Spatial and temporal patterns in the diet of barn owl (Tyto alba) in Cyprus

Spatial and temporal patterns in the diet of barn owl (Tyto alba) in Cyprus Background: The barn owl, a nocturnal raptor with cosmopolitan distribution, shows a great adaptability to differ - ent environments. Regarding prey, the barn owl is a rather selective species, but if changes in the abundance of the selected prey occur, it becomes an opportunistic predator and easily incorporates other prey in its diet, using a wide range of prey species and foraging habitats. Small rodents are usually the prey mostly used. Compared to the popula- tions of north and eastern Europe, barn owl populations in the Mediterranean area have been the least studied. In Cyprus, where barn owl is a common bird species, there are no studies on its diet and feeding ecology. This study was carried out to contribute to the spatial and temporal patterns barn owl diet in Cyprus also providing information on small mammals’ presence and species composition on the island. Methods: This study was based on 1407 regurgitated pellet analysis that were collected from 26 sites representing six major habitat types on central and southern Cyprus from summer 2013 to summer 2014. The diet of the barn owl was described in terms of seasonal average biomass and numerical percentages of each prey species and com- pared by Kruskal–Wallis test. Seasonal prey diversity and evenness indices were also calculated. Principal component analysis (PCA) was performed on the prey biomass proportion data assigned to six major habitat types with regard to elevation, vegetation and human uses. Results: Low prey diversity was found comprised mainly of rodents (overall means 96.2 and 95.7% by number and biomass, respectively). Mice followed by rats were most important prey whereas insectivores, birds and insects were minor components of the owl’s diet. Evenness and diversity values were relatively similar among seasons. PCA differentiated mainly between lowland areas where mice were more abundant prey and mountainous areas where rats dominated in the diet. Insectivores correlated with birds, prey types characterizing several lowland and highland habitats. Conclusions: The barn owl prey composition in Cyprus suggests an opportunistic foraging behavior, low prey spe- cies diversity with variations in the main rodent prey that could be explained by their distribution, seasonal activity and habitat preferences. Keywords: Barn owl, Cyprus, Feeding ecology, Tyto alba Background food supply and refuge and enables it to inhabit areas The barn owl ( Tyto alba (Scopoli, 1769); order Strigi- such as Negev desert, Israel [5], Simpson desert, Aus- formes) is a nocturnal raptor with cosmopolitan dis- tralia [6] and Atacama desert, Chile [7]. The barn owl tribution, being common in the temperate and tropical shows a great adaptability to different environments zones of the world [1–3]. It exhibits low resistance to explaining its cosmopolitan distribution [7]. As a con- cold [4]. Its presence in arid environments depends on sequence, use of a wide range of prey species [1, 2] and foraging habitats [8] have been reported. Although for- aging opportunism, that is use of a wide range of prey *Correspondence: vgoutner@bio.auth.gr 1 species depending on their availability, has been sug- School of Biology, Aristotle University of Thessaloniki (AUTH), 541 24, Thessaloniki, Greece gested as a common behaviour exhibited by the species Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 2 of 8 [7, 9–12], it has also been indicated that barn owl is an The locations sampled are presented below. The respec - A selective predator, so its diet does not represent the tive names are indicated in Fig. 1. true abundance of prey in the wild [13–17]. According to Tores et  al. [18] and Muñoz-Pedreros et  al. [17] the Group 1. Mountain with Pinus brutia pine forests barn owl cannot be defined as a pure opportunist or a and maquis pure selective hunter. This strategy of flexible hunting Apliki makes the barn owl a very successful predator, explain- A nest was found in a Quercus alnifolia zone, with pines ing its wide cosmopolitan distribution and the ability and maquis (1000 m asl). to colonize new environments, a plastic diet strategy much greater than that of most other species of raptors. Potamitissa In conclusion, barn owl is a rather selective species, but A natural nest was found in a cavity of an oriental plane if changes in the abundance of the selected prey occur, tree in a clump of trees (alders, plane, pine and olive it becomes an opportunistic predator and easily incor- trees) and scattered low vegetation of thorny shrubs porates other prey to its diet even prey of low energy (820 m asl). value [19], remaining