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bInstitute of Complex Analysis of Regional Problems, Far East Branch, Russian Academy of Sciences,. Birobidzhan, Jewish Autonomous oblast, 679016 Russia.
ISSN 1062-3590, Biology Bulletin, 2016, Vol. 43, No. 7, pp. 685–692. © Pleiades Publishing, Inc., 2016. Original Russian Text © P.V. Kvartalnov, L.V. Kapitonova, 2015, published in Zoologicheskii Zhurnal, 2015, Vol. 94, No. 12, pp. 1413–1421.

The Thick-Billed Warbler (Phragamaticola aedon, Passeriformes, Acrocephalidae) as a Host Species for the Common Cuckoo (Cuculus canorus, Cuculiformes, Cuculidae) in the Middle Amur River Basin P. V. Kvartalnova, * and L. V. Kapitonovab, ** a

Faculty of Biology, Moscow State University, Moscow, 119234 Russia Institute of Complex Analysis of Regional Problems, Far East Branch, Russian Academy of Sciences, Birobidzhan, Jewish Autonomous oblast, 679016 Russia *e-mail: [email protected] **e-mail: [email protected]

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Received January 26, 2015

Abstract—The thick-billed warbler (Phragamaticola aedon) is known as one of the main host species for the common cuckoo (Cuculus canorus) in Primorsky Krai and the environs of Khabarovsk. The interaction of these species in the middle Amur River basin is discussed for the first time. In 2013–2014, at the Khingan Nature Reserve, four cuckoo eggs were found in the nests of thick-billed warblers. There are also unpublished data on the findings of cuckoo eggs and nestlings in the nests of the thick-billed warbler from the same area. The similarity of coloring of the parasite and host eggs confirms that the thick-billed warbler is one of the main host species for the common cuckoo in the middle Amur River basin. At the same time, our observations, as well as data from other researchers, show that, in the studied area, the thick-billed warbler usually recognizes cuckoo eggs and destroys them. A description of cuckoo eggs found in Khingan Nature Reserve is given, and the problems of interactions between the nest parasite and its host species are discussed. Keywords: common cuckoo, thick-billed warbler, brood parasitism, avian egg coloration, ecological races, Cuculidae, Acrocephalidae DOI: 10.1134/S1062359016070104

INTRODUCTION The common cuckoo (Cuculus canorus) is widespread in northern Eurasia, including the Russian Far East (Numerov, 1993; Stepanyan, 2003). At present, it is not rare either in natural landscapes of the middle Amur River basin or in those transformed by man (Babenko, 2000; Averin and Burik, 2007; Averin, 2010; Antonov and Parilov, 2010). In spite of the frequent occurrence and wide distribution, the biology of this species has not yet been studied sufficiently, one of the reasons being that the cuckoo is an obligate nest parasite: it is impossible to study its reproductive biology without thoroughly studying in parallel the reproduction of the host species. In comparison with many other nest parasites, the range of host species for the common cuckoo is extremely wide. They include around 300 species from 27 families of songbirds, and in the nests of more than a hundred species, cuckoo eggs and chicks are found on a regular basis (Numerov, 2003). One of the main features of the common cuckoo as a nest parasite is the similarity of the coloration of its

eggs, sometimes down to small details, to the eggs of passerine birds that serve as hosts for its chicks. This leads to a high diversity of colorations of the cuckoo eggs, on the basis of which researchers traditionally distinguish races (gentes) corresponding to the groups of females that lay eggs of a certain color, with no geographical isolation of such races and no correspondence between them and the differences in the appearance of adult birds (Malchevsky, 1958, 1987; Numerov, 2003). Another tradition in studying nest parasitism postulates that each race corresponds not to a certain egg coloration but a specific host species, which allows researchers to distinguish fractional races (Balatskii, 1994). The widest understanding of “races” reduces their number to 8−10 across the entire distribution area of the species (Numerov, 2003), but even in this case, several distinct races are found in the Russian Far East (Malchevsky, 1987; Balatskii, 1994). Judging by the number of the eggs found, one of the main hosts of the common cuckoo in this region is the thick-billed warbler (Malchevsky, 1987; Numerov, 1993, 2003), but the majority of such findings are lim-

