No Brood Parasitism by the Great Spotted Cuckoo Clamator Glandarius on the Azure-Winged Magpie Cyanopica Cyanus

Bird Study (2005) 52, 204–209

No brood parasitism by the Great Spotted Cuckoo Clamator glandarius on the Azure-winged Magpie Cyanopica cyanus

JULIANA VALENCIA1*, CARLOS DE LA CRUZ2, JUAN CARRANZA1 and ELENA SOLÍS2 1Unidad de Biología y Etología, Facultad de Veterinaria, Universidad de Extremadura, 10071 Cáceres, Spain and 2Area de Biología Animal, Facultad de Ciencias, Universidad de Extremadura, 06071 Badajoz, Spain

Capsule No case of parasitic interaction was found after 12 years of intensive monitoring of a marked population in Spain where both species are sympatric. Aims To evaluate whether the Azure-winged Magpie is parasitized, and suggest possible causes that affect its relationship with the Great Spotted Cuckoo. Methods Data from a long-term field study of marked individuals in a population of Azure-winged Magpie in Spain, were collected from about 60 nests per year over 12 years. Results Although common in the area, no eggs or young of the Great Spotted Cuckoo were found in an Azure-winged Magpie nest. Conclusion The Great Spotted Cuckoo does not appear to parasitize the Azure-winged Magpie, and we suggest that elevated predation rates on nests may be an important, overlooked factor potentially affecting the choice of host species by this brood parasite.

Avian interspecific brood parasites lay their eggs in the Magpie and only occasionally parasitize the nests of other species. Parasite species differ in the Carrion Crow Corvus corone (Cramp 1985, Soler 1990, degree of specialization when selecting host species, Arias de Reyna 1998). The Jackdaw Corvus monedula, and some parasites progressively add new host species Red-billed Chough Pyrhocorax pyrhocorax and Raven as their ranges expand (Payne 1997, Rothstein & Corvus corax, have also been reported as occasional Robinson 1998). The suitability of a particular host hosts (Soler 1990, see Arias de Reyna 1998). Another depends on a suite of life history characteristics that corvid, the Azure-winged Magpie Cyanopica cyanus, interact during the co-evolutionary history with the has been reported as a possible host of the Great parasite, including egg rejection and egg mimicry Spotted Cuckoo (Cramp 1985, Arias de Reyna 1998). (Davies & Brooke 1988, Rothstein 1990). Adaptations The Azure-winged Magpie in the Iberian Peninsula achieved after the co-evolution with a particular host inhabits open woodlands and dehesas with Holm Oak species probably preadapt the parasite species to Quercus ilex and Cork Oak Q. suber as dominating parasitize related species with similar life histories species (Araujo 1975, Saez-Royuela 1980), as well as (Rothstein & Robinson 1998). in areas with pine Pinus spp., olive Olea europaea or The Great Spotted Cuckoo Clamator glandarius is a chestnut Castanea sativa trees (Mountfort 1958). The brood parasite that occurs in four disjunct populations distributions of Azure-winged Magpie and Magpie in in Africa and the Mediterranean basin (Cramp 1985, southwestern Iberia widely overlap; they use the same Fry et al. 1988). The number of host species in Africa habitats and nest in the same tree species, breed at the ranges from 16 in southern Africa, including the same time, have similar body sizes (Azure-winged Sturnidae and Corvidae, to a few corvid species in Magpie is only 25% smaller) and eat similar foods Central Africa and one main host in the Mediterranean during their breeding seasons (Cramp & Perrins 1994). basin, the Magpie Pica pica (Cramp 1985, Arias de Experimental studies have shown that the Azure- Reyna 1998). The well-studied populations of Great winged Magpie meets the conditions of an appropriate Spotted Cuckoo on the Iberian Peninsula specialize on host for the Great Spotted Cuckoo. For example, Great Spotted Cuckoo chicks experimentally introduced into *Correspondence author. Email: [email protected] Azure-winged Magpie nests fledged as successfully as

