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Intraspecific nest parasitism in the Spotless StarlingSturnus unicolorJ.M. Calvo , J.A. Pascual , B. deceuninck & S.J. PerisPublished online: 29 Mar 2010.

To cite this article: J.M. Calvo , J.A. Pascual , B. deceuninck & S.J. Peris (2000) Intraspecific nest parasitism in the SpotlessStarling Sturnus unicolor , Bird Study, 47:3, 285-294, DOI: 10.1080/00063650009461188

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© 2000 British Trust for Ornithology

Intraspecific nest parasitism occurs whenfemales lay eggs in the nests of conspecifics anddo not provide any further parental care. Thisreproductive strategy has been found in at least200 bird species, particularly in precocial birds(Anseriformes and Galliformes),1�5 but also inhole-nesting passerines such as Hirundinidae,Ploceidae and Sturnidae.1,6�8 Intraspecific nestparasitism has been studied in the EuropeanStarling Sturnus vulgaris in several localitiesincluding Britain,6,9,10 Russia,11 Sweden,12

Belgium13 and North America.14�16 In contrast,little is known about this reproductive strategy in a close relative, the Spotless StarlingS. unicolor,17�21 which breeds only in the western

Mediterranean,22 although its range is currentlyexpanding.23

The possible causes of nest parasitism andthe identity of parasitic females have beenexamined in the European Starling. Evans10

lists four possible categories of parasiticfemales: (1) paired females that contest nest-boxes occupied by other pairs; (2) femaleswhose breeding attempt was disrupted justbefore the start of laying or before completionof the clutch; (3) unpaired (probably young)females who have copulated with a malealready mated and with a nest-site; and (4) �professional� nest parasites who distributesome of their eggs around other nests eitherbefore or after laying in a nest of their own, or,at its extreme, distributing all their eggs andnot making nests of their own. Romagnano

Bird Study (2000) 47, 285–294

Intraspecific nest parasitism in the SpotlessStarling Sturnus unicolor

JESUS M. CALVO1, JUAN A. PASCUAL2, BERNARD DECEUNINCK3 and SALVADOR J. PERIS1*1Departamento de Biología Animal-Zoología, Facultad de Biología, Universidad de Salamanca,

37071 Salamanca, Spain, 2Rhone-Poulenc Agro, BP 153, 06903 Sophia Antipolis Cédex, France and 3Ligue Française pour la Protection des Oiseaux/BirdLife France, La Corderie Royale, BP 263, F-17305

Rochefort Cédex, France

Intraspecific nest parasitism in two colonies of Spotless Starling Sturnus unicolor breeding in nestboxes was studied in central Spain from 1991 to1994. Nests were monitored regularly and three criteria were used to detectnest parasitism: the appearance of more than one egg per day during the layingperiod of the host; the appearance of an egg after the start of incubation; eggswith unusual shape or pigmentation. The proportion of parasitized nests in firstclutches (37%) was twice that of intermediate (19%) or second (20%) clutchesin colony B, whereas parasitism occurred in first (35%) and intermediate(12%) but not in second clutches in colony A. Most clutches (52�70%) wereparasitized during the host�s laying period and received one parasitic egg. In10% of the parasitized clutches in colony B, one of the host�s eggs disappearedon the day the parasitic egg was added, suggesting that the parasitic femaleremoved this egg. Although parasitism increased clutch size significantly, it ledto a decrease in host breeding success, mainly through the removal of eggs andthe loss of host nestlings and the survival of parasitic chicks. Observations suggested that parasitic females were young individuals without their ownnests and/or those whose breeding attempt had been disrupted while laying intheir own nest.

*Correspondence author.Email: peris@gugu.usal.es

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et al.15 identified two categories of parasite: (1) afemale that already has a nest, but loses it tocompetitors, or a paired or unpaired femalethat never successfully occupies a nest; (2) afemale that is parasitic at the same time that sheraises a clutch of her own. Power16 simplifiedthe categorization of parasites by presentingevidence that most parasitism is by femaleswithout nests of their own, possibly mostlyyearlings.

We present data on the occurrence of intra-specific nest parasitism in two double-broodedpopulations of Spotless Starlings breeding in central Spain and we examine the conse-quences of parasitism for both the parasite andthe host.

