe.

Changes in type of reaction during the incubation period.

If a nest is parasitized late on during the host's incubation period, the

cuckoo egg may remain unhatched and therefore represents no threat to

the host. If rejection of the parasite's egg is a costly process, one would

predict that rejection rates should be higher during the egglaying and

early incubation stages than later. This has been shown to be true by

ROTHSTEIN (1976) and BURGHAM & PICMAN (1989) for cowbird hosts in

North America (see also CLARK & ROBERTSON, 1981). However, this rela-

tionship is not at all well supported among the cuckoo hosts (see e.g.DAVIES & BROOKE, 1988; 1989a). To the best of our knowledge, only the

results for the bluethroat in Central Norway provide any support for this

prediction. It may seem surprising that this was found only for the

bluethroat which probably has low rejection costs because it is a grasp

ejector (MoKsNEs et al., subm). This means that it is able to grasp the

parasite's egg as a whole and eject it without damage to its own eggs (cf.

ROHWER & SPAW, 1988). For the other single species there were too few

observations in stage III to permit any analysis of this question.

The explanation for the apparent tendency of the cuckoo's hosts to

reject the parasite's egg late on during the incubation period, unlike the

cowbird's hosts, may be that the cuckoo's egg represents a serious threat

to the host species even when laid after incubation has started. The

incubation period for the cuckoo egg is shorter (11-12 days) than for most

of the host species (12-14 days, HAFTORN, 1971; WYLLIE, 1981). Young

cuckoos are also able to eject relatively large host nestlings (MoKsNEs &

RØSKAFT, 1987). We have seen a four days-old cuckoo chick (weight

14.0 g) eject a fieldfare nestling (weight 10.0 g) from the nest (MoicsNEs

& RØSKAFT, unpubl.). Compared to small-sized passerines, such as those

in the group of the most common hosts, this means that the cuckoo chick

is able to eject host nestlings of up to at least 50% of their adult weight,

which they normally reach about 6-8 days after hatching (HoGsTAD,

1977). The critical factor for the cuckoo would thus seem to be that its

egg shall be successfully hatched. Thus, most hosts are actually safe from

the threat of parasitism by the cuckoo only during the later stages of the

incubation period.


Reactions towards the dummy cuckoo.

WYLLIE (1981) states that host aggression rarely deters cuckoos. How-

ever, many host species seem capable of recognizing the specific threat

of a brood parasite approaching their nest, whereupon they become

aggressive (ROBERTSON & NORMAN, 1977; FOLKERS, 1982 ; FOLKERS &

LOWTHER, 1985; PAYNE et al., 1985; DAVIES & BROOKE, 1988; BRISKIE &

SEALY, 1989; BURGHAM & PICMAN, 1989; MOKSNES & RØSKAFT, 1989).

If, by behaving aggressively, the hosts are able to chase the intruder away

(e.g. MOLNAR, 1944; ROBERTSON & NORMAN, 1976; SLACK, 1976; SCOTT,

1977), thus preventing the parasite from laying its egg in their nest, this

would seem to be an adaptive anti-parasite strategy. Such behaviour

seems reasonable, especially if the parasite has already located the host

nest. But if the brood parasite has not yet done so, host aggression near

the nest could be rnaladaptive, because this behaviour could give infor-

mation to the parasite about the location of the nest (SMITH et al., 1984).

In such cases a better strategy might be to remain inconspicuous, or even

to hide, as MCLEAN (1987) observed female whiteheads Mohoua albicillato do when exposed to a dummy, long-tailed cuckoo Eudynamys taitensis.However, it seems unlikely that the common cuckoo normally uses host

aggression as a guide when searching for host nests, because the hosts

may reject the cuckoo's egg more frequently once they have observed the

cuckoo at their nest (DAvIEs & BROOKE, 1988; MOKSNES & RØSKAFT,

1989; in the present study one spotted flycatcher and one garden warbler,

both of which had at first accepted a non-mimetic model egg, later

rejected it after seeing the dummy cuckoo at their nest). The cuckoo

locates most of the nests by observing the host's nest-building activities

from a hidden position e.g. in a tree (cf. WYLLIE, 1981). Egg-laying

mostly occurs in the afternoon, a time at which the hosts, during their

egg-laying period, can be least expected to be at their nest, and the

female cuckoo takes, on average, less than 10 seconds to lay its egg in the

nest (CHANCE, 1940; SEEL, 1973; WYLLIE, 1981). It would therefore seem

important for the cuckoo to lay its egg without being noticed by the

potential foster parents. Aggressive behaviour by the host species, there-

fore, would appear to involve a negligible risk of being parasitized.