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ited to the territory of Ussuriland (Primorsky Krai). The extreme northwestern boundary of distribution of the cuckoo race associated with parasitism on the thick-billed warbler is the environs of the city of Khabarovsk (village of Berezovka), so that the opinion has been put forward that this race is endemic to Ussuriland (Balatskii et al., 1999; Balatskii, 2010). In the West, the thick-billed warbler is distributed to the Ob River valley and Teletskoe Lake in Altai (Stepanyan, 2003), but in Siberia, no cuckoo eggs were found in the nests of this species (Balatskii et al., 1999; Balatskii, 2010). In the southeastern Baikal region, to the west of Amur oblast, both the common cuckoo and the thick-billed warbler are widespread common species. Nonetheless, cases of parasitism of the cuckoo on the thick-billed warbler were not registered in this region (Shchyokin, 2007). It is considered that, in this region, the host species of the common cuckoo are the olive-backed pipit (Anthus hodgsoni), Blyth’s pipit (Anthus godlewskii), the Siberian rubythroat (Luscinia calliope), the yellow-breasted bunting (Emberiza aureola), and, probably, the fieldfare (Turdus pilaris). An egg of the common cuckoo found in the Baikal region in the nest of an olive-backed pipit was similar to the host eggs in coloring (Shchekin, 2007). The particularities of parasitism of the cuckoo on the thick-billed warbler outside the environs of Ussuriland and Khabarovsk have not been described in the literature. MATERIALS AND METHODS Our studies were performed on the Zeisko-Bureinskaya plain, on the territory of Antonovskoe Forestry of Khingan Nature Reserve (environs of Kleshenskoe Lake). From May 25, 2013, to July 11, 2013, and from May 26, 2014, to July 30, 2014, P.V. Kvartalnov studied the biology of the thick-billed warbler and Radde’s warbler (Phylloscopus schwarzi), simultaneously searching for nests of other bird species. In 2014, O.A. Luk’yanchuk participated in these studies. A special search for bird nests that could serve as hosts for the cuckoo was performed by L.V. Kapitonova from May 31, 2014, to June 18, 2014. Earlier (in 1974–1978), in the same places, a study of the nesting birds, including the biology of the thickbilled warbler and representatives of the family Sylviidae, was performed by S.V. Vinter. In collaboration with colleagues, he prepared a monograph, which remained unpublished (S.V. Vinter, А.А. Mezhennyi, Е.P. Sokolov, and N.L. Orlov “Birds of the BureyaKhingan Lowland (Middle Amur River Basin)”). Part of the manuscript (notes on the thick-billed warbler) was courteously provided to us by Vinter and data from it are discussed in our report. We also used the data obtained from A.A. Antonov, a Khingan Nature Reserve employee, as well as data from the diaries of V.V. Nikolaev transferred to us by N.N. Balatskii.

In the places where our observations were conducted, the largest area is occupied with floodplain motley grass meadows and bogs, including lake shores. Birch (Betula platyphylla and Betula davurica) and oak (Quercus mongolica) woods grow on elevations, with the participation of aspen (Populus tremula) and linden (Tilia amurensis), and with an undergrowth of hazel (Corylus heterophylla) and (in humid places) goat willow (Salix caprea). The most thorough searches for nests were conducted within the boundaries of the lowland, on the right bank of the Borzya River, with vast motley grass and sedge meadows, sparse forests of willow and woods of Siberian silver birch, aspen, and willow. The shrub tier is represented mainly by hazel, which grows in motley grass meadows and in closed thickets and woodland, both in separate shrubs and tree clumps of fairly large sizes. In the thickets, the shrubby bushclover (Lespedeza bicolor) is also common, forming in some places dense thickets in clearings. In the Russian Far East, the common cuckoo uses the nests of several main hosts species to lay its eggs (Numerov, 1993, 2003). Of them, the most numerous species in Antonovskoe Forest was the thick-billed warbler, with the black-faced bunting (Emberiza spodocephala), the Siberian rubythroat, and the Siberian stonechat (Saxicola (torquata) maura) slightly behind in numbers. Of the species that were hosts for the cuckoo in the Baikal region (Shchekin, 2007), the olive-backed pipit was not rare, while the yellowbreasted bunting was common only in 2013. In addition, a common species nesting in mixed colonies with the thick-billed warbler was the brown shrike (Lanius cristatus). In the nests of this species, findings of cuckoo eggs and chicks are known (Spangenberg, 1964; Numerov, 1993, 2003), but it is considered that they could belong to the Indian cuckoo (Cuculus micropterus), whereas for the common cuckoo, the Siberian red-backed shrike can be only a accidental host species (Balatskii, 1994). During our studies, we found 145 nests with clutches (including incomplete ones) or chicks belonging to the following species of songbirds: the thick-billed warbler (n = 59), black-browed reed warbler (Acrocephalus bistrigiceps) (n = 1), Gray’s grasshopper warbler (Locustella fasciolata) (n = 5), the lanceolated warbler (Locustella lanceolata) (n = 1), the thick-billed warbler (n = 16), the dusky warbler (Phylloscopus fuscatus) (n = 6), the olive-backed pipit (Anthus hodgsoni) (n = 1), the brown shrike (n = 19), the Siberian stonechat (n = 2), the Siberian rubythroat (n = 5), the long-tailed tit (Aegithalos caudatus) (n = 1), the long-tailed rosefinch (Uragus sibiricus) (n = 1), the black-faced bunting (n = 21), the yellow-throated bunting (Emberiza elegans) (n = 2); the chestnut-eared bunting (Emberiza fucata) (n = 1), the Japanese reed bunting (Emberiza yessoensis) (n = 2), and the common reed bunting (Emberiza schoeniclus) (n = 1). Moreover, in 2013, in the environs of the Kleshenskoe BIOLOGY BULLETIN