STUDY AREA AND METHODS

The study was carried out in two breedingcolonies situated in the province of Salamanca(west-central Spain). Colony A (40°20′N,6°35′W) was in a forest of deciduous oakQuercus pyrenaica, whereas colony B (40°52′N,5°48′W) was in a more open forest land-scape dominated by evergreen oak Q. ilex.Intraspecific nest parasitism was studied innests built in boxes during 1991 in colony A and from 1992 through 1994 in colony B.Wooden nestboxes, measuring 170 × 280 ×200 mm with a circular entrance 52 mm indiameter, were firmly attached to trees 15�45 mapart. Colony A had 85 nestboxes in a singlelarge plot. Colony B consisted of a total of140�185 nestboxes in five plots (maximum distance between adjacent plots was 6 km).

Intraspecific nest parasitism was identifiedthroughout the breeding season by frequentlyinspecting nestboxes from early April to earlyJuly. In 1991 and 1992, nests were checked dailyduring laying and incubation and every 1�3days during nestling stage. In 1993 and 1994,nests were visited as in the previous two yearsin one plot of colony B, whereas in the otherfour plots, nests were inspected every 2�3 daysduring laying and incubation. Nests were visited mainly between 08:00 hours and 12:00hours, solar GMT, to maximize detection ofparasitic eggs and avoid nest abandonment.24

Eggs were numbered with indelible ink whenfirst detected to allow identification of parasiticeggs. Clutches were considered complete whenno new eggs appeared in the nest for two

consecutive days. The ground below andaround nestboxes was searched for broken orwhole discarded eggs.

Three conventional criteria10,16 were used todetect parasitic eggs:1 (1) the appearance ofmore than one egg/day before the host completed its clutch, as birds normally lay nomore than one egg per day;25,26 (2) the appear-ance of eggs in a nest after the host hadcompleted its clutch; and (3) the appearance ofeggs within a clutch with different size, shape,colour or pigmentation.

Clutches were assigned to three laying periods based on the date of clutch initia-tion.13,15,17 These were first clutches (1st),initiated in April; intermediate clutches (I), ini-tiated in May and second clutches (2nd),initiated in June. First clutches were always laidhighly synchronously and second clutcheswere initiated after the young from the firstclutches had fledged. Intermediate clutches arebroods that were laid in the period betweenlaying the first and second broods.27

Parasitic eggs were separated into those laidduring the host�s laying period, which are likely to hatch and produce fledglings, andthose laid after the host�s laying period, whichare less likely to hatch.

Parasitic eggs laid before the host clutch wasinitiated28 (Table 8), that were usually immedi-ately ejected by the hosts, and parasitic eggsfound during the nestling stage (eight in colonyA, and 13, 26 and 7 for 1992, 1993 and 1994,respectively, in colony B), were not included inthe analyses because they did not hatch andtherefore did not influence the breeding perfor-mance of the host.

Hatchlings from parasitic eggs laid in thenest during the host�s laying period were indis-tinguishable from the host�s own hatchlings, asSpotless Starling eggs hatched synchronously.We estimated fledging success of these hatch-lings (i.e. no. of fledglings/no. of hatchlings) inevery nest that contained one of these parasiticnestlings. Nestlings from parasitized eggs laidafter the host�s laying period, which hatchedasynchronously, were identified individuallywith paint on their toenails. This permitteddetermination of their survival or death duringthe nestling period.

All statistical methods used can be found inSokal & Rohlf.29 All chi-squared analyses wereperformed on numerical data.

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Intraspecific nest parasitism 287

RESULTS

Frequency of nest parasitism

In colony A, 19.1% of nests were parasitized.More parasitism was detected in first clutches(35.3%) than intermediate clutches (12%), andno parasitism was observed in second clutches(Table 1). Unlike colony A, parasitism wasfound at each laying stage in colony B. Theoverall frequency of parasitism in colony B(25.3%, data from all three years combined) ofthe first clutches (36.8%) was approximatelytwice that of both intermediate (18.8%) and second (20.5%) clutches.

In colony B, the frequency of parasitism infirst and second clutches increased from year to year (Table 1) but the interannual differ-ences were not significant (χ2 test; first clutches,χ2 = 3.75, df = 2, ns; second clutches, χ2 = 1.39, df = 2, ns).