Another strategy would be to prevent a parasite from laying by staying

in the nest when the parasite approaches. This behaviour has been

observed by female yellow warblers Dendroicapetechia when exposed to

cowbirds (HoEsoN & SEALY, 1989; see also BURGHAM & PICMAN, 1989).

Similar behaviour was observed in the present study at two nests of the


spotted flycatcher, where one of the parents, when it arrived, sat on the

nest and showed no aggression towards the dummy cuckoo.

The aggressive behaviour shown by the potential cuckoo hosts towards

the dummy cuckoo closely accorded with earlier observations (EDWARDs

et al. , 1949; SMITH & HOSKING, 1955), and also with the behaviour of

these species towards live cuckoos in the field (MoKsNEs & RØSKAFT,

unpubl.). EDWARDSet al. , (1949) have also reported aggressive behaviour

by the yellowhammer towards a dummy cuckoo. As predicted, the host

species assumed to have been engaged in a coevolutionary arms race with

the cuckoo, recognized the dummy cuckoo as an enemy, while those

assumed to lack this background (the unsuitable hosts) did not. How-

ever, there were some exceptions. In contrast to DAVIES & BROOKE,

(1989a), but in accordance with SMITH & HOSKING (1955), we did not

observe any aggressive behaviour by the dunnock. However, many

species were less aggressive when only one of the parents was present at

the nest when the dummy cuckoo was presented, and this was the case

in all the experiments with dunnocks.The low level of aggression found for the unsuitable hosts, compared

to the findings for the frequently-used and rare hosts, together with the

positive correlation found between the powers of egg discrimination and

aggression, indicates that we were observing specific responses to the

brood parasite. This view is supported by the observations of SMITH &

HOSKING (1955). They concluded that the cuckoo hosts were able to rec-

ognize a dummy cuckoo in a manner that enabled them to differentiate

the cuckoo from other birds like the sparrow hawk Accipiter nisus, and jay

Garrulus glandarius, and also from mammalian predators like the stoat

Mustela erminea. If the observed aggressive behaviour in the present study

had included a significant element of predator response, then the results

for the unsuitable hosts should not have differed from those for the

frequently-used and rare hosts. A predator response should also have

increased during the nesting cycle (PATTERSON et al. , 1980;

MONTGOMERIE & WEATHERHEAD, 1988; BURGHAM & PICMAN, 1989). This

did not happen (but see KNIGHT & TEMPLE, 1986). However, the

possibility of predator responses can not be entirely ruled out (see

BURGHAM & PICMAN, 1989). According to REGELMANN & CURIO (1986),

the male tends to defend the brood against predators more strongly than

the female. The stronger responses made towards the dummy cuckoo by

the male host parent than by the female, seen in the present study, may

indicate a predator response, but this behaviour may also contain an ele-

ment of status signalling (see below). The few aggressive responses


observed in the group of unsuitable hosts (wheatear, redwing and green-

finch) may include an element of predator response. However, the com-

bined results of the rate of egg rejection and of aggressive behaviour by

the greenfinch indicates that this species has perhaps been engaged in an

evolutionary arms race with the cuckoo and should therefore not have

been included in the group of unsuitable hosts.

In the view of the observed responses made by the great tit and the

blue tit, one could argue that aggressive individuals should respond to the

threat posed by a dummy of any larger-sized species when placed near

their nest. This was tested on the meadow pipit, using a dummy of the

willow grouse Lagopus lagopus (MOKSNES & RØSKAFT, 1989). In contrast

to the response made towards the dummy cuckoo, no sign of any

response towards the dummy grouse was observed (see also SMITH et al. ,1984; PAYNE et al. , 1985; MCLEAN, 1987; BURGHAM & PICMAN, 1989;

HOBSON & SEALY, 1989).

Before the responses made towards the dummy cuckoo placed in the

vicinity of the hosts' nest can be discussed in more detail, further

experiments, using dummies of a cuckoo, a predator species and a con-

trol, are necessary.

Stage in the breeding period.

