The last meal: large insects predominate the diet of the European Roller Coracias garrulus prior to population extinction

ABSTRACT

Capsule: The diet of a European Roller Coracias garrulus population, approximately 10 years before its extinction, comprised of large-bodied orthopterans and coleopterans.

Aims: To explore the diet composition of declining population of the European Roller.

Methods: In 2005, 2006 and 2009, we monitored 18 nesting sites of the European Roller in southern Poland. Pellets and prey remain found in nest-holes were analysed.

Results: In total, 1646 prey items were found. Orthoptera (60.4% of prey items) and Coleoptera (38.5%) predominated while vertebrates were caught rarely. Large-bodied species (orthopterans, bush-crickets, beetles Prionus coriarius and Cetonia aurata) including ground-dwellers (mole cricket, field crickets) constituted a substantial proportion of the diet.

Conclusion: The results obtained show that, approximately 10 years before extinction of the local population in southern Poland, European Rollers preyed on large beetles and orthopterans, which is typical for that species. It seems that recent agriculture abandonment and natural succession may have reduced the abundance of these prey species and their availability for European Rollers and thus contribute to their extinction.

Recent changes in agriculture have led to a reduction in available food resources for insectivorous farmland birds (Fuller et al. 1995, Hart et al. 2006). The agricultural intensification that has taken place during recent decades in western and northern Europe is linked with substantial crop homogenization, increased harvesting frequency and insecticide use. These changes negatively affect the invertebrates which are the natural food resource for many farmland birds and several studies have reported deep declines in insect abundance (Shortall et al. 2009, Hallmann et al. 2017). In contrast, in eastern Europe, large areas of the agricultural landscape have recently been abandoned after the collapse of communism and again after the introduction of the Common Agricultural Policy of the European Union (Tryjanowski et al. 2011, Balzsi 2017). This has led to encroachment of tall herbaceous vegetation, shrubs and trees which may often increase biomass of invertebrates but substantially decrease their availability for birds (Hoste-Danyłow et al. 2010) as many species need short vegetation for foraging (Johst et al. 2001, Rodríguez et al. 2014, Chrenkova et al. 2017).

Therefore, recent changes in agricultural landscapes have led to a reduction in food availability for many farmland birds which in turn has seriously affected their survival and contributed to negative population trends (Johst et al. 2001, Ghilain & Bélisle 2008, Butler et al. 2010). It seems that the European Roller Coracias garrulus (hereafter Roller) is one species that has been impacted by both agriculture intensification, which results in a decline in invertebrates, and agriculture abandonment, which limits prey availability. Central European populations of the Roller have been vanishing rapidly during recent decades and negative trends have been reported from Estonia, Latvia, Lithuania, Poland, Belarus, Ukraine and Slovakia (BirdLife International 2004). In Poland, its population has experienced a deep decline during recent decades, from approximately 1000 pairs in 1980 to only 16–20 pairs in 2016 (Tomiałojć & Stawarczyk 2003, Chodkiewicz et al. 2018), while in Belarus, the decline was even sharper (Tarantovich 2016). Drivers of these negative changes remain unknown; however, a decrease in food availability is one of the possible factors.

Generally, Rollers hunt for large-bodied invertebrates and forage mainly on the ground (Cramp 1985, Aviles 1997, Bohuš & Krištin 2004). However, the species occurs in many different regions in both southern (from Portugal to Greece and Turkey) and eastern Europe, reaching Estonia in the north. Over such an extensive spatial scale, there is extensive variation in both environmental conditions (e.g. vegetation structure and height, management, climate, etc.) and invertebrate communities. One might expect, therefore, that the Rollers’ foraging ecology and its prey composition is also highly variable over the species distribution range and reflect local availability of preferred prey. However, empirical data on the Rollers’ diet composition in many regions are lacking, especially from northeastern parts of its range, where local populations are currently on the verge of extinction.

Here, we analyse diet composition of a declining population of the Roller in southern Poland. This local population become extinct in 2015 but we collected data on over 1600 prey items a few years before its extinction. We aimed to describe the feeding habits of Rollers in southern Poland in the context of other dietary studies of this species. As the proportion of Coleoptera in the diet tends to be greater at higher latitudes (Glutz von Blotzheim & Bauer 1980), we expected that this prey group would predominate in Poland. It is not clear, however, if diet composition remains the same in populations in sharp decline, like the Polish one. Addressing these questions may help to understand the mechanisms of the decline.

Methods

Study area

We conducted research in southern Poland (50.3388–50.4559° N, 21.8642–22.0287° E). This region historically was dominated by the extensive agriculture with small patches of grassland and arable fields located mainly along river valleys, as well as large, pine-dominated, managed forests. Small woods placed along river valleys and canals were dominated by willow Salix, birch Betula and Black Alder Alnus glutinosa. Most of farmsteads were clustered in small villages. During recent decades, however, land-use and agriculture have changed dramatically; a substantial proportion of land has been abandoned as local agriculture production became unprofitable. Grazing by cattle ceased, parts of pastures and meadows were converted to arable land but most of them were encroached by shrubs and trees.