Frequency and success of parasitic eggs

The frequency of parasitic eggs by colony, yearand laying stage is shown in Table 2. In colonyB, parasitism frequency was 69.7% during laying and 30.3% during incubation, whereasin colony A similar proportions of parasiticeggs were laid during laying (52%) and incuba-tion (48%). Colonies A and B, however, did not differ significantly in the proportion of parasitic eggs laid during the laying period of the host (χ2 = 3.00, df = 1, P = 0.083).

Most parasitic eggs laid during the host�slaying period hatched, both in colony A (83.3%)and in colony B (60.1%) (Fig. 1), and the differ-ence between colonies was not significant (χ2 = 2.562; df = 1). In contrast, hatching successof parasitic eggs laid during incubation was significantly greater in colony A (63.6%)compared with colony B (28.0%) (χ2 = 5.548;

Table 1. Number (%) of parasitized clutches by colony, year and laying period.

Np

Colony Year NT 1st Intermed. 2nd Total Testa PL PI

A 1991 110 18 (35.3) 3 (12.0) 0 (0) 21 (19.1) P < 0.001 12 11B 1992 282 29 (29.6) 21 (18.4) 12 (17.1) 62 (21.9) ns 45 22B 1993 309 48 (39.3) 18 (18.4) 19 (21.6) 85 (27.5) P < 0.001 68 27B 1994 218 25 (43.8) 29 (19.6) 4 (30.7) 58 (26.6) P < 0.001 41 23

NT, Total number of complete clutches over entire breeding season; Np, number and percentage of parasitized clutchesby laying period (1st, intermediate and 2nd) and totals of parasitized clutches for each year – totals differ from the addition of PL and PI because some clutches were parasitized during both the laying and incubation stages; PL, number of clutches parasitized during the laying stage of the host; PI, number of clutches parasitized during the incubation stage of the host. aResults of G-tests comparing the frequency of nests parasitized during each of three laying periods.

Table 2. Number (%) of parasitic eggs by colony, year and laying period.

Ep

Colony Year ET 1st Intermed. 2nd Total Testa PL PI

A 1991 518 19 (7.9) 4 (3.4) 0 (0) 23 (4.4) P < 0.001 12 11B 1992 122 839 (9.1) 27 (5.3) 14 (4.7) 80 (6.5) P < 0.05 56 24B 1993 138 163 (10.9) 22 (5.0) 20 (5.4) 105 (7.6) P < 0.001 75 30B 1994 946 35 (13.9) 40 (6.1) 4 (8.8) 79 (8.3) P < 0.001 53 26

ET, total number of parasitic and non-parasitic eggs laid in complete clutches over entire breeding season; Ep, numberand percentage of parasitic eggs by laying period (1st, intermediate and 2nd) and totals of parasitic eggs for each year;PL, number of parasitic eggs laid during the laying stage of the host; PI, number of parasitic eggs laid during the incubation stage of the host. aResults of G-tests comparing the frequency of parasitic eggs during each of three layingperiods.

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df = 1; P < 0.05). Whereas in colony A hatchingsuccess did not differ between parasitic eggsadded during the laying or incubation stages(χ2

Yates = 0.359; df = 1; ns), in colony B, the likeli-hood of hatching was higher for parasitic eggs added during the laying stage of the host(χ2 = 21.768; df = 1; P < 0.001). Pooling theresults of both colonies, in nests where eggshatched, there were no significant differencesbetween the hatching success of parasitic eggslaid during the laying stage of the host (90.7%;117/129) and that of eggs in non-parasitizednests (92.8%; 1856/2000) (χ2 = 0.789; df = 1). Incontrast, hatching success of parasitic eggs laid

during incubation was 44.2% (19/43), which issignificantly lower than that of non-parasitizednests (χ2 = 78.433; df = 1; P < 0.001). Overall,hatching success was higher for parasitic eggs laid during the laying stage of the host (χ2 = 26.561; df = 1; P < 0.001).

It was not possible to determine the successof parasitic eggs laid during the host�s layingstage, because all eggs within these clutchesusually hatched synchronously and nestlingsfrom parasitic eggs could not be identified indi-vidually. Despite this, in nests where eggshatched and for the pooled results of bothcolonies, we estimated the fledging success of

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Figure 1. Time of laying and hatching success of parasitic eggs in relation to the stage of laying or incubation of host.(a) Colony A 1991; (b) colony B 1992; (c) colony B 1993; (d) colony B 1994. ■ , Hatched; ■■ , not hatched. Laying period: day 1, date of first egg laying. Incubation period: day 1, day following clutch completion.

