Intraspecific Nest Parasitism in the Spotless Starling Sturnus Unicolor

Bird Study (2000) 47, 285–294

Intraspecific nest parasitism in the Spotless Starling 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 to 1994. Nests were monitored regularly and three criteria were used to detect nest parasitism: the appearance of more than one egg per day during the laying period of the host; the appearance of an egg after the start of incubation; eggs with unusual shape or pigmentation. The proportion of parasitized nests in first clutches (37%) was twice that of intermediate (19%) or second (20%) clutches in colony B, whereas parasitism occurred in first (35%) and intermediate (12%) but not in second clutches in colony A. Most clutches (52–70%) were parasitized during the host’s laying period and received one parasitic egg. In 10% of the parasitized clutches in colony B, one of the host’s eggs disappeared on the day the parasitic egg was added, suggesting that the parasitic female removed this egg. Although parasitism increased clutch size significantly, it led to a decrease in host breeding success, mainly through the removal of eggs and the loss of host nestlings and the survival of parasitic chicks. Observations suggested that parasitic females were young individuals without their own nests and/or those whose breeding attempt had been disrupted while laying in their own nest.

Intraspecific nest parasitism occurs when Mediterranean,22 although its range is currently females lay eggs in the nests of conspecifics and expanding.23 do not provide any further parental care. This The possible causes of nest parasitism and reproductive strategy has been found in at least the identity of parasitic females have been 200 bird species, particularly in precocial birds examined in the European Starling. Evans10 (Anseriformes and Galliformes),1–5 but also in lists four possible categories of parasitic hole-nesting passerines such as Hirundinidae, females: (1) paired females that contest nest- Ploceidae and Sturnidae.1,6–8 Intraspecific nest boxes occupied by other pairs; (2) females parasitism has been studied in the European whose breeding attempt was disrupted just Starling Sturnus vulgaris in several localities before the start of laying or before completion including Britain,6,9,10 Russia,11 Sweden,12 of the clutch; (3) unpaired (probably young) Belgium13 and North America.14–16 In contrast, females who have copulated with a male little is known about this reproductive already mated and with a nest-site; and strategy in a close relative, the Spotless Starling (4) ‘professional’ nest parasites who distribute S. unicolor,17–21 which breeds only in the western some of their eggs around other nests either before or after laying in a nest of their own, or, *Correspondence author. at its extreme, distributing all their eggs and Email: [email protected] not making nests of their own. Romagnano

© 2000 British Trust for Ornithology 286 J.M. Calvo et al. et al.15 identified two categories of parasite: (1) a consecutive days. The ground below and female that already has a nest, but loses it to around nestboxes was searched for broken or competitors, or a paired or unpaired female whole discarded eggs. that never successfully occupies a nest; (2) a Three conventional criteria10,16 were used to female that is parasitic at the same time that she detect parasitic eggs:1 (1) the appearance of raises a clutch of her own. Power16 simplified more than one egg/day before the host the categorization of parasites by presenting completed its clutch, as birds normally lay no evidence that most parasitism is by females more than one egg per day;25,26 (2) the appear- without nests of their own, possibly mostly ance of eggs in a nest after the host had yearlings. completed its clutch; and (3) the appearance of We present data on the occurrence of intra- eggs within a clutch with different size, shape, specific nest parasitism in two double-brooded colour or pigmentation. populations of Spotless Starlings breeding Clutches were assigned to three laying in central Spain and we examine the conse- periods based on the date of clutch initia- quences of parasitism for both the parasite and tion.13,15,17 These were first clutches (1st), the host. initiated in April; intermediate clutches (I), initiated in May and second clutches (2nd), initiated in June. First clutches were always laid STUDY AREA AND METHODS highly synchronously and second clutches The study was carried out in two breeding were initiated after the young from the first colonies situated in the province of Salamanca clutches had fledged. Intermediate clutches are (west-central Spain). Colony A (40°20′N, broods that were laid in the period between 6°35′W) was in a forest of deciduous oak laying the first and second broods.27 Quercus pyrenaica, whereas colony B (40°52′N, Parasitic eggs were separated into those laid 5°48′W) was in a more open forest land- during the host’s laying period, which are scape dominated by evergreen oak Q. ilex. likely to hatch and produce fledglings, and Intraspecific nest parasitism was studied in those laid after the host’s laying period, which nests built in boxes during 1991 in colony are less likely to hatch. A and from 1992 through 1994 in colony B. Parasitic eggs laid before the host clutch was Wooden nestboxes, measuring 170 × 280 × initiated28 (Table 8), that were usually immedi- 200 mm with a circular entrance 52 mm in ately ejected by the hosts, and parasitic eggs diameter, were firmly attached to trees 15–45 m found during the nestling stage (eight in colony apart. Colony A had 85 nestboxes in a single A, and 13, 26 and 7 for 1992, 1993 and 1994, large plot. Colony B consisted of a total of respectively, in colony B), were not included in 140–185 nestboxes in five plots (maximum the analyses because they did not hatch and distance between adjacent plots was 6 km). therefore did not influence the breeding perfor- Intraspecific nest parasitism was identified mance of the host. throughout the breeding season by frequently Hatchlings from parasitic eggs laid in the inspecting nestboxes from early April to early nest during the host’s laying period were indis- July. In 1991 and 1992, nests were checked daily tinguishable from the host’s own hatchlings, as during laying and incubation and every 1–3 Spotless Starling eggs hatched synchronously. days during nestling stage. In 1993 and 1994, We estimated fledging success of these hatch- nests were visited as in the previous two years lings (i.e. no. of fledglings/no. of hatchlings) in in one plot of colony B, whereas in the other every nest that contained one of these parasitic four plots, nests were inspected every 2–3 days nestlings. Nestlings from parasitized eggs laid during laying and incubation. Nests were after the host’s laying period, which hatched visited mainly between 08:00 hours and 12:00 asynchronously, were identified individually hours, solar GMT, to maximize detection of with paint on their toenails. This permitted parasitic eggs and avoid nest abandonment.24 determination of their survival or death during Eggs were numbered with indelible ink when the nestling period. first detected to allow identification of parasitic All statistical methods used can be found in eggs. Clutches were considered complete when Sokal & Rohlf.29 All chi-squared analyses were no new eggs appeared in the nest for two performed on numerical data.