Diet analysis

During 2005, 2006 and 2009, we monitored 18 nesting sites of the Roller. These were mostly in tree holes, excavated by Green Woodpeckers Picus viridis, Grey-headed Woodpeckers Picus canus and Black Woodpeckers Dryocopus martius, mainly in Black Alder, willow, lime Tilia and birch. Two nests were in nest-boxes. Nesting trees were located in small infield woods, mainly adjacent to rivers or ditches.

Generally, adult Rollers provisioning nestlings bring whole prey to the nest (Cassola & Lovari 1979) and pellets made of indigestible items are produced two to three times per day by the nestlings (Ganya et al. 1969). Food provisioning is up to 10 food items per nestling per hour (Cramp 1985). Also, some prey remains are to be found decomposing in the nest during hatching and nestling stages. The accumulation of pellets and prey remains in the nest is considerable, enabling diet description, although pellet analysis and prey remains give slightly different results than studies using nest cameras to identify prey delivered by parents (Francksen et al. 2016, Catry et al. 2018) and can overestimate consumption of prey species which have identifiable hard parts (Rosin & Kwieciński 2011). However, pellet analysis gives comprehensive information on Roller diet composition (Catry et al. 2018).

To investigate the diet of nestling Rollers, the nest-hole contents were removed in the late summer, after the young fledged or the brood was depredated. In the case of tree holes, the breeding chamber was vacuumed by using a vacuum cleaner powered with a generator. When the contents were compact, they were first broken into pieces then vacuumed. Nests placed in nest-boxes were removed as a whole.

The removed nests were placed in plastic bags. The material then was disintegrated in the laboratory and searched for any undigested prey body parts such as legs, mandibles, head, pronotum, elytra, wings and ovipositors. All prey elements were sorted and labelled according to taxonomic order and preserved for species identification. Next, the remains were identified by taxa specialists to genus or species level if possible, using keys to identification and reference collections (mainly Orthoptera, Coleoptera). The minimum number of individuals of each species was calculated on the basis of the most frequent body elements belonging to a certain species (Tidmarsh 2004).

Results

In total, we recorded 1646 prey items in the prey remains of 18 nests of Rollers. The diet was dominated by Orthoptera and Coleoptera. Large orthopterans, bush-crickets, mole crickets and field crickets were the most common. In the case of beetles, the large-bodied saproxylic longhorn beetle Prionus coriarius was also important, followed by the nectar feeder Cetonia aurata. Remains of vertebrates were found only rarely (Table 1 and Figure 1).

Figure 1. Number of prey individuals (proportional to area of rectangles) found in European Rollers’ nests in southern Poland, as presented in Table 1.

Table 1. Diet composition (number of prey individuals) of the European Roller in southern Poland. Data from pellets and prey remains found in nests of 18 pairs in 2005, 2006 and 2009.

Prey item	N	Prey item	N
Tettigonia viridissima	10	Rhantus sp.	1
Tettigonia viridissima/cantans	9	Dytiscidae total	1
Decticus verrucivorus	332	Tenebrio molitor	2
Metrioptera roeselii	37	Tenebrionidae total	2
Tettigonidae Indet.	2	Agonum sp.	1
Tettigonidae total	390	Broscus cephalotes	1
Calliptamus italicus	4	Carabus auronitens	5
Chortippus sp.	22	Carabus granulatus	4
Psophus stridulus	1	Carabus violaceus	1
Acrididae Indet.	10	Carabus sp.	1
Acrididae total	37	Cicindela hybrida	1
Gryllus campestris	388	Poecilus sp.	4
Gryllotalpa gryllotalpa	179	Carabidae Indet.	9
Orthoptera total	994	Carabidae total	27
Carpocoris fuscispinus	1	Byrrhus sp.	2
Carpocoris purpureipennis	1	Byrrhidae total	2
Coreus marginatus	0	Agriotes sputator	1
Dolycoris baccarum	1	Agriotes sp.	4
Eurygaster maura	5	Agrypnus murinus	3
Peribalus strictus	1	Elateridae Indet.	20
Heteroptera total	9	Elateridae total	28
Amphimallon sp.	8	Nicrophorus sp.	5
Anomala dubia	62	Phosphuga atrata	6
Aphodius fimetarius	1	Silpha obscura	3
Cetonia aurata	84	Silpha sp.	6
Cetoninae sp.	7	Silphidae Indet.	4
Copris lunaris	1	Silphidae total	24
Melolontha sp.	1	Aromia moschata	1
Oryctes nasicornis	3	Prionus coriarius	113
Polyphylla fullo	1	Spondylis buprestoides	80
Protaetia metallica	6	Cerambycidae Indet.	12
Trichius fasciatus	1	Cerambycidae total	206
Scarabaeidae Indet.	38	Coleoptera Indet.	44
Scarabaeidae total	213	Coleoptera total	634
Geotrupes sp.	7	Arianta arbustorum	3
Geotrupidae total	7	Gastropoda total	3
Leptinotarsa decemlineata	51	Anura sp.	2
Chrysomelidae total	51	Amphibia total	2
Otiorhynchus sp.	2	Lacertidae Indet.	1
Entiminae Ind.	5	Reptilia total	1
Hylobius sp.	1	Microtus arvalis	1
Curculionidae total	8	Micromys minutus	1
Cantharis fusca	13	Sorex araneus	1
Cantharis sp.	8	Mammalia total	3
Cantharidae total	21	Sum	1646