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Intraspecific nest parasitism 289

these eggs to be 45.5%, with no significant differences between the fledging success of parasitic eggs and of eggs in non-parasitizednests (44.4%) (χ2 = 0.055; df = 1). However, thesuccess for nestlings from parasitic eggs addedduring incubation that hatched after the rest ofthe clutch was significantly lower (9.3%) thanthat of non-parasitized nests (χ2 = 27.897; df = 1;P < 0.001) (Table 3). Moreover, the fledging success of all parasitic eggs was 33.4%, signifi-cantly lower than that of non-parasitized nests(χ2 = 7.721; df = 1; P < 0.01).

Effect of nest parasitism on the host

The most frequent number of parasitic eggs pernest was one, but two eggs (colony A) or up tofour eggs (colony B) were found in some nests(Table 4). Clutch size was significantly higherin parasitized than in non-parasitized nests(Table 5). The fact that parasitized nests aver-aged 1.0 (colony A) or 1.1 (colony B) eggs morethan non-parasitized nests and that most para-sitized nests (> 72%) had only one parasitic egg,suggests that parasitism did not reduce thenumber of eggs laid by the host female.However, parasitism did reduce the clutch sizeof the host in some nests, where egg removal

was detected and ascribed to parasitic females.Egg removal was not detected in colony A andhad a low incidence in colony B (Table 6). Eggremoval occurred in both parasitized (six of 62)and non-parasitized (seven of 220) nests,although it was more frequent in the former (χ2 = 4.64; df = 1; P = 0.03).

The number of eggs hatched was higher inparasitized nests, but the number of fledglingsand the overall breeding success did not differsignificantly between parasitized and non-parasitized nests (Table 5).

Identity of parasitic females

No parasitic female was observed while laying.However, two cases, involving females in theirfirst reproductive year were related to conspe-cific parasitism. The two birds were captured incolony A in an empty nestbox trap shaped as aregular nestbox30 at 09:30 and 13:00 hours, solarGMT. The host Spotless Starling females layeggs early in the morning,31 whereas Feare et al.24

determined that parasitic females of EuropeanStarling tended to lay in other individuals�nests later, around mid-morning, after themorning laying of host females. Both birds werecaptured while nearby nests were in the laying

Table 3. Breeding success of parasitic eggs laid during the incubation of the host. Only nests with at least one fledglinghave been included.

No. of No. of eggsTotal no. of parasitic eggs producing Breeding

Colony Year parasitic eggs hatched (%) fledglings success (%)

A 1991 10 6 (60.0) 2 20.0B 1992 15 7 (46.7) 1 6.7B 1993 14 5 (37.7) 1 7.1B 1994 4 1 (25.0) 0 0.0B 1992–94 33 13 (39.4) 2 6.1

Table 4. Frequency of parasitic eggs found per clutch.

No. (%) of parasitic eggs/nest

Colony Year 1 2 3 4

A 1991 19 (90.5) 2 (9.5) 0 (0) 0 (0)B 1992 51 (82.2) 6 (9.7) 3 (4.8) 2 (3.2)B 1993 71 (83.5) 9 (10.6) 4 (4.7) 1 (1.2)B 1994 42 (72.4) 12 (20.7) 3 (5.2) 1 (1.7)B 1992–94 164 (80.0) 27 (13.2) 10 (4.9) 4 (1.9)

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stage and both had a full-grown egg in the cloacalarea ready for laying. A likely explanation forcatching females ready to lay in an empty nestis that they were parasitic females attemptingto leave the egg in another female�s nest.

If a shortage of suitable nest-sites leads toconspecific parasitism, then a positive correla-tion should exist between the frequency ofparasitism and nestbox occupancy. However,our data do not support this hypothesis, as theparasitism frequency among first clutches wasnot related to the proportion of nestboxes containing complete clutches (Spearman�s correlation test: rs = �0.50; n = 4; ns; data from1992�94 for colony B). Indeed, the year with thelowest nestbox occupancy (1994) had the highest parasitism frequency (Table 7).