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Lake, M.V. Golovina examined 11 inhabited nests of the Siberian stonechat (Golovina and Opaev, 2014; Golovina, unpublished communication). RESULTS AND DISCUSSION All eggs and chicks of the common cuckoo in the eastern part of the Zeisko-Bureinskaya plain were found in the nests of the thick-billed warbler. Of them, three eggs and one chick were found by Vinter and his colleagues, one chick was found by Antonov (unpublished data), and four eggs were found by Kapitonova, Kvartalnov, and Luk’yanchuk. Nests with cuckoo eggs or chicks constituted 13.8% of all inhabited nests of the thick-billed warbler found by Vinter et al. (n = 29), and 6.8% of all inhabited nests of the same species found by us (n = 59) or 8.0% of the nests with full clutches (n = 50). Vinter et al. (unpublished communication) found the eggs of the common cuckoo in the thick-billed warbler nests on June 29, 1975; June 12, 1976; and June 12, 1978 near Dolgoe Lake (at the border of Antonovskoe Forestry, in the area of our work) and in the lower reaches of the Bureya River near the village of Ukrainka. In the first nest, the cuckoo egg disappeared nine days later and the thick-billed warblers were brooding their own clutch. In the second and third nests, the thick-billed warblers continued laying their own eggs after the appearance of the cuckoo egg, but later on, the cuckoo eggs were removed: one of them, six days after, and the other, no less than eight days after it was laid. On June 29, 1975, in another nest of the thick-billed warbler, an eight-day-old cuckoo chick was found, which later successfully flew out. Аntonov (unpublished communication) found a cuckoo chick in the nest of a thick-billed warbler on July 8, 2009, in Lebedinskoe Forestry of Khingan Nature Reserve, in the floodplain of the Amur River (48°92.788′ N 130°50.949′ E). In the photograph made by Antonov, a cuckoo chick approximately ten days old can be seen (its eyes are open, most feathers are just appearing, but many coverts on the head and wings are unfolding, the chick demonstrates threat toward humans; see: Numerov, 1978). The circumstances of our findings were the following. The first egg was found by Kvartalnov in the nest of a thick-billed warbler that was examined for the first time on June 3, 2013, at the very beginning of its construction. The nest was built in the grass under a low dry willow bush at a height of 11 cm from the ground, on a floodplain meadow with separate shrubs and willows, near the boundary of the meadow and the quagmire on the Borzya River (49°24.208′ N 129°44.334′ E). The first egg in this nest appeared on June 9, 2013; on June 11, 2013, it contained three thick-billed warbler eggs, and on June 12, 2013, four eggs. On June 16, 2013, the nest contained three thick-billed warbler eggs and one cuckoo egg, laid “in exchange” after the BIOLOGY BULLETIN