those introduced into Magpie nests (Redondo & Arias our study area has been confirmed by observation of de Reyna 1989). Most remarkably, Friedmann (1964) individuals and the sound of calls in every study year, and Soler et al. (2003) reported the presence of Great together with observations of parasitized Magpie nests. Spotted Cuckoo eggs in Azure-winged Magpie clutches We monitored nests for 12 years, from 1984 to 1986 preserved in museums that originated from several sites and from 1995 to 2003. Fieldwork extended from late in Iberia (including Badajoz province, near our study March to early July each year, to include the whole area). However, if parasitism does occur, it is surprising breeding period of Azure-winged Magpie in our study that no field study has confirmed the existence of area (Cruz 1988, Valencia et al. 2000). Nests were parasitism in current populations. found by inspecting every tree in the area from the We use data from a long-term study conducted since beginning of the breeding period. The entire area was 1984 on the reproductive biology and behaviour of an searched repeatedly so that every tree was visited at Azure-winged Magpie population where the Great least once a week. Areas with more Azure-winged Spotted Cuckoo occurs in sympatry. Here we analyse Magpie activity were surveyed more frequently. Once the information registered over years of field study, with discovered, the content of each nest was inspected detailed monitoring of many nests, to determine every two days. Eggs were individually numbered as whether the Azure-winged Magpie is currently being they were laid so that the addition or loss of any egg was parasitized by the Great Spotted Cuckoo, and to discuss recorded at each inspection. Nests were inspected until the likely causes that may be at work on the basis of our after hatching with the same periodicity until the knowledge on the reproductive biology of this species. chicks were 14 days old, when the chicks are likely to jump out of the nest.

METHODS The study area is located in Badajoz province, 22 km RESULTS north of Badajoz (southwest Spain, 39°03′N, 6°48′W), Laying by Azure-winged Magpies took place in the at the centre of the distribution area of this species in study area between April and June, with some varia- Iberia (Sacarrao 1967, 1972). The study area is also tions between years, so that first egg-laying occurred within the breeding distribution of the Great Spotted during 64.3 ± 8.3 days every year (Fig. 1). During the Cuckoo (Cramp 1985). The presence of the cuckoo in 12 breeding seasons, 690 nests (average 57.5 ± 25.2 per

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Figure 1. Laying phenology of Azure-winged Magpie in the years of study. Bars show the period when the first egg was laid in the monitored nests.

120

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Number of nests 40

0 1984 1985 1986 1995 1996 1997 1998 1999 2000 2001 2002 2003

Figure 2. Number of nests monitored with eggs () and chicks () in the years of study. year) were monitored; new eggs were marked and any have been laid and immediately ejected by one of the change of eggs or chicks was recorded every two pair. This possibility is unlikely, however, because the days (Fig. 2). Despite this monitoring effort and the Azure-winged Magpie reportedly takes several days to availability for more than two months every year of eject cuckoo eggs (average 3.6 days and 8.3 days in two suitable nests for laying brood parasites, we did not find populations reported by Arias de Reyna 1998). Avilés any foreign eggs in the nests. As female Azure-winged (2004) has recently investigated egg rejection by Magpies lay one egg every day, even a mimetic extra Azure-winged Magpie in a colony only 60 km from our egg should also have been detected, but this did study colony. Habitat features and the presence of not happen. Even in the case of an overlooked egg, Azure-winged Magpies are homogeneous throughout monitoring of nests after hatching would have revealed the area between the two colonies, and there are the presence of any brood parasites. A total of 414 nests no barriers that would suggest a long period of (34.5 ± 22.01 per year) out of the 690 monitored reproductive isolation between populations. Avilés hatched and we did not find a foreign chick in any of (2004) experimentally parasitized 24 Azure-winged them (Fig. 2). Thus, our data allow us to rule out the Magpie nests. Five of them were predated. Out of the occurrence of either inter- or intraspecific brood remaining 19, in no case was the parasite egg ejected in parasitism in the species in our study area. the first day after placement; 73.7% (14) were finally ejected, and ejection events occurred between days 3 and 6 from experimental release (Avilés 2004). In the DISCUSSION area where Avilés undertook the experiments, there Our data show that the breeding phenology of the were also Magpies that were parasitized by the Great Azure-winged Magpie is compatible with the laying Spotted Cuckoo, and he found no case of parasitism by phenology of the Great Spotted Cuckoo (Cramp 1985, the Great Spotted Cuckoo on the Azure-winged Cramp & Perrins 1994). It is similar to that of the Magpie. These results strongly indicate that early Magpie, which is the main host species of the Great ejection of parasite eggs can be discarded as a likely Spotted Cuckoo in Iberia (Cramp & Perrins 1994, cause for the observed lack of parasitism. Arias de Reyna 1998, Soler et al. 1999), but despite a Another possibility is that a mimetic egg is laid at the high number of monitored nests over a long period, end of the laying sequence and then the clutch size is brood parasitism was absent in our study area. regarded as n + 1 instead of n. Finally, the parasite may It is unlikely that foreign eggs could have been have damaged one host egg when she laid, which may present without being detected, but several possibilities have been removed by the breeding pair, as occasion- deserve consideration. One is that a foreign egg could ally is reported for magpie clutches parasitized by the