Another source of parasites might be femaleswhose first nests have failed during the layingstage and who may complete their clutches inother females� nests. If this is so, the frequencyof parasitism should be related to the frequencyof nest failures. This was the case in colony B,where nest parasitism increased with anincrease in nest failures in unparasitized nests(Table 8). The frequency of parasitism wasalways approximately three times higher thanthe rate of nest failure.

DISCUSSION

Altogether, 25% of Spotless Starlings� nests wereparasitized during the laying or incubationstages of the host. Using similar methodology,

Table 5. Breeding success (mean ± sd) of non-parasitized (NO) and parasitized (PA) clutches where eggs hatched. n, Number of clutches. Differences between non-parasitized and parasitized nests were tested using Mann–Whitney U-tests for clutch size, number of eggs hatched and number of young fledged, and with G-tests with the Yate’s correc-tion for breeding success.

Clutch No. of eggs No. of young BreedingColony Year Type n size hatched fledged success (%)

A 1991 NO 40 4.50 ± 0.82 4.37 ± 0.87 3.30 ± 1.60 73.3*** *** ns ns

PA 20 5.50 ± 0.69 5.20 ± 0.69 4.05 ± 1.32 73.6B 1992 NO 196 4.15 ± 0.72 3.77 ± 0.89 2.29 ± 1.45 54.6

*** *** ns nsPA 56 5.20 ± 1.07 4.48 ± 1.14 2.66 ± 1.73 51.2

B 1993 NO 156 4.24 ± 0.67 3.97 ± 0.82 1.29 ± 1.48 30.4*** *** ** ns

PA 56 5.32 ± 1.06 4.57 ± 1.09 1.89 ± 1.45 35.5B 1994 NO 82 4.21 ± 0.71 3.94 ± 0.86 1.29 ± 1.59 30.6

*** ** ns **PA 23 5.26 ± 1.32 4.74 ± 1.29 0.87 ± 1.39 16.5

B 1992–94 NO 434 4.19 ± 0.70 3.87 ± 0.86 1.74 ± 1.56 41.5*** *** ns ns

PA 135 5.25 ± 1.10 4.56 ± 1.14 2.03 ± 1.67 38.6

Breeding success was calculated as the percentage of eggs that produced fledglings.*P < 0.05; **P < 0.01; ***P < 0.001.

Table 6. Intraspecific nest parasitism and egg removal in colony B in 1992.

No. (%) ofNo. (%) of No. (%) of clutches with

Laying Total no. parasitized clutches with parasitism andperiod of clutches clutches egg removal egg removal

1st 98 29 (29.6) 3 (3.1) 2 (6.9)Intermediate 114 21 (18.4) 6 (5.3) 2 (9.5)2nd 70 12 (17.1) 4 (5.7) 2 (16.6)Total year 282 62 (22.0) 13 (4.6) 6 (9.7)

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other authors found similar frequencies of parasitized nests in Spotless Starlings breedingin Corsica (19�33%)18,19 and Portugal (24%).21

These frequencies of nest parasitism for theSpotless Starling are higher than those found in the European Starling in studies that alsoemployed conventional methods: 11�15%.13�15

However, estimates based upon laboratorytechniques, such as electrophoresis and post-ovulatory follicle analyses, increased thefrequency of parasitism in the EuropeanStarling to values of 20�23%.10,15,32,33 Thus, conventional methods may underestimate thetrue frequency of brood parasitism, particular-ly by using the third criterion employed by us(i.e. eggs within a clutch with unusual pigmen-tation, size or shape) because some eggs maygo unnoticed.10,16,33,34 Nevertheless, conven-tional methods can be as sensitive as laboratory techniques in some populations, as shown by Romagnano et al.34 As inter-clutch variationis considerably greater than intra-clutch variation in the European Starling,35,36 eggs laid by different females in the same nest are

distinguishable on the basis of size, shape and colour.10,14 This also appears to be the casein the Spotless Starling,17 as parasitic eggs wereeasily recognized. However, as inter- and intra-clutch variation in egg form has not beenanalysed in detail in the Spotless Starling, we cannot rule out the possibility that someparasitic eggs were missed. Therefore, the percentages of nest parasitism in the SpotlessStarling presented here should be consideredconservative, taking into account the differ-ences found in the European Starling whenconventional or laboratory techniques wereused.