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egg-laying was completed by the thick-billed warbler. The nest was not examined until June 8, when the cuckoo egg was damaged by the warbler (a small hole was made in the shell, on the side, the egg itself was still in the nest and its contents had not yet dried or leaked out). On that day, the egg’s measurements were taken. The cuckoo egg: 23.0 × 15.2 mm (weight not determined). The thick-billed warbler egg: 22.0 × 15.2 mm (weight 2.54 g); 21.5 × 14.6 mm (2.28 g); 22.0 × 14.5 mm (2.36 g). The shell of the cuckoo egg was collected and transferred to the Zoological Museum of Moscow State University. The thick-billed warbler chicks started to hatch on June 27, 2013. One of the chicks died on the day of hatching, two chicks successfully flew out of the nest on July 9, 2013. The second known egg (figure) was laid by the cuckoo into the nest found by Kapitonova on June 1, 2014, in a sparse willow forest, 50 m from the edge of a birch copse (49°24.413′ N 129°44.587′ E). A clump of willow trees was growing in the middle of a wet sedge tussocky meadow. The nest was made on the willow branches at a height of about 182 cm from the ground, partly hidden from view by the foliage. No birds could be seen nearby. On the day it was found, the nest was empty and looked incompletely built. On June 3, 2014, in the first half of the day, the nest was empty, no birds were found nearby either. On June 4, 2014, one thick-billed warbler egg and one cuckoo egg were found in the nest. On June 5, 2014, the nest contained one cuckoo egg and two eggs of the nest’s host; the cuckoo egg was removed by us on that day. On June 8, 2014, the thick-billed warbler female was brooding a full clutch of eggs (5 eggs), which we extracted on that day. The size of the cuckoo egg was 22.85 × 17.65 mm. The weight of the dry cuckoo egg shell was 0.24 g. The sizes of the thick-billed warbler eggs were 19.9 × 16.0 mm; 19.4 × 15.5 mm; 19.7 × 16.2 mm; 19.4 × 15.9 mm. The cuckoo egg and the thick-billed warbler clutch were transferred to the Oological Bank of G.N. Bachurin (Bachurin, 2011). The third cuckoo egg (figure) was found in a nest examined for the first time by Kapitonova on June 13, 2014 (49°24.297′ N 129°44.929′ E). The nest was located at the edge of a coppice, in a clump of trees (birch and goat willow) with an underbrush of hazel and young, low birch undergrowth. The nest was built on the stems of a hazel in the thicket of dry and live branches at a height of 120 cm from the ground and partly hidden from view by the foliage. One of the birds was close by and flew off into the neighboring trees. On that day, the nest was ready and empty. On June 17, 2014, the nest contained 3 thick-billed warbler eggs and 1 cuckoo egg. The adult bird that incubated the clutch flew off from the nest. On the ground under the nest, one fragment of the shell of a thick-billed warbler egg was lying. The cuckoo must have laid its egg “in exchange,” having eaten or thrown away one of the eggs of the nest’s host. The cuckoo egg was 23.6 × 18.3 mm in size. The weight of the dry shell was 0.28 g. The sizes

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Clutches of the thick-billed warbler with the eggs of the common cuckoo laid in them found on June 13, 2014 (top), and June 1, 2014 (bottom), in Antonovskoe Forestry of Khingan Nature Reserve (Amur Oblast). The cuckoo egg is the third from the right in each row. The photographs were made by L.V. Kapitonova.

of the thick-billed warbler eggs were 20.6 × 15.6 mm; 21.1 × 15.6 mm; and 21.2 × 16.1 mm. The cuckoo egg and the thick-billed warbler clutch were removed and transferred to the Oological Bank of Bachurin. The fourth cuckoo egg was found by Kvartalnov and Luk’yanchuk on July 8, 2014, in a thick-billed warbler nest, which on that day also contained one host egg (49°24.897′ N 129°44.235′ E). The bird that was brooding flew away. The nest was built at the base of an angelica leaf, 40 cm from the ground, in the middle of high grass, at the border of a floodplain meadow and a copse with a dense undergrowth of young aspens. On July 13, 2014, two thick-billed warbler eggs were in the nest. The cuckoo egg was absent. Under the nest we found only a shell of the third warbler egg presumably destroyed by the female cuckoo in the day she laid her egg. The subsequent fate of the thickbilled warbler nest was not traced. The size of the cuckoo egg was 22.5 × 17.5 mm, and the sizes of intact thick-billed warbler eggs were 22.3 × 16.0 mm and 22.7 × 16.5 mm. This nest was the latest of all thickbilled warbler nests found by us in 2014. Judging by the size and coloration, all cuckoo eggs found by us could have come from different females. The distance between the nests of the thick-billed warblers where cuckoo eggs were found in 2014 amounted to 0.47 km (between the first and second nests), 1.00 km (between the first and third nests), and 1.40 km