in its territory even when the selected prey types decrease [17]. The barn owl feeds Athrakos mainly on small mammals (7–24  g), probably without An artificial nest placed on a pine tree was in use and pel - discriminating between large and small prey [20]. In lets were collected from a nearby roost. Sparse vegetation the Mediterranean region, a combination of suitable with Cistus shrubs and some arable land surrounded the climatic conditions and long-term human presence has sites (676 m asl). favoured the establishment of this species, supporting relatively high population densities [21]. Compared to Prastio Kellakiou the populations in north and eastern Europe, those in An artificial nest was in use placed in a hilly area covered the Mediterranean area have been the least studied [8]. with a variety of natural vegetation, such as Quercus alni- Barn owl is a common resident in Cyprus and its folia, Cistus sp., Eucalyptus sp., fruit and pine trees, and population is estimated at 250–750 breeding pairs cypress trees (490 m asl). (these estimates are conservative) [22]. AGROLIFE project [23] in cooperation with Game and Fauna Pelentri Service explored an alternative to rodenticide rodent An artificial nest was in use situated on a pine tree in an control via use of barn owl nesting boxes. In Cyprus, area of scarce pine trees, Quercus alnifolia, Cistus sp. and information on the breeding ecology and trends of the fruit trees (800 m asl). barn owl is limited [24], whereas there are no studies on its diet and feeding ecology. Similarly, very few such Lefkara studies occur in the eastern Mediterranean [10, 25]. An artificial nest was in use situated under a bridge in The aim of the present study was (a) to contribute an area surrounded with pine trees, cypresses trees and to the spatial and temporal patterns barn owl diet in reedbeds (430 asl). Cyprus, providing information lacking so far; (b) based on prey use of the owl, to provide data on the presence Group 2. Lowlands with agricultural crops and species composition of small mammals on the Avdimou island, where relevant information is scarce. An artificial nest on a pine tree in a lowland area was in use. Reedbeds surrounded the area (380 m asl). Another Methods artificial nest placed in the same area on an electric The study area power pole was also in use. Cyprus (35°00′N, 33°00′E), is the third largest island in the Mediterranean Sea  covering an area of 9250  km Paramali (Fig.  1). The location of the island, with Africa to the An artificial nest in use was situated on a cypress tree on south, Turkey and central Europe to the north and the cultivated land (20 m asl). Middle East to the east, is very important for the avifauna of the island. Cyprus includes a diversity of habitats such Agios Dimitrianos (Episkopi) as sand dunes and rocky coastline, wetlands, streams Two nests were located on pine trees surrounded by cul- and lakes, scrubland, agricultural land (e.g. cereal fields, tivations, scattered pines and fruit trees (23 m asl). orchards, vineyards), desert-like uncultivated or rocky land, and forests (mostly pine forests) [26]. Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 3 of 8 Fig. 1 Map of Cyprus indicating the sampling sites of barn owl pellets. Sampling sites have been assigned to groups according to habitat type (1–6) Pareklisia Group 3. Hilly areas with crops and livestock facilities A roost site was found in a rocky area near habitations, Kofinou sparse vegetation and cultivations with Pistacia lenticus. An artificial nest in use was placed near livestock areas. The surrounding vegetation was composed of culti - vated trees (mainly almond) and low shrubs (169 m asl). Avdellero A nest was placed under a bridge within a livestock graz- ing area (135 m asl). Anglisides An artificial nest and roost sites in use were under a Achelia stone-built bridge. Reedbeds, acacias and olive trees Four artificial nests placed on cultivated land were in use were the most important vegetation around this site (35 asl). (174 m asl). Timi Klavdia An artificial nest in use was situated in a forest sur - An artificial nest was in use was placed under a bridge. rounded by cultivations and low vegetation at about sea The surrounding habitat was similar to Anglisides (170 m level. asl). Kellia Makounta An artificial nest in use was placed under a bridge in an A nest was found in a craggy mountainous area. The area with riparian vegetation of reedbeds and acacias surrounding habitat was dominated by agricultural and (55 m asl). tree cultivations (100 m asl). Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 4 of 8 Panagia Aimatousa Data analysis A roost site was located near livestock facilities in an area The pellets were analyzed using reference books [34– surrounded by olive trees. 