Great Spotted Cuckoo (Soler et al. 1997). If the (Lotem 1993, Redondo 1993). We have evidence that removed egg was already marked we would have Azure-winged Magpies readily accept chicks from noticed it, so it could only happen if the last-laid, neighbouring nests even when they are of different sizes unmarked egg was removed just before we inspected (Cruz et al. unpubl. data), and Redondo & Arias de the nest, which is unlikely for the reasons discussed Reyna (1989) showed that Great Spotted Cuckoo above. Moreover, had the addition of the cuckoo egg chicks introduced into nests of Azure-winged Magpie been overlooked, it would have been detected when fledged. Thus, evidence from our study area and from the parasite hatched. the existing literature strongly suggests that if the Great We also know that during three additional years in Spotted Cuckoo parasitized Azure-winged Magpie our study area (1992–94), the intensive study by nests, they would be accepted and the chicks reared. González (1996) also failed to find evidence of foreign If the Azure-winged Magpie is a good potential host eggs or chicks in the Azure-winged Magpie nests she for the Great Spotted Cuckoo, then why is parasitism studied. Therefore, taking account of that study too, we so rare? In Iberia, the Great Spotted Cuckoo prefers the are confident that brood parasitism has not occurred on Magpie as a host species, and it is successful with this our study area over 15 years of research. relationship (Arias de Reyna 1998, Soler & Soler These results contrast with the reports (Friedmann 2000). However, it is not highly specialized, and selects 1964, Soler et al. 2003) of Great Spotted Cuckoo eggs hosts among the corvids and other species such as the in 19th century Azure-winged Magpie clutches Hoopoe Upupa epops (Cramp 1985) or the African Pied preserved in museums. We know that the procedures Starling Spreo bicolor (Payne 1997). Data from African used then for collecting clutches were not reliable. For populations indicate that when the Great Spotted instance, local people were paid to collect clutches Cuckoo has been present somewhere for a long time, with parasite eggs so we cannot exclude the possibility the number of host species used tends to increase that fraudulent material was accepted. Nevertheless, (Friedmann 1948, Cramp 1985). New host species because clutches reported by Friedmann (1964) and are successively incorporated, presumably as older Soler et al. (2003) originated from different localities in hosts become less available or more efficient in the co- Spain and Portugal and covered a period of at least evolutionary ‘arms race’ against the cuckoo. 30–35 years, we believe it is unlikely that this is the A factor that possibly influences the choice and case for all. maintenance of host species is the frecuency of nest It is not clear why the Great Spotted Cuckoo does predation. The parasite may monopolize food and not currently parasitize Azure-winged Magpie popula- maximize growth, but if many nests are depredated, tions. A remarkable feature of Azure-winged Magpie food provisioning would matter less and the parasite colonies is that individuals co-operate in communal will equally be affected. Azure-winged Magpie broods defence of nests (Cramp & Perrins 1994), which could are frequently depredated (above 80%; Cruz et al. also dissuade potential brood parasites. Experiments by 1990). Once depredated, the pair may replace the Arias de Reyna and co-workers (see Arias de Reyna clutch or they may help other pairs in the colony rear 1998) have shown that the intensity of communal the remaining broods (Valencia et al. 2003). defence by the Azure-winged Magpie against Great Consequently, the reproductive output of a breeding Spotted Cuckoo models varied among populations. colony is based on a few crowded nests rather than on Thus, it was higher where both species were sympatric many nests (Valencia et al. 2003). This is not likely to (Andujar population) than where the cuckoo was be favourable for a brood parasite, as it would therefore absent (Montoro; Arias de Reyna 1998). need to lay eggs in many nests to expect some success. Azure-winged Magpies may recognize and reject In the Magpie, predation on broods is only 22.5% parasite eggs. Rejection frequencies of experimentally (Soler et al. 1995). Therefore, the expected success of a introduced eggs have been reported at 62.5% (Arias de parasite egg laid in an Azure-winged Magpie nest Reyna & Hidalgo 1982, Arias de Reyna 1998) and should be on average corrected by 0.26 compared to 73.7% (Avilés 2004). However, this may not be strong that in a Magpie nest due only to differences in evidence for the absence of brood parasitism because expected predation (0.20/0.775 nest-survival ratio rejection frequencies in some Magpie populations between both potential hosts). The main secondary reach 100% (Soler et al. 1999) and this species remains host of the Great Spotted Cuckoo in Spain is the the main host for the Great Spotted Cuckoo in Europe. Carrion Crow, for which predation may be inter- Rejection of chicks is less likely than that of eggs mediate between both magpie species. Richner (1989)