(between the second and third nests). The nests were placed approximately on one line, the first nest between the second and the third. In 2013, we noted a devastation of the clutch of the thick-billed warbler, presumably, made by the common cuckoo. The nest, built in a willow crown 329 cm from the ground, at the edge of a small birch and willow copse was found on June 10, 2013 (49°24.295′ N 129°44.472′ E). It was examined for the first time on June 13, 2013. On that day it contained 5 eggs (full clutch). By June 16, 2013, one egg had disappeared. On June 20, 2013, the nest contained three eggs. By June 26, 2013, it was devastated completely: under the nest, on the ground, fragments of shells of two eggs were found, one of which remained relatively whole with bill holes through which its contents leaked out. Evidently, these eggs were not eaten but thrown out of the nest. Apparently, both these and the other eggs were removed from the nest by a cuckoo. As a rule, other avian predators, such as the magpie (Pica pica) and Schrenck’s bittern (Ixobrychus eurhythmus) destroy the clutches entirely, not partly. According to our observations, the level of intraspecies aggression in the thick-billed warbler is low, and the eggs could not have been damaged by the birds of this species. The pair from the devastated nest, like the majority of thick-billed warbler pairs in the observation area, left its site after the destruction of its clutch. The distance BIOLOGY BULLETIN

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between the ravaged nest and the nest where we found the egg of the common cuckoo in 2013 was 230 m. In all cases of damage or disappearance of cuckoo eggs, the host eggs remained intact, which indicates that they were destroyed or removed from the nests by the thick-billed warblers themselves. The high frequency of discrimination of the parasite’s eggs by the thick-billed warblers draws attention: all five eggs that were traced destroyed or disappeared (Vinter et al., unpublished data; our data), and the breeding success of the cuckoo in the region is evidenced only by the finding of two fledglings. The eggs collected by Kapitonova were fresh, so we cannot judge the possible attitude of the hosts toward them, and they cannot be considered definitively accepted. Vinter et al. (unpublished communication) considered that the thickbilled warblers found the cuckoo eggs after their position in the nests was changed by humans. It is unlikely that this served as the main reason. Nikolaev (unpublished data) witnessed a thick-billed warbler disposing of a cuckoo egg before it was examined by a human. A ready but still empty nest of a thick-billed warbler was found by Nikolaev on June 4, 1989, in the environs of Khabarovsk. On June 8, 1989, at 4 p.m., the attention of the observer was attracted by two common cuckoos: the male that had been previously actively cuckooing, was silently following the female, which moved at a distance from the thick-billed warbler nest. When Nikolaev approached the nest, the warbler was perching on the edge and flew away as soon as he approached at a distance of 1.5 m. The nest contained three host eggs and one cuckoo egg, which was pecked through at the side. The hole was fresh, made on the same day. It is known that many primary hosts of cuckoos deal with nest parasitism by throwing out the cuckoo eggs. The most thorough research on the possibility of distinguishing the parasite’s eggs were performed with the reed warbler (Acrocephalus scirpaceus) in Europe (Davies et al., 1996). For reed warblers, the recognition of cuckoo eggs is facilitated by the variability of coloring of their own eggs, both within the clutches and in the nests of different females. Noticeable differences in the coloration of the host and parasite eggs and the variability in coloring of the thick-billed warbler egg in different clutches facilitate the identification and elimination of planted eggs. An egg found in 2013 had a light grayish-pinkishbrownish background color. Small speckles or spots were practically absent. Brown lines formed a pronounced brown around the blunt end. The length of the lines was comparable to that of the surface lines on the thick-billed warbler eggs in the same nest but some of them were noticeably thicker. Among the crown lines, short ones were conspicuous, with dots similar to commas, of the same brown color. Brown dots scattered singly in other parts of the egg and amid the crown lines were present in small quantities. Only at BIOLOGY BULLETIN

