This study illustrates the importance of considering old references and sources not included in the Science Citation Index to get missing information about biodiversity. For disciplines with a long tradition, such as food regime studies, it would be common sense not to restrict bibliographic searches to the latest decades. Our results show that, when available, cicadas are predated on by many terrestrial birds of the WP, including cuckoos, owls, bee-eaters, woodpeckers, falcons, reed-warblers, larks, crows and jays, buntings, shrikes, pipits and wagtails, flycatchers and chats, tits, sparrows, leaf-warblers, starlings, warblers and thrushes. Cicadas are indeed commonly found in the diet of insectivorous birds such as bee-eaters, Sylvia warblers and pipits during the breeding season (Turrian and Jenni 1991; Kossenko and Fry 1998), but can also make up as much as 70% of food items delivered to nestlings in the mostly granivorous Pale Sparrow (Cramp et al. 1998). Even for medium-sized raptors, like the Peregrine Falcon, these insects can constitute a main prey (Ellis et al. 2007). More surprisingly, cicadas are important food for several species of terns and herons that can feed on nymphs emerging near the shore of ponds and wetlands, or in grasslands (Privileggi et al. 2009). Some Laridae, like the Mediterranean Gull and the Gull-billed Tern, can feed young mostly with insects (Goutner 1994; Bertolero and Rivaes 2015). Cicadas can also be a preferred prey, hunted on the wing and in the ground (e.g. by the Roseate Tern Sterna dougallii, foraging near nesting colonies; Forbusch 1924).
An estimated 34% of WP bird species are only known to consume Cicadidae from studies carried out outside the WP, including an estimated 9% outside the Palearctic. These are bird species with cosmopolitan distribution or very large range, whose diet has been studied in other biogeographic realms. It is likely that they also eat cicadas in the WP whenever they are available. In the Afrotropical and Oriental realms, local abundance of cicadas could be relevant for the survival of WP overwintering birds. However, studies on diets of terrestrial birds in these wintering grounds, with the exception of some falcons and raptors (e.g. Verma 2005; Kopij 2007) are scarce. When available, the coarse taxonomic classification of prey items does not allow verifying the occurrence of cicadas in samples. On the other hand, WP bird species that overwinter in the south of the region (including the Mediterranean Basin) do not encounter cicadas, that are belowground and emerge at the end of the spring and in summer.
It is still soon to draw solid conclusions about the relative importance of cicadas as prey for birds in the WP. The diet of many bird species has not been studied in detail and, when it has, studies have seldom offered a broad geographical and temporal scope (Cramp et al. 1998). The results obtained are therefore biased towards those species that have been more intensively studied. Moreover, many studies lack proper quantification of prey items based on large samples. Nevertheless, the predominance of studies conducted in Mediterranean and Middle East countries, finding cicadas in the diet, matches the north–south gradient in species richness and also cicada abundance in landscapes. An additional, although probably minor problem, stems from studies in which Cicadidae in samples have been incorrectly cited and which could have gone undetected despite the search filters. Most gaps in diet studies have not been filled in recent years. However, a change in methods commonly used towards observational studies and non-invasive approaches analysing the contents of pellets or droppings (Fig. 3) has been taking place. Moreover, promising molecular techniques are being developed, like DNA sequencing-based diet analyses (Alberdi et al. 2019). The increasing affordability of molecular sequencing techniques may help expand these studies in the future, with a focus on threatened species, underrepresented in studies so far. In sum, the figure of 16% of WP bird species consuming cicadas is more an expression of our current knowledge of bird diets than an estimate of the real proportion of species preying on Cicadidae.
Logically, the follow-up question is what new species can we expect to find eating cicadas? A possible reasoning considers predators-prey body size relationships (Barnes et al. 2010). Fifteen bird species are either known to eat periodical cicadas or to be demographically affected by cicada emergences in the hardwood forests of the eastern United States (Koenig and Liebhold 2005). Their body masses range from the 17 g of the Red-eyed Vireo (Vireo olivaceus) to the 453 g of the American Crow (Corvus brachyrhynchos) (Birds of North America 2019). In turn, the body mass of Magicicada spp. (3 species of 13-year cicadas) oscillates between 0.15 g for males and 0.21 g for females (Rowell and Grammer 2019). The weight of birds known to eat cicadas in the WP ranges from 5.5 g in the Goldcrest (Regulus regulus) to more than 1000 g in the Raven (Corvus corax), the Great White Egret, the Grey Heron (Ardea cinerea) and the Peregrine falcon (Falco peregrinus). The largest cicada in the WP, Lyristes plebejus, is 1.8 g and the common forest species Cicada orni is 0.7 g (unpublished data). But species belonging to genera Cicadetta or Tettigettalna, among others, are much lighter and easier to seize and process by the small beaks of some insectivores. The consumption of cicadas by the Goldcrest shows that there is no body size limitation for birds to prey on Cicadidae species. It is therefore likely that most bird families and species in the WP can potentially eat cicadas. The potential list should exclude marine and wetland birds with specialized aquatic diets, nectarivorous sunbirds and possibly large raptors and vultures. Regarding habitats, cicadas are captured by birds from marshes and grasslands, to shrublands and forests. This predation is likely more intense in woodlands, where higher species richness and abundance are usually found (Puissant 2006).
Western Palearctic cicadas are difficult to find when hidden in vegetation or still against their background of bark or twigs. They also have good sight and are relatively quick flyers over short distances. Adults are unlikely to be easily captured in dense vegetation. However, preying on flightless nymphs can be much easier. Predation takes place mostly when they emerge from belowground and are walking to reach a support to moult. Although this only takes a few minutes, emerged nymphs can support high predation rates (of 24%) in Mediterranean forests, mostly by birds (Patterson et al. 1997). Additional predation can happen while moulting and drying wings on substrates close to the ground. While walking or moulting, nymphs are mainly predated on by ground-foraging birds (Sazima 2009). It is interesting to note that many cicada species emerge before dawn, probably to avoid most predators. Owls can then become their main avian predators (Vezinet 2003).
Recent reviews have quantified the global contribution of insectivorous birds to the ecosystem service of regulating insect populations (Nyffeler et al. 2018). Since both insect populations, and birds species that feed on insects are threatened and continue declining worldwide (Sánchez-Bayo and Wyckhuys 2019; Sekercioğlu et al. 2004), studies of bird species diets are now of foremost relevance. Large insects in particular have suffered abundance declines (Shortall et al. 2009) and cicadas can be a temporarily abundant alternative prey. Cicadas are found aboveground in late spring and summer, coinciding with chick rearing and the post-fledging period, in the WP. The juvenile survival of species selecting cicada as main prey, like the Eurasian Jay, may therefore increase in response to a locally high cicada density (Patterson et al. 1991).