The rate of parasitism in Spotless Starlings inthis study was significantly higher in firstclutches than in intermediate or second clutches.Indeed, initiation of these clutches was highlysynchronous and more young were fledgedthan from intermediate or late clutches.Evans,10 Romagnano et al.15 and Pinxten et al.13

also found that first clutches in EuropeanStarling were highly synchronous and experi-enced the highest frequencies of parasitism, as in our study. Yom-Tov37 suggested that synchronous breeding reduces nest parasitism:the more synchronous a population, the lesschance of being parasitized. Alternatively,given the relatively small anti-parasite advan-tage,38 synchrony may simply have reflected acommon response to environmental condi-tions.39 On the other hand, there weredifferences between colonies in the frequencyof parasitism throughout the breeding season,as parasitism occurred in all three laying stagesin colony B whereas no parasitism occurredamong second clutches in colony A. Such

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Intraspecific nest parasitism 291

Table 7. Number (%) of available nestboxes containingcomplete clutches (nestbox occupancy) and number (%)of parasitized nests in the first laying period. n, Total number of nestboxes.

Occupied ParasitizedColony Year n nestboxes clutches

A 1991 85 58 (68.2) 18 (31.0)B 1992 165 110 (66.6) 29 (26.4)B 1993 185 139 (75.1) 48 (34.5)B 1994 140 66 (47.1) 25 (37.9)

Table 8. Number (%) of nest failures in non-parasitized incomplete clutches, of complete parasitized clutches, and ofunoccupied nestboxes receiving one egg, in colony B, in all plots in 1992 and in plot 5 in 1992–94.

No. (%) of nest failures in non-parasitized Complete Unoccupied

Laying incomplete parasitized nestboxesYear period clutches clutches receiving 1 egg

1992 1st 8 (10.8) 31 (29.5) 7Intermed. 7 (7.1) 22 (18.2) 9

2nd 4 (6.3) 12 (16.0) 2Total 19 (8.0) 65 (21.6) 18

1992–94 1st 3 (9.4) 12 (27.3) 5Intermed. 3 (7.0) 14 (24.5) 5

2nd 2 (6.1) 9 (21.4) 0Total 8 (7.4) 35 (24.5) 10

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differences have also been observed in theEuropean Starling. In some populations para-sitism was restricted to first and intermediateclutches13 while in others it occurred on clutcheslaid over the entire breeding season.10,14,15

Intraspecific nest parasitism is an advanta-geous reproductive strategy for parasites iftheir eggs produce fledglings. In order toincrease egg success, the best laying time forthe parasite is during the host�s laying period,as eggs laid during the incubation stage haveless chance of hatching. Renard & Verheyen19

and Power16 concluded that intraspecific nestparasitism does not seem to be a very efficientreproductive strategy in starlings because: (1) only 36% (Spotless Starling) and 49%(European Starling) of the parasitic eggs wereadded during the laying period of the host and(2) parasitic eggs laid during the incubationstage never produced fledglings. In this study,68% of parasitic eggs were laid during thehost�s laying stage, of which 62% hatched syn-chronously with the rest of the clutch;moreover, 9% of the eggs laid during incuba-tion also produced fledglings. Nevertheless,65�95% of the parasitic eggs in our colonieswere unsuccessful, indicating that, overall, parasitism resulted in a low breeding success.These results indicate a strong selection for parasitic females to lay synchronously with the host. However, our results suggested thatparasitic females were probably less successfulat producing fledglings than they would be ifthey could raise their own clutch. But if forsome reason they cannot, intraspecific nest parasitism is better than nothing. This was alsodemonstrated by Evans,10 Romagnano et al.15

and Pinxten et al.13

What are the consequences of being para-sitized? We found that in about half of theparasitized nests the parasitic eggs hatchedand, consequently, hosts had to rear one extranestling. As the survival of nestlings is probably inversely related to brood size inStarlings,40,41 the addition of one hatchling mayreduce the number of host�s offspring fledgedbecause of increased competition. In our study,mean clutch size and eggs hatched were signif-icantly higher in parasitized nests. Moreover,young fledged and breeding success did notdiffer between parasitized and non-parasitizednests. Then, as a parasite nestling fledged in atleast a third of parasitized nests, the number of

offspring fledged in some parasitized nestsincludes parasite and non-parasite nestlings. Itsuggests a different kind of reproductive costfor the parents, related to the loss of their genetic offspring and the survival of youngfrom parasitic eggs.