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some distance from the crown, single, thin, sufficiently long lines located closer to the blunt end could be seen. In the crown area, brownish stripes, stains, and ripples in the form of indistinct speckles in the deeper layers of the shell could be discerned. The first egg found in 2014 (figure) had a grayishpinkish-brownish background color, thinly scattered thin sinuous stripes and lines closer to the blunt end, and few small smears shaped like commas of brownish red color. Both distinct, bright surface lines and stripes and smaller, shorter and less noticeable ones in the deeper (at least two) layers were present. In some spots, the lines and stripes formed chaotic accumulations. Across the entire background, very small dots and spots were sparsely scattered at two levels, at least: the surface level and the deeper one, which gave the background a dirty appearance. These dots were of the same color as the lines. The second egg (figure) was similar to the first one in coloration, but the lines and stripes on it were thinner. There were fewer commas, the spots and smears were of the same color and on the same three layers. The remaining coloration elements were the same. The third egg found in 2014 differed more from the previous eggs than the other eggs differed between themselves. It had a pinkish-brownish background (lighter than in other cuckoo eggs examined by us). The indistinct speckles in the deep layers of the shell created the appearance of dirtiness. Another distinctive feature of this egg was the almost complete absence of superficial bright lines and any other coloration elements on the surface. The relatively thick (compared with the warbler eggs), single lines on this egg looked more like indistinct brown smears. The general impression of the egg was bleak, with a weakly pronounced, indistinct brownish pattern. Thus, in terms of coloration, the common cuckoo eggs found by us can be divided into three variation groups: with a dusty background and prominent pattern (n = 2) (figure); with a dusty background and weakly discernible pattern (n = 1); and with a clear background and distinct pattern (n = 1). The cuckoo eggs found by us differed from warbler eggs at first glance by the background color. In the warblers, at the stage of unincubated eggs, it is light pink, whereas in the cuckoos, it is also pinkish but with a marked grayish brown or brown tint. On the whole, the background tone of cuckoo eggs is darker than that of warbler eggs. The differences are also perceptible in the patterns. The length of lines on cuckoo eggs is noticeably smaller than on thick-billed warbler eggs. Large dots and commas are absent on cuckoo eggs. In addition, most cuckoo eggs are characterized by marble coloration where surface lines have different thickness along the line, now becoming dense, now less distinct. The surface pattern is nondurable and is washed away in the course of incubation due to contact with the bird’s feathers that got damp from moving through

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the wet grass because of dew or rain. The shape of the cuckoo eggs found by us is standard, ovoid. The shape of thick-billed warbler eggs is egglike or, more frequently, elongated, oblong-oval. Compared with the thick-billed warbler eggs, the eggs of the common cuckoo are larger. Judging by the description of Vinter et al. (unpublished communication), cuckoos laid eggs with a weakly pronounced surface pattern in the same region forty years ago as well. Such eggs were also found in the thick-billed warblers’ nests in the north-west of Primorskii krai, in the environs of Luchegorsk (Balatskii, unpublished communication). Only one cuckoo egg found by Vinter et al. (unpublished communication) in Amur oblast was very “similar” to the thick-billed warbler eggs. Cuckoo eggs that were almost identical in coloration to thick-billed warbler eggs, with a well-developed surface pattern, were found in the nests of the thick-billed warbler in Ussuriland and in southern Khabarovsk Krai (Balatskii, 1994; Balatskii et al., 1999; Bachurin, unpublished communication). A photograph of such an egg in the nest of a thick-billed warbler was made by Yu.B. Shibnev and featured in several publications (Lesler and Schulze-Hagen, 2011; Hauber, 2014), where the egg was erroneously attributed to the lesser cuckoo (Cuculus poliocephalus), which does not parasitize on this species (Balatskii, 1994; Numerov, 2003). Both the published illustrations (Balatskii et al., 1999) and the photos of eggs sent to us by Balatskii and Bachurin reveal that the surface lines on such cuckoo eggs are relatively uniform in thickness and resemble elements of coloration of bunting (Emberiza spp.) and tree warbler (Iduna spp.) eggs but do not have the marble pattern characteristic only of the thick-billed warbler eggs. In addition, the pattern on the cuckoo eggs is durable and should not change in the course of incubation. Despite undoubted similarity, the common cuckoo eggs in the thick-billed warbler nests are easily distinguished from the host eggs by coloration. It should be noted that the thick-billed warbler eggs in the nest presumably devastated by a cuckoo in 2013 had a weakly pronounced surface pattern and differed little in coloration from the egg laid in that year by a cuckoo in another nest in the same thick-billed warbler colony. Vinter et al. paid attention to the existence of thick-billed warbler eggs similar in coloration to cuckoo eggs (unpublished communication), but found such eggs only in 4 of the 24 clutches examined. Interestingly, thick-billed warblers allow the cuckoo eggs to stay for several days in the nest before getting rid of them. The causes of this phenomenon were studied in Bulgaria in the marsh warblers (Acrocephalus palustris) (Antonov et al., 2008). It was shown in experiments that birds sometimes lack the strength needed to break through the solid shell of a fresh cuckoo egg. Moreover, making the decision to remove the egg can take some time, owing to the problems of