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

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

A 1991 110 18 (35.3) 3 (12.0) 0 (0) 21 (19.1) P < 0.001 12 11 B 1992 282 29 (29.6) 21 (18.4) 12 (17.1) 62 (21.9) ns 45 22 B 1993 309 48 (39.3) 18 (18.4) 19 (21.6) 85 (27.5) P < 0.001 68 27 B 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 clutches by 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.

RESULTS Frequency and success of parasitic eggs Frequency of nest parasitism The frequency of parasitic eggs by colony, year In colony A, 19.1% of nests were parasitized. and laying stage is shown in Table 2. In colony More parasitism was detected in first clutches B, parasitism frequency was 69.7% during (35.3%) than intermediate clutches (12%), and laying and 30.3% during incubation, whereas no parasitism was observed in second clutches in colony A similar proportions of parasitic (Table 1). Unlike colony A, parasitism was eggs were laid during laying (52%) and incuba- found at each laying stage in colony B. The tion (48%). Colonies A and B, however, did overall frequency of parasitism in colony B not differ significantly in the proportion of (25.3%, data from all three years combined) of parasitic eggs laid during the laying period the first clutches (36.8%) was approximately of the host (χ2 = 3.00, df = 1, P = 0.083). twice that of both intermediate (18.8%) and Most parasitic eggs laid during the host’s second (20.5%) clutches. laying period hatched, both in colony A (83.3%) In colony B, the frequency of parasitism in and in colony B (60.1%) (Fig. 1), and the differ- first and second clutches increased from year ence between colonies was not significant to year (Table 1) but the interannual differ- (χ2 = 2.562; df = 1). In contrast, hatching success ences were not significant (χ2 test; first clutches, of parasitic eggs laid during incubation χ2 = 3.75, df = 2, ns; second clutches, χ2 = 1.39, was significantly greater in colony A (63.6%) df = 2, ns). compared with colony B (28.0%) (χ2 = 5.548;

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

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

A 1991 518 19 (7.9) 4 (3.4) 0 (0) 23 (4.4) P < 0.001 12 11 B 1992 122 839 (9.1) 27 (5.3) 14 (4.7) 80 (6.5) P < 0.05 56 24 B 1993 138 163 (10.9) 22 (5.0) 20 (5.4) 105 (7.6) P < 0.001 75 30 B 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, number and 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 laying periods.