Parasitism also affected the host in those parasitized nests in which the parasite removedone or more host eggs. The percentage of parasitized nests with egg removal found in the European Starling (27�34%)13,14 is notablyhigher than in the Spotless Starling in our study(10% in colony B, 0% in colony A). The low incidence of egg removal in the SpotlessStarling here and elsewhere (7%),18 shows thatparasitism in this species involves an increasein the total number of eggs per parasitized nestwithout generally affecting the clutch size ofthe host. Yamaguchi & Saitou8 observed inGrey Starling S. cineraceus that host eggs werenever removed. This finding, with the circum-stance that the parasite females did not alwaysselect the most successful time for parasitism(parasitic eggs appeared before laying periodof the host, during the incubation and even innest with hatchlings), led these authors to conclude that the Grey Starling is not special-ized in parasitism and that intraspecific nestparasitism has not evolved very far. Evans10

suggested that intraspecific nest parasitismmay be the first stage towards the evolution ofinterspecific nest parasitism.

What factors affect the frequency of conspe-cific nest parasitism in Spotless Starling, andwhich females were responsible for laying theparasitic eggs in our colonies? Karlsson12 andEvans10 found that the parasitism rate was positively correlated with nestbox occupancy,concluding that nest-site availability deter-mined the incidence of nest parasitism inEuropean Starlings. We found that parasitismfrequency was relatively high in most years,and not positively correlated with the propor-tion of nestboxes containing first clutches.These findings indicate that a shortage of suitable nest-sites is not a critical selective pressure explaining nest parasitism in theSpotless Starling. As in the present study,Romagnano et al.15 and Pinxten et al.13 foundthat the parasitism rate among first clutcheswas highest when the fewest nestboxes contained first clutches. This suggests that nestparasitism in starlings is a reproductive strategy

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Intraspecific nest parasitism 293

used by some females even when there is a surplus of good nest-sites.

In the European Starling, Evans10 found thatparasitism was positively correlated to deser-tion rate of unparasitized nests in first clutches.Pinxten et al.13 observed a marked femaledumping an egg in the clutch of a neighbouringnest after deserting her own nest due to distur-bance shortly before clutch initiation. Like theEuropean Starling, we found that the incidenceof nest parasitism in Spotless Starlings increasedwith an increase in the proportion of nest failures among first clutches. Although theseresults suggest that females deserting or losingtheir nest before completing the clutch mightbe an important source of parasites, their contribution to the overall rate of parasitism inour colonies remains unknown. For instance, itis not known whether such females keep layingeggs for several days after being disrupted andwhether they distribute their parasitic eggsbetween one or more nests. In some nests, thefirst-laid egg disappeared the following day(Table 8) and a new clutch was initiated a fewdays later in the same nest. These first eggsmay have been parasitic eggs that were addedprior to the onset of laying by the host femaleand were removed by the host to avoid para-sitism.28 These eggs may have been depositedby females that lost or deserted partially com-pleted clutches, depositing the remaining egg(s)in the nest of a conspecific or dumping them inempty nestboxes, as observed by Hamilton &Orians,42 Yom-Tov1 and Pinxten et al.13

Evans,10 Romagnano et al.15 and Power16

suggested that some parasitic EuropeanStarlings might be unmated (generally young)females without their own nests, fertilized by apaired or unpaired male. As polygyny andextra-pair fertilizations were observed inSpotless Starlings in colony B,27,31 this impliesthat unpaired females could have copulatedwith paired or unpaired males and become parasitic. Two yearling females caught in anestbox trap with an egg ready to be laid mightbe females in this category.

The information presented here suggests thatintraspecific nest parasitism in the SpotlessStarling is an opportunistic, phenotypicallyflexible strategy, used by females when a previous breeding attempt has been disruptedor when they have no access to suitable nest-sites.

ACKNOWLEDGEMENTS

This study was funded by CICYT (projectAGR91-0662) and Junta de Castilla y León(Ayudas a la investigación) of Spain. J.A.Pascual was supported by a predoctoral fellow-ship from the Ministerio de Educación yCiencia (Spain). We thank S. Lehman for help infieldwork, and Rosma and �Billy�, owners of the�Torrecilla� ranch, for giving permission towork on their estate property. The manuscriptwas greatly improved by the suggestions ofS.G. Sealy and an anonymous referee.

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(MS received 26 July 1999; revised MS accepted 14 March 2000)

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