recognizing the planted eggs. The thick-billed warbler is a large bird but, according to our observations, it does not catch prey that requires much force to handle, so the thickness of a cuckoo egg could be an issue for it. However, the delay in removing the egg may be evidence of sufficiently successful mimicry. The eggs of the brown shrike, which were planted into the thickbilled warbler nests as an experiment by Balatskii et al. (1999), were immediately removed by the hosts, despite the fact that they resembled the warbler eggs both in color and the size and shape, although they differed considerably in pattern (with the prevalence of spot instead of stripes). We observed a cuckoo searching for a thick-billed warbler nest only once. On June 21, 2014, a magpie (Pica pica) was examining willow clumps where there were four nests of the thick-billed warbler with clutches. The nests were located at a distance of 8−37 m from each other, and the distance between the outermost nests was 56 m. In a low willow bush not far away (15 m from the bushes with the nests), a cuckoo was sitting in a convenient position to look after the magpie and the thicket from which the warblers could fly out. The cuckoo flew away at the approach of man. The thick-billed warblers showed no sign of alarm and did not attack the magpie. Apparently, the birds in all the nests were brooding and did not leave the clutches (they were frightened away by us after the magpie and the cuckoo had flown away). Evidently, active brooding (some warblers allowed us to touch them) protects the clutch better than preventive aggression: chicks flew out later from the three nests, in the fourth one, the clutch remained unfertilized. Of the birds that nestled in the thick-billed warblers’ neighborhood, male brown shrikes (n = 6) and European stonechats (n = 1) attacked the cuckoos, flying outside the limits of their nesting plots. All cases of aggression of these birds toward cuckoos were registered from May 30 to June 11, during the period of brooding. An intense reaction of the thick-billed warblers to a common cuckoo was noted only once on June 22, 2013, when we were observing a pair of thick-billed warblers that had settled at the border of a copse and meadow. The birds were silently flying from bush to bush. When a cuckoo male perched in close proximity to them and started cuckooing, the female warbler began making alarmed noises (“bill snaps”), while the male followed the cuckoo two times but, though flying very close to it, neither attacked the bird nor screeched. The nest of this pair of thick-billed warblers was not found. On June 22, 1988, in the environs of Khabarovsk, Nikolaev (unpublished communication) observed the thick-billed warblers assaulting a common cuckoo at their nest, which contained a clutch (apparently, a repeat one) with five slightly incubated eggs. At sunset, the cuckoo swooped down on the nest 4−5 times but was driven away by the hosts, who pursued it until dark. The female cuckoo must have tried to lay its egg in the thick-billed warblers’ nest that day. BIOLOGY BULLETIN

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The thick-billed warblers’ nests were not found at random; we tried to find the largest number of nests in a certain area during the entire breeding period. In 2013, P.V. Kvartalnov monitored a plot of 15 ha; in 2014, with the participation of Kapitonova and Luk’yanchuk, it was extended to 25 ha. The nests within the control area were observed during the entire period of survey, and their fate was traced in detail. Despite the high density of thick-billed warblers (no less than 19 pairs attempted to build nests in 2013, and no less than 28 pairs in 2014) and the constant presence of cuckoos, only two of the four known cuckoo eggs were found on the site in different years. Other cuckoos’ eggs were found because we searched for nests outside the control site as well (these nests were examined less regularly and the fate of many of them was not traced). It appears that each female cuckoo used a territory exceeding the area of our intensive observations or laid few eggs. It should be noted that, apart from cuckoos, thickbilled warblers have many enemies devastating their nests. First of all, they include the magpie and Schrenck’s bittern, who search for the nests specifically, as well as the Amur badger (Meles amurensis), which destroys the clutches and chicks in nests built too low. The participation of these predators was confirmed by our direct observations or by finding unmistakable traces of their visits near the nests. Other animals that probably participate in the devastation of nests are the Siberian weasel (Mustela sibirica), fox (Vulpes vulpes), raccoon dog (Nyctereutes procyonoides), and Siberian chipmunk (Tamias sibiricus), which are not infrequent in the area of our observations, as well as other predators. The proportion of devastated nests is quite high (of the 45 thick-billed warbler nests with clutches, the fate of which was traced by us, 17 were destroyed by predators (37.8%)). Combined with the high frequency of findings of cuckoos’ eggs by the hosts and the small percent of parasite invasion of the host’s nests, the presence of predators specializing on devastating the thick-billed warbler nests must make the success of cuckoo breeding in Khingan Nature Reserve extremely low. Indeed, no young female cuckoos that were born in this area were found by us. To reveal the particulars of coexistence of the thick-billed warbler and the common cuckoo, as well as the coevolution of these species in terms of variability of the egg coloration, further research is required, either with replenishment of the museum fund of oological material orwithout removing the clutches. ACKNOWLEDGMENTS The authors thank the direction and employees of the Khingan Nature Reserve for their hospitality and assistance in conducting the works, O.A. Luk’yanchuk for help in field studies, A.A. Antonov, N.N. Balatskii, S.V. Vinter, and M.V. Golovina for the BIOLOGY BULLETIN