a b 5 16

14 4 12

3 10 8

2 6

4 1 2

0 0 1 2 3 4 5 1 2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 1 2 3 4 5 6 7 8 9 10 Laying period Incubation period Laying period Incubation period

c d 20 20 18 18

Number of parasitic eggs 16 16 14 14 12 12 10 10 8 8 6 6 4 4 2 2 0 0 1 2 3 4 5 6 1 2 3 4 5 6 7 8 9 1011 1 2 3 4 5 6 1 2 3 4 5 6 7 8 9 1011 Laying period Incubation period Laying period Incubation period Time (days) Time (days)

BSFigure 99/37 1. Time Fig of laying 1 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 Redrawperiod: day 1, date of first egg laying. Incubation period: day 1, day following clutch completion.

df = 1; P < 0.05). Whereas in colony A hatching during incubation was 44.2% (19/43), which is success did not differ between parasitic eggs significantly lower than that of non-parasitized added during the laying or incubation stages nests (χ2 = 78.433; df = 1; P < 0.001). Overall, 2 (χ Yates = 0.359; df = 1; ns), in colony B, the likeli- hatching success was higher for parasitic hood of hatching was higher for parasitic eggs laid during the laying stage of the host eggs added during the laying stage of the host (χ2 = 26.561; df = 1; P < 0.001). (χ2 = 21.768; df = 1; P < 0.001). Pooling the It was not possible to determine the success results of both colonies, in nests where eggs of parasitic eggs laid during the host’s laying hatched, there were no significant differences stage, because all eggs within these clutches between the hatching success of parasitic eggs usually hatched synchronously and nestlings laid during the laying stage of the host (90.7%; from parasitic eggs could not be identified indi- 117/129) and that of eggs in non-parasitized vidually. Despite this, in nests where eggs nests (92.8%; 1856/2000) (χ2 = 0.789; df = 1). In hatched and for the pooled results of both contrast, hatching success of parasitic eggs laid colonies, we estimated the fledging success of

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

No. of No. of eggs Total no. of parasitic eggs producing Breeding Colony Year parasitic eggs hatched (%) fledglings success (%)

A 1991 10 6 (60.0)2 20.0 B 1992 15 7 (46.7)1 6.7 B 1993 14 5 (37.7)1 7.1 B 1994 4 1 (25.0)0 0.0 B 1992–94 33 13 (39.4) 2 6.1 these eggs to be 45.5%, with no significant was detected and ascribed to parasitic females. differences between the fledging success of Egg removal was not detected in colony A and parasitic eggs and of eggs in non-parasitized had a low incidence in colony B (Table 6). Egg nests (44.4%) (χ2 = 0.055; df = 1). However, the removal occurred in both parasitized (six of 62) success for nestlings from parasitic eggs added and non-parasitized (seven of 220) nests, during incubation that hatched after the rest of although it was more frequent in the former the clutch was significantly lower (9.3%) than (χ2 = 4.64; df = 1; P = 0.03). that of non-parasitized nests (χ2 = 27.897; df = 1; The number of eggs hatched was higher in P < 0.001) (Table 3). Moreover, the fledging parasitized nests, but the number of fledglings success of all parasitic eggs was 33.4%, signifi- and the overall breeding success did not differ cantly lower than that of non-parasitized nests significantly between parasitized and non- (χ2 = 7.721; df = 1; P < 0.01). parasitized nests (Table 5).

Effect of nest parasitism on the host Identity of parasitic females The most frequent number of parasitic eggs per No parasitic female was observed while laying. nest was one, but two eggs (colony A) or up to However, two cases, involving females in their four eggs (colony B) were found in some nests first reproductive year were related to conspe- (Table 4). Clutch size was significantly higher cific parasitism. The two birds were captured in in parasitized than in non-parasitized nests colony A in an empty nestbox trap shaped as a (Table 5). The fact that parasitized nests aver- regular nestbox30 at 09:30 and 13:00 hours, solar aged 1.0 (colony A) or 1.1 (colony B) eggs more GMT. The host Spotless Starling females lay than non-parasitized nests and that most para- eggs early in the morning,31 whereas Feare et al.24 sitized nests (> 72%) had only one parasitic egg, determined that parasitic females of European suggests that parasitism did not reduce the Starling tended to lay in other individuals’ number of eggs laid by the host female. nests later, around mid-morning, after the However, parasitism did reduce the clutch size morning laying of host females. Both birds were of the host in some nests, where egg removal captured while nearby nests were in the laying

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)