reported a nest failure rate of 64% for this species, so Arias de Reyna, L. 1998. Coevolution of the great spotted cuckoo although the proportion due to predation was not and its hosts. In Rothstein, S.I. & Robinson, S.K. (eds) Parasitic Birds and Their Hosts; Studies in Coevolution, Vol. 9: 129–142. Oxford determined, it must be far below the 80% reported for University Press, Oxford. the Azure-winged Magpie (Cruz et al. 1990). Arias de Reyna, L. & Hidalgo, S. J. 1982. An investigation into There is some evidence that the frequency of preda- egg-acceptance by azure-winged magpies and host-recognition by tion on host nests influences the behaviour of the great spotted cuckoo chicks. Anim. Behav. 30: 819–823. Avilés, J.M. 2004. Egg rejection by Iberian azure-winged magpies Great Spotted Cuckoo. Arias de Reyna (1998) Cyanopica cyanus in the absence of brood parasitism. J. Avian Biol. discussed whether the Great Spotted Cuckoo may 35: 295–299. actively defend Magpie nests against predators. He Cooper, J.H. 2000. First fossil record of Azure-winged Magpie found less predation on parasitized nests versus unpara- Cyanopica cyanus in Europe. Ibis 142: 150–151. Cramp, S. 1985. The Birds of the Western Palearctic, Vol. 4. Oxford sitized nests in the same area. However, in the absence University Press, Oxford. of experiments he could not distinguish any anti- Cramp, S. & Perrins, C.M. 1994. The Birds of the Western Palearc- predatory effect caused by the parasite from a choice by tic, Vol. 8. Oxford University Press, Oxford. the parasite of those nests with lower risk of predation Cruz, C. 1988. Contribución al conocimiento de la biología del Rabi- largo (Cyanopica cyanus Pall., 1776). PhD Thesis, Universidad de (see Arias de Reyna 1998). 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(MS received 4 December 2003; revised MS accepted 17 September 2004)