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information provided, and G.N. Bachurin and N.A. Formozov for participation in the discussion of the results. We also thank A.D. Numerov for the thoughtful work with the manuscript. A.S. Opaev assisted in the organization of works in 2013. This study was supported by the Russian Foundation for Basic Research, project no. 13-04-01771. REFERENCES Antonov, A.I. and Parilov, M.P., Kadastr ptits Khinganskogo zapovednika i Bureisko-Khinganskoi (Arkharinskoi nizmennosti) 1995-2009 gg (The Inventory of Birds of the Khingan Reserve and Bureya-Khingan (Arkharinskaya Lowland) in 1995–2009), Khabarovsk: Institut vodnykh i ekologicheskikh problem DVO RAN, 2010. Antonov, A., Stokke, B.G., Moksnes, A., and Roskaft, E., Getting rid of the cuckoo Cuculus canorus egg: why do hosts delay rejection?, Behav. Ecol., 2008, vol. 19, pp. 100–107. Averin, A.A., The avifauna of the Jewish Autonomous Region, Regional. Probl., 2010, vol. 13, no. 1, pp. 53–59. Averin, A.A. and Burik, V.N., Pozvonochnye zhivotnye Gosudarstvennogo prirodnogo zapovednika “Bastak” (Vertebrates of the Bastak State Nature Reserve), Birobidzhan: Institut kompleksnogo analiza regional’nykh problem DVO RAN, 2007. Babenko, V.G., Ptitsy Nizhnego Priamur’ya (Birds of the Lower Amur Region), Moscow: Prometei, 2000. Bachurin, G.N., The oological bank of cuckoos—the first ten years, in Theoretical and Practical Aspects of Oology in Modern Zoology: Proceedings of the Iv International Scientific and Practical Conference, Kiev: Fitosotsiotsentr, 2011, pp. 200–204. Balatskii, N.N., Determination of eggs of Cuculidae of Palaearctic, in Sovremennaya ornitologiya (Modern Ornithology), Moscow: Nauka, 1994, pp. 31–46. Balatskii, N.N., Priority ecological cuckoo populations on the territory of Northern Eurasia, in Aktual’nye voprosy izucheniya ptits Sibiri: Mater. Sibirskoi ornitol. konf., posvyashchennoi pamyati i 75-letiyu E.A. Irisova (Actual Problems of Studying the Birds of Siberia: Proceedings of Siberian Ornithological Conference Dedicated to Memory and 75th Anniversary of E.A. Irisov), Barnaul: Azbuka, 2010, pp. 58–61. Balatskii, N.N., Nikolaev, V.V., and Bachurin, G.N., The common cuckoo and the thick-billed warbler in the Far East, Russ. Ornitol. Zh., 1999, vol. 8, express issue no. 75, pp. 14–22. Davies, N.B., Brooke, M., and Kacelnik, A., Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic eggs, Proc. Roy. Soc. Lond. B, 1996, vol. 263, pp. 925–931. Golovina, M.V. and Opaev, A.S., Comparative analysis of the biology and behavior of two species of stonechats (Saxicola, Turdidae, Aves), in Tezisy dokl. III mezhdunarod. konf. studentov, aspirantov i molodykh uchenykh “Fundamental’nye i prikladnye issledovaniya v biologii” (Abstracts of III International Conference for Students, Graduate Students, and Young Scientists “Fundamental and Applied Research in Biology”), Donetsk: Noulidzh, 2014, pp. 47–48. Hauber, M.E., The Book of Eggs, Lewes: Ivy Press, 2014, p. 24.

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Translated by N. Smolina

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