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 Breeding Colony 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 73.6 B 1992 NO 196 4.15 ± 0.72 3.77 ± 0.89 2.29 ± 1.45 54.6 *** *** ns ns PA 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 35.5 B 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. stage and both had a full-grown egg in the cloacal Another source of parasites might be females area ready for laying. A likely explanation for whose first nests have failed during the laying catching females ready to lay in an empty nest stage and who may complete their clutches in is that they were parasitic females attempting other females’ nests. If this is so, the frequency to leave the egg in another female‘s nest. of parasitism should be related to the frequency If a shortage of suitable nest-sites leads to of nest failures. This was the case in colony B, conspecific parasitism, then a positive correla- where nest parasitism increased with an tion should exist between the frequency of increase in nest failures in unparasitized nests parasitism and nestbox occupancy. However, (Table 8). The frequency of parasitism was our data do not support this hypothesis, as the always approximately three times higher than parasitism frequency among first clutches was the rate of nest failure. not related to the proportion of nestboxes containing complete clutches (Spearman’s DISCUSSION correlation test: rs = –0.50; n = 4; ns; data from 1992–94 for colony B). Indeed, the year with the Altogether, 25% of Spotless Starlings’ nests were lowest nestbox occupancy (1994) had the parasitized during the laying or incubation highest parasitism frequency (Table 7). stages of the host. Using similar methodology,

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

No. (%) of No. (%) of No. (%) of clutches with Laying Total no. parasitized clutches with parasitism and period 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)

Table 7. Number (%) of available nestboxes containing distinguishable on the basis of size, shape complete clutches (nestbox occupancy) and number (%) and colour.10,14 This also appears to be the case of parasitized nests in the first laying period. n, Total in the Spotless Starling,17 as parasitic eggs were number of nestboxes. easily recognized. However, as inter- and intra- Occupied Parasitized clutch variation in egg form has not been Colony Year n nestboxes clutches analysed in detail in the Spotless Starling, we cannot rule out the possibility that some A 1991 85 58 (68.2) 18 (31.0) parasitic eggs were missed. Therefore, the B 1992 165 110 (66.6) 29 (26.4) percentages of nest parasitism in the Spotless B 1993 185 139 (75.1) 48 (34.5) Starling presented here should be considered B 1994 140 66 (47.1) 25 (37.9) conservative, taking into account the differences found in the European Starling when conventional or laboratory techniques were other authors found similar frequencies of used. parasitized nests in Spotless Starlings breeding The rate of parasitism in Spotless Starlings in in Corsica (19–33%)18,19 and Portugal (24%).21 this study was significantly higher in first These frequencies of nest parasitism for the clutches than in intermediate or second clutches. Spotless Starling are higher than those found Indeed, initiation of these clutches was highly in the European Starling in studies that also synchronous and more young were fledged employed conventional methods: 11–15%.13–15 than from intermediate or late clutches. However, estimates based upon laboratory Evans,10 Romagnano et al.15 and Pinxten et al.13 techniques, such as electrophoresis and post- also found that first clutches in European ovulatory follicle analyses, increased the Starling were highly synchronous and experi- frequency of parasitism in the European enced the highest frequencies of parasitism, Starling to values of 20–23%.10,15,32,33 Thus, as in our study. Yom-Tov37 suggested that conventional methods may underestimate the synchronous breeding reduces nest parasitism: true frequency of brood parasitism, particular- the more synchronous a population, the less ly by using the third criterion employed by us chance of being parasitized. Alternatively, (i.e. eggs within a clutch with unusual pigmen- given the relatively small anti-parasite advan- tation, size or shape) because some eggs may tage,38 synchrony may simply have reflected a go unnoticed.10,16,33,34 Nevertheless, conven- common response to environmental condi- tional methods can be as sensitive as laboratory tions.39 On the other hand, there were techniques in some populations, as shown differences between colonies in the frequency by Romagnano et al.34 As inter-clutch variation of parasitism throughout the breeding season, is considerably greater than intra-clutch as parasitism occurred in all three laying stages variation in the European Starling,35,36 eggs in colony B whereas no parasitism occurred laid by different females in the same nest are among second clutches in colony A. Such

Table 8. Number (%) of nest failures in non-parasitized incomplete clutches, of complete parasitized clutches, and of unoccupied 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 nestboxes Year period clutches clutches receiving 1 egg

1992 1st 8 (10.8) 31 (29.5) 7 Intermed. 7 (7.1) 22 (18.2) 9 2nd 4 (6.3) 12 (16.0) 2 Total 19 (8.0) 65 (21.6) 18 1992–94 1st 3 (9.4) 12 (27.3) 5 Intermed. 3 (7.0) 14 (24.5) 5 2nd 2 (6.1) 9 (21.4) 0 Total 8 (7.4) 35 (24.5) 10