Aggression towards a brood parasite may entail such costs as the danger

of being injured, or discovered, by predators. If this is so, then aggressive

behaviour should decrease towards the end of the incubation period,

because by this time the cuckoo no longer represents a serious threat. A

tendency of such a decrease was found among the meadow pipits when

only one parent was present at the nest during the experiment. A similar

behavioural pattern has been found for the red-winged blackbird Agelaiusphoeniceus, the yellow warbler and the least flycatcher Empidonax minimustowards the brown-headed cowbird (FOLKERs & LOWTER, 1985; BRISKIE

& SEALY, 1989; BURGHAM & PICMAN, 1989; HOBSON & SEALY, 1989).

One or both host parents at the nest.

A higher level of aggression was shown towards the dummy cuckoo when

both parents were present than when only one parent was present. This

may indicate that only the presence of two or more birds of the host

species ensures success in repelling a cuckoo from the nest, and thus in

preventing the parasite from laying an egg (MOLNAR, 1944).


However, these observations may also indicate that such aggressive

behaviour may also contain an element of status signalling or self-

advertisement (SLAGSVOLD, 1984). The parental investment hypothesis

(TRIVERs, 1972, 1985) predicts that the offspring will be defended less

vigorously by individuals that invest less in reproduction. Accordingly,

the female, who at least invests equally to the male (but see BREITWISCH,

1989), would normally be expected to make a stronger response towards

a brood parasite or a predator than the male. Female yellow warblers did

in fact react more strongly towards their brood parasite (BURGHAN4&

PICMAN, 1989; HOBSON & SEALY, 1989). In the present study, however,

the male turned out to be the more aggressive parent in those cases where

the sex could be determined. An explanation of these observations couldbe that an element of status signalling is involved (cf. SLAGSVOLD, 1984).

However, this needs further testing.

General conclusion.

The results of this study support the hypothesis that the differences in thedegree of response by potential host species made towards parasitism by

the cuckoo, reflect different stages in a continuous coevolutionary arms

race with the cuckoo (DAvIEs & BROOKE, 1989b). This hypothesis predicts

that when a host has evolved the power of discrimination to non-mimetic

cuckoo eggs, then the cuckoo may turn to another host species that still

accepts non-mimetic eggs, or, if this is not possible, will try to deceive

the initial host species by evolving a mimetic egg, specific for that par-

ticular gentes of cuckoos. One would therefore expect to find, as we have

found in this study, interspecific variation in the responses to cuckoo

parasitism. This may explain why some species are acceptors and some

are rejectors. This model also explains the variation in response of a par-

ticular species, for which a rejector gene may need a long time to spread

if the parasitism rate is low (KELLY, 1987; DAVIES & BROOKE, 1989b).

In theory, one can never expect the rejection rate to be 100% , because

the cuckoo will have lost out in the coevolutionary arms race well before

the host population reaches this stage.

The lack of aggression and of egg discrimination shown by most of the

unsuitable hosts, for which ecological barriers have prevented any evolu-

tionary interaction between the cuckoo and its potential hosts, indicates

that the species in the other groups have evolved their responses in the

course of a coevolutionary arms race with the cuckoo. The group of

rarely-used hosts seem to have evolved highly effective powers of


discrimination and are, at the present time, ahead of the cuckoo in theircoevolutionary arms race. However, these species also need to be testedwith mimetic model eggs.

The group of the most common hosts, which nowadays representfavorite hosts of the cuckoo, have evolved little power of discriminationtowards non-mimetic cuckoo eggs. The meadow pipit as a widelydistributed and numerous species, would seem to represent a host speciesof a great potential for the cuckoo in this part of Europe.

The results of this study clearly demonstrate the need for furtherexperiments, designed to gather further information about the

mechanisms underlying the interactions between the cuckoo and itshosts, especially for some of the species in the group of unsuitable hosts(e.g. the thrushes). There is also a need for theoretical work to lead to a

better understanding of the coevolutionary aspects of brood parasitism.

Summary

Responses of 33 potential host species towards a non-mimetic, dummy, cuckoo eggplaced in their nest were tested (N = 372). For 22 of these species, their behaviouralresponses towards a dummy cuckoo placed near their nest were also tested (N = 193). Thespecies were grouped in A) most common hosts: species which at the moment are losingout in the coevolutionary arms race with the cuckoo and which today represent favoritehosts; B) frequently-used hosts: species which at the moment are assumed to be truecuckoo hosts, but which are not so commonly used as those in group A; C) rarely-usedhosts: species which would appear to be suitable hosts, but which despite of this, arerarely used. These species are assumed to be ahead of the cuckoo in the coevolutionaryarms race; D) unsuitable hosts: species with a breeding biology which either prevents,or counteracts, cuckoo parasitism. They are therefore assumed never to have beenengaged in a coevolutionary arms race with the cuckoo.