Discussion

Orthoptera and Coleoptera were the most important diet components of breeding Rollers in Poland. Our study confirmed that the diet of the Roller was dominated mainly by large-bodied insects active on the ground (field crickets, mole crickets) or in low vegetation in grasslands and fields (bush-crickets). In general, these results are similar to several previous studies describing the diet of Rollers (Glutz von Blotzheim & Bauer 1980, Cramp 1985) but some differences are noticeable.

In Rollers, the diet is dominated by two groups of invertebrates: orthopterans and coleopterans, which pooled together often exceed 95% of all prey (Rębiś 1998, Sosnowski & Chmielewski 1996, Tidmarsh 2004). However, the share of the former in the diet tended to be higher in the southern part of Roller’s distribution range (Glutz von Blotzheim & Bauer 1980). For instance, in the south of France, the share of Orthoptera equalled 64% of prey consumed (Tidmarsh 2004), 51% in Spain (Aviles 1997) and 57% in south-central Russia (Glutz von Blotzheim & Bauer 1980). In contrast, in northern parts of the species distribution range, the importance of orthopterans in the diet is much lower: 27% in southern Hungary (Gyula 1998) and between 12% (Rębiś 1998) and 26% (Sosnowski & Chmielewski 1996) in Poland. Also, Bohuš & Krištin (2004, recalculated) reported that in Slovakia the diet was dominated by Coleoptera (57% of recorded prey items), as also found in Estonia (Luutsepp et al. 2011), while close to Petersburg (Russia) and in Brandeburg (Germany) the shares of Coleoptera were even higher (60% and 78%, respectively; Glutz von Blotzheim & Bauer 1980). Recent findings from Belarus report that beetles constituted 75% of prey (Tarantovich 2016). Thus, our results indicating a higher share of orthopterans (60%) than beetles (39%) in the Roller diet are slightly unexpected and similar to those reported from the south of Europe. On the other hand, substantial variation in the Orthoptera to Coleoptera ratio in the diet can be observed at a relatively small spatial scale (Kiss et al. 2014). Also, Bohuš & Krištin (2004) reported marked differences in diet composition between years, most likely reflecting local and temporal habitat composition and prey availability, while Catry et al. (2018) showed that diet composition can substantially differ between adults and nestlings, with orthopterans being more often consumed by the latter.

Most studies analysing the Roller diet found that vertebrates – mainly reptiles and small mammals – were very rare (Gyula 1998, Sosnowski & Chmielewski 1996), which is similar to our findings. But this may be partly due to the method used. Vertebrates are less common in pellets and prey remains from nest-holes, while more often reported when direct observations are taken into account (Rębiś 1998, see also Catry et al. 2018 for differences in diet composition based on pellet analysis and camera images) so full diet descriptions require different methods of diet analysis. Among invertebrates, large-bodied species were common, but several are recognized as pests in agriculture or forestry (in our study: Anomala dubia, Gryllotalpa gryllotalpa, Spondylis buprestoides, see also Luutsepp et al. 2011). Thus, some of them can be limited by insecticide spraying on the arable fields, orchards or in forests, which in turn may affect food availability for the Roller. Indeed, several invertebrate species that are important in the diet of farmland birds have recently become rare. Field crickets, which form an important component of the diet of the Roller but also of Montagu’s Harriers Circus pygargus (Mirski et al. 2016), were common in extensively used farmland but are now rare in many regions of western Europe (Hochkirch et al. 2007) and rarely reported in the Roller diet in that region (Tidmarsh 2004). Furthermore, invertebrate abundance has declined substantially in many European regions (Lindhe et al. 2011, Honek et al. 2014, Hallmann et al. 2017), although it is not clear if similar patterns hold on in central and eastern Europe where agriculture is less intensive (Tryjanowski et al. 2011).

Decreasing insect abundance may be an important problem not only for Rollers but also for several other bird species that hunt mainly large-bodied invertebrates (e.g. Eurasian Hoopoe, Upupa epops; Guillod et al. 2016). Larger prey ensures better energetic yield, which is critical during the nestling provisioning phase of reproduction. It cannot be excluded, therefore, that recent negative population trends of bird species feeding on large-bodied invertebrates, such as Little Owls Athene noctua, shrikes, Rooks Corvus frugilegus, White Storks Ciconia ciconia, Hoopoes and Montagu’s Harriers (Chrenkova et al. 2017), may be partly driven by food shortages. This mechanism, however, may be generated by different types of agriculture transformations (e.g. abandonment or intensification) and thus different conservation measures may be appropriate in different regions.

Acknowledgements

The authors wish to thank to Seweryn Grobelny, Miłosz Mazur and Marek Przewoźny for their help in the identification of invertebrates.