© 2000 British Trust for Ornithology, Bird Study, 47, 285–294 292 J.M. Calvo et al. differences have also been observed in the offspring fledged in some parasitized nests European Starling. In some populations para- includes parasite and non-parasite nestlings. It sitism was restricted to first and intermediate suggests a different kind of reproductive cost clutches13 while in others it occurred on clutches for the parents, related to the loss of their laid over the entire breeding season.10,14,15 genetic offspring and the survival of young Intraspecific nest parasitism is an advanta- from parasitic eggs. geous reproductive strategy for parasites if Parasitism also affected the host in those their eggs produce fledglings. In order to parasitized nests in which the parasite removed increase egg success, the best laying time for one or more host eggs. The percentage of the parasite is during the host’s laying period, parasitized nests with egg removal found in as eggs laid during the incubation stage have the European Starling (27–34%)13,14 is notably less chance of hatching. Renard & Verheyen19 higher than in the Spotless Starling in our study and Power16 concluded that intraspecific nest (10% in colony B, 0% in colony A). The low parasitism does not seem to be a very efficient incidence of egg removal in the Spotless reproductive strategy in starlings because: Starling here and elsewhere (7%),18 shows that (1) only 36% (Spotless Starling) and 49% parasitism in this species involves an increase (European Starling) of the parasitic eggs were in the total number of eggs per parasitized nest added during the laying period of the host and without generally affecting the clutch size of (2) parasitic eggs laid during the incubation the host. Yamaguchi & Saitou8 observed in stage never produced fledglings. In this study, Grey Starling S. cineraceus that host eggs were 68% of parasitic eggs were laid during the never removed. This finding, with the circum- host’s laying stage, of which 62% hatched syn- stance that the parasite females did not always chronously with the rest of the clutch; select the most successful time for parasitism moreover, 9% of the eggs laid during incuba- (parasitic eggs appeared before laying period tion also produced fledglings. Nevertheless, of the host, during the incubation and even in 65–95% of the parasitic eggs in our colonies nest with hatchlings), led these authors to were unsuccessful, indicating that, overall, conclude that the Grey Starling is not special- parasitism resulted in a low breeding success. ized in parasitism and that intraspecific nest These results indicate a strong selection for parasitism has not evolved very far. Evans10 parasitic females to lay synchronously with suggested that intraspecific nest parasitism the host. However, our results suggested that may be the first stage towards the evolution of parasitic females were probably less successful interspecific nest parasitism. at producing fledglings than they would be if What factors affect the frequency of conspe- they could raise their own clutch. But if for cific nest parasitism in Spotless Starling, and some reason they cannot, intraspecific nest which females were responsible for laying the parasitism is better than nothing. This was also parasitic eggs in our colonies? Karlsson12 and demonstrated by Evans,10 Romagnano et al.15 Evans10 found that the parasitism rate was and Pinxten et al.13 positively correlated with nestbox occupancy, What are the consequences of being para- concluding that nest-site availability deter- sitized? We found that in about half of the mined the incidence of nest parasitism in parasitized nests the parasitic eggs hatched European Starlings. We found that parasitism and, consequently, hosts had to rear one extra frequency was relatively high in most years, nestling. As the survival of nestlings is and not positively correlated with the propor- probably inversely related to brood size in tion of nestboxes containing first clutches. Starlings,40,41 the addition of one hatchling may These findings indicate that a shortage of reduce the number of host’s offspring fledged suitable nest-sites is not a critical selective because of increased competition. In our study, pressure explaining nest parasitism in the mean clutch size and eggs hatched were signif- Spotless Starling. As in the present study, icantly higher in parasitized nests. Moreover, Romagnano et al.15 and Pinxten et al.13 found young fledged and breeding success did not that the parasitism rate among first clutches differ between parasitized and non-parasitized was highest when the fewest nestboxes nests. Then, as a parasite nestling fledged in at contained first clutches. This suggests that nest least a third of parasitized nests, the number of parasitism in starlings is a reproductive strategy