In the most common hosts the median acceptance rate of the non-mimetic egg was86%, in the frequently-used hosts 33%, in the rarely-used hosts 10% and in theunsuitable hosts 100% . In the most common hosts the median rate of aggression showntowards the cuckoo dummy was 50%, but the most numerous species in this group, themeadow pipit, showed aggressive behaviour in 60% of the cases. The median aggressionrate both in the frequently-used hosts and the rare hosts was 100% and in the unsuitablehosts 0% . The bluethroat was the only species which accepted the non-mimetic dummyegg at a higher rate later on during the incubation period than during earlier stages. Apositive correlation was found between the power of egg discrimination and the rate ofaggression shown towards the dummy cuckoo. Such aggression was stronger when bothparents were present at the nest than when only one parent was present.

The results of this study lend support to the hypothesis that the differences in thedegree of responses by the host species towards parasitism by the cuckoo reflect differentstages in a continuous coevolutionary arms race with cuckoos.

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ZusammenfassungWir untersuchten die Reaktionen von 33 potentiellen Wirtsarten des Kuckucks auf nicht-mimetische Kunst-Kuckuckseier, die in ihre Nester gelegt wurden (N = 372). Das

Verhalten von 22 dieser Arten gegenfiber einem Kuckuck-Dummy in Nestnåhe wurdeebenfalls getestet (N = 193). Die Arten wurden in 4 Gruppen aufgeteilt: A) gewöhnlichsteWirtsarten: Arten die momentan im koevolutionåren "Wettriisten" dem Kuckuckgegenfiber im Nachteil sind und gegenwärtig zu den bevorzugten Wirten gehören; B)håufig genutzte Wirte: Arten, die zwar wahrscheinlich echte Kuckuckswirte sind, abernicht so stark frequentiert werden wie die in Gruppe A; C) kaum genutzte Wirtsarten:Arten, die zwar als Wirte geeignet zu sein scheinen, aber dennoch nur selten parasitiertwerden. Wir nehmen an, dass diese Arten dem Kuckuck im koevolutionåren Wettlaufmomentan fiberlegen sind; D) als Wirte ungeeignete Arten: Arten, deren Brutbiologieentweder den Kuckucksparasitismus verhindert oder ihm entgegenwirkt. Es wirdangenommen, dass diese Arten keinerlei koevolutionårem Wettlauf mit dem Kuckuckausgesetzt waren.

Die meisten gewöhnlichen Wirte akzeptierten die nichtmimetischen Eier mit einer mit-tleren Rate von 86% , die häufig genutzten Wirte akzeptierten 33%, die kaum genutzten10% und die ungeigneten 100% . Die mittlere Aggressionsrate der gewöhnlichsten Wirt-sarten gegenfiber dem Kuckuck-Dummy lag bei 50% , aber die zahlenmåssig stårksteArt, der Wiesenpieper, reagierte in 60% aller Teste aggressiv. Die mittlere Aggressions-rate sowohl der häufig wie auch der selten parasitierten Arten lag bei 100% , und dieder ungeeigneten Arten bei 0% . Das Blaukehlchen akzeptierte als einzige Art dienichtmimetischen Kunst-Kuckuckseier wåhrend fortgeschrittener Brutzeit in einemhöheren Grad als in der Anfangsphase. Die Häufigkeit der Eidiskriminierung und dieAggressionsrate gegenfiber dem Kuckuck-Dummy waren positiv korreliert. Das Aggres-sionsverhalten war stårker ausgeprägt wenn sich beide Eltern in Nestnähe aufhielten alswenn nur ein Partner anwesend war.

Die Ergebnisse dieser Untersuchung stützen die Hypotese, dass Unterschiede in derIntensitåt der Reaktion der Wirtsarten gegenüber Brutparasitismus die unterschiedlichenStadien eines koevolutionåren Wettlaufs mit dem Kuckuck widerspiegeln.

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Behavioural Responses of Potential Hosts Towards Artificial Cuckoo Eggs and Dummies

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