© 2000 British Trust for Ornithology, Bird Study, 47, 285–294 Intraspecific nest parasitism 293 used by some females even when there is a ACKNOWLEDGEMENTS surplus of good nest-sites. In the European Starling, Evans10 found that This study was funded by CICYT (project parasitism was positively correlated to deser- AGR91-0662) and Junta de Castilla y León tion rate of unparasitized nests in first clutches. (Ayudas a la investigación) of Spain. J.A. Pinxten et al.13 observed a marked female Pascual was supported by a predoctoral fellow- dumping an egg in the clutch of a neighbouring ship from the Ministerio de Educación y nest after deserting her own nest due to distur- Ciencia (Spain). We thank S. Lehman for help in bance shortly before clutch initiation. Like the fieldwork, and Rosma and ‘Billy’, owners of the European Starling, we found that the incidence ‘Torrecilla’ ranch, for giving permission to of nest parasitism in Spotless Starlings increased work on their estate property. The manuscript with an increase in the proportion of nest was greatly improved by the suggestions of failures among first clutches. Although these S.G. Sealy and an anonymous referee. results suggest that females deserting or losing their nest before completing the clutch might REFERENCES be an important source of parasites, their contribution to the overall rate of parasitism in 1. Yom-Tov, Y. (1980) Intraspecific nest parasitism in our colonies remains unknown. For instance, it birds. Biol. Rev., 55, 93–108. is not known whether such females keep laying 2. Rohwer, F.C. & Freeman, S. (1989) The distribution of eggs for several days after being disrupted and conspecific nest parasitism in birds. Can. J. Zool., 67, whether they distribute their parasitic eggs 239–253. between one or more nests. In some nests, the 3. MacWhirter, R.B. (1989) On the rarity of intraspecific first-laid egg disappeared the following day brood parasitism. Condor, 91, 485–492. (Table 8) and a new clutch was initiated a few 4. Sorenson, M.D. (1992) Comment: Why is conspecific nest parasitism more frequent in waterfowl than other days later in the same nest. These first eggs birds? Can. J. Zool., 70, 1856–1858. may have been parasitic eggs that were added 5. Bjorn, T.H. & Erikstad, K.E. (1994) Patterns of prior to the onset of laying by the host female intraspecific nest parasitism in the High Arctic com- and were removed by the host to avoid para- mon eider Somateria mollisima borealis. Can. J. 28 sitism. These eggs may have been deposited Zool., 72, 1027–1034. by females that lost or deserted partially com- 6. Yom-Tov, Y., Dunnet, G.M. & Anderson, A. (1974) pleted clutches, depositing the remaining egg(s) Intraspecific nest parasitism in the Starling Sturnus in the nest of a conspecific or dumping them in vulgaris. Ibis, 116, 87–90. empty nestboxes, as observed by Hamilton & 7. Anderson, M. (1984) Brood parasitism within species. Orians,42 Yom-Tov1 and Pinxten et al.13 In Producers and Scroungers: Strategies of Exploita- Evans,10 Romagnano et al.15 and Power16 tion and Parasitism (ed. C.J. Barnard), pp. 195–227. suggested that some parasitic European Croom Helm, London. Starlings might be unmated (generally young) 8. Yamaguchi, Y. & Saitou, T. (1997) Intraspecific nest females without their own nests, fertilized by a parasitism in the Grey Starling Sturnus cineraceus. paired or unpaired male. As polygyny and Ecol. Res., 12, 211–221. extra-pair fertilizations were observed in 9. Feare, C.J. (1984) The Starling. Oxford University Spotless Starlings in colony B,27,31 this implies Press, Oxford. that unpaired females could have copulated 10. Evans, P.G.H. (1988) Intraspecific nest parasitism in with paired or unpaired males and become the European Starling Sturnus vulgaris. Anim. parasitic. Two yearling females caught in a Behav., 36, 1282–1294. nestbox trap with an egg ready to be laid might 11. Numerov, A.D. (1978) Cases of abnormal egg laying by starlings Sturnus vulgaris L. Proc. Oka State be females in this category. Reserve, 14, 356–357. The information presented here suggests that 12. Karlsson, J. (1983) Breeding of the starling. PhD intraspecific nest parasitism in the Spotless Thesis, University of Lund, Sweden. Starling is an opportunistic, phenotypically 13. Pinxten, R., Eens, M. & Verheyen, R.F. (1991) Con- flexible strategy, used by females when a specific nest parasitism in the European Starling. previous breeding attempt has been disrupted Ardea, 79, 15–30. or when they have no access to suitable 14. Lombardo, M.P., Power, H.W., Stouffer, P.C., Romag- nest-sites. nano, L.C. & Hoffenberg, A.S. (1989) Eggs removal

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