36], but excluding those that contained only hair. Mean weight of each prey taxon was taken from the literature [37, 38]. Mice of the genus Mus and rats Rattus were not Group 4. Areas with dry vegetation identified at the species level because it was impossible One roost site was found near Zodia (85 asl) and three to distinguish them by cranial characters. Although their at Pano Koutrafas (241  m asl), in dry craggy areas with identification could be possible through DNA analysis of bushes, acacias and some fruit tree cultivations. hair found in the pellets, this approach was beyond the scope of the present study. Rats most likely belonged to Group 5. Mountainous areas with vineyards and olive trees the species Rattus rattus as the presence of Rattus nor- Trachypedoula vegicus on Cyprus is dubious [36]. Insects were iden- A roost was found on a stone-built bridge. The surround - tified at the level of family due to the poor condition ing area included vineyards, olive cultivations and bush- of their remains in the pellets. The diet of the barn owl land (500 m asl). was described in terms of seasonal average biomass and numerical percentages of each prey species. Average prey Vretsia weight of each species in each period was estimated by Two nests were located in deserted buildings in a village. multiplying the numbers of each prey item by its mean Nearby areas were covered with vineyards and citrus weight, adding the weights produced and dividing the fruit cultivations (500 m asl). sum by the total numbers of prey in each sample. The diet of barn owl was analysed for each field sample in terms of Group 6. Lowlands with maquis vegetation numbers and biomass. Median prey weights were com- Kouklia pared among different seasons by Kruskal–Wallis test. Roosts were located on a bridge and nearby areas sur- These tests were performed using R [39] and Statistica rounded with maquis and olive and carob trees. version 7.0 (StatSoft, Tulsa, USA) softwares. The prey diversity was estimated at a class level (mammals, birds, Pellet collection insects) by using the antilog of the Shannon-Weiner Available evidence indicates that pellet analysis is still index [40, 41], while the evenness index for the mammals the most suitable method for studying the diet of owls was calculated by using the Hill’s ratio [42, 43]. especially the medium sized ones [9, 27, 28]. Analys- The prey types were assigned to six major habitat types ing a small sample of pellets can give adequate informa- with regard to elevation, vegetation and human uses tion about prey composition in the field and it takes less (Fig.  1). Principal component analysis was performed on working hours than mammal trapping [29, 30]. Despite the prey biomass proportions data from the six habitat the controversy whether pellets represent the true com- types. The analysis showed that 99.6% of the variation in munity structure of the prey [15], pellets can give infor- the dataset was explained by the first three components mation about prey-species communities and other while the first two components explain 77.9% of the vari - biogeographic data [1, 31, 32]. Pellets are relatively easy ance in the data. Only the first 2 components were con - to find and small bones remain well preserved within sidered in the analysis based on the Kaiser stopping rule, them [2]. Pellet analysis is a useful tool for the manage- i.e. the number of components with eigenvalues over 1 ment and protection of owl species and their habitats [1] [44]. while the outcome from the analysis can be used to assess ecosystem health [2, 33]. Results Pellets were collected at the end of every season for Prey composition and seasonal variation in barn owl’s diet 1  year, from summer 2013 to summer 2014. They were In a total of 1407 pellets analyzed during the study, 3312 collected from natural nests (situated at old buildings, prey items were identified (mean 2.35 prey items per pel - tree cavities and under bridges) and nesting boxes placed let, ranging from 1 to 8). The diet of the species was made and monitored by the Game and Fauna Service. The nests up almost exclusively of small mammals, both in num- were located at a variety of habitats, including coastal ber and biomass (overall means 96.2 and 95.7%, respec- areas, lowlands (0–500 m elevation) and mountain areas tively) (Table 1). Of the small mammals, mice (Mus spp.) (above 500 m elevation) with different types of vegetation dominated the owl’s diet both by numbers and biomass (see above for a detailed presentation of the localities). in most seasons, followed by rats (Rattus spp.) with their relative proportions varying seasonally (Table 1). Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 5 of 8 Lesser White-toothed shrew (Crocidura suaveo- lens), though numerically higher than rats in summer and autumn of 2013, were much less important by bio- mass due to their small size. The numerical distribution of these three major prey types differed significantly through the study period (Kruskal–Wallis χ = 69.638, df = 13, p < 0.0001). Etruscan shrew (Suncus etruscus) was of minor importance among the mammalian prey present in proportions being highest in summer 2013 and relatively similar in the other seasons (Table 1). Βirds were found in low proportions in the diet (2.6–6.0% by biomass) whereas insects were unimportant as prey (Table  1). Evenness and diversity values were relatively similar among seasons with spring and summer 2014 evenness values being lowest (Table 1). Spatial variation in barn owl’s diet PCA biplot (Fig.  2) shows the correlations among prey types and also the habitat and temporal variation in barn owl’s diet. Mice showed a positive correlation with insects and slight to negative correlations to other prey types, particularly rats that were slightly positively cor- related only to birds. Etruscan and lesser white-toothed Fig. 2 Biplot containing the first two principal components presenting the differentiation of barn owl prey according to shrews and birds were very highly positively correlated habitat. Symbol meaning: 1: Mountain with pine trees and maquis; with each other and negatively correlated with insects. 2: Lowlands with agricultural crops; 3: Hilly areas with crops and Mice and insects were mostly involved in the owl’s diet in livestock facilities; 4: Areas with dry vegetation; 5: Mountain hilly areas with crops and livestock facilities, areas with areas with vineyards and olive trees; 6: Lowlands with maquis dry vegetation, and lowlands with agricultural crops in vegetation. Different colours denote the 5 different sampling periods during 2013–2014. A Autumn, W Winter, S Spring, U Summer (i.e. both years and across seasons. Nevertheless, insects were 2A13 = Samples from lowlands with agricultural crops during autumn not an important prey category (as shown in Table  1). of 2013) Shrews and birds were more important in lowlands with Table 1 Seasonal diet of barn owl in Cyprus in % numbers (N) and % biomass (B), from summer 2013 to summer 2014 Prey type Summer 2013 Autumn 2013 Winter 2013–2014 Spring 2014 Summer 2014 N B N B N B N B N B Insects 2.7 0.1 1.3 0.1 0.4 0.1 0.4 0.1 – – Birds 1.8 3.0 4.2 5.8 3.0 3.8 1.7 2.6 3.5 6.0 Mammals 95.5 96.9 94.5 94.1 96.6 96.1 97.9 97.3 96.5 94.0 Mice (Mus spp.) 64.6 52.0 70.4 48.8 72.2 44.2 76.9 57.2 76.9 62.3 Rats (Rattus spp.) 9.1 36.4 11.9 41.4 16.2 49.5 9.7 36.3 6.6 27.0 Lesser White-toothed shrew (Croci- 20.8 8.4 10.7 3.7 7.5 2.3 9.6 3.6 11.0 4.4 dura suaveolens) Etruscan shrew (Suncus etruscus) 0.9 0.1 1.5 0.2 0.7 0.1 1.7 0.2 2.0 0.3 Total number of prey 331 – 1063 – 759 – 934 – 225 – Prey diversity 1.24 1.28 1.18 1.12 1.16 Evenness 0.69 0.71 0.70 0.58 0.60 Median prey weight (g) 4.86 3.73 2.45 2.30 1.49 Interquartile range: 25–75% 22.93 26.74 30.40 24.19 21.9 Average prey weight (g) 14.93 17.29 19.61 16.1 14.8 Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 6 of 8 agricultural crops, lowlands with maquis vegetation and although potentially available for predation, bats were mountain areas with vineyards and olive trees. Rats con- not taken, and this was probably due to a greater diffi - tributed to the owl’s diet in a variety of habitats, more culty in capturing them compared to other mammalian importantly in mountain areas with pine trees, maquis, prey. Bats have been found in barn owl pellets in the vineyards and olive trees and lowlands with agricultural Mediterranean but Obuch and Benda [21] suggested that crops. there was no specialization to bat hunting by the barn owl in this region although some studies would suggest specialization [52, 55, 56]. Birds were a minor constitu- Discussion ent in barn owl’s diet. Some studies showed an increase Prey diversity and variability in bird predation when other prey species were rare [2, This paper constitutes a novel study of the spatial and 10, 57]. In this study, birds were relatively small-sized temporal feeding habits of the barn owl on Cyprus. Simi- species (Turdus sp., Sturnus sp., Passer sp., Fringillidae), lar studies in the eastern Mediterranean  region have roosting mostly in communal perches [58]. An increased only been known for some islands and terrestrial eco- bird proportion in the diet during the autumn and sum- systems of Greece [10, 28, 45, 46] and a limited number mer months may have reflected an increased availability of sites sampled from Turkey, NW Syria, SW Lebanon, of this prey type, presumably due to the seasonal abun- N Israel, and N Egypt (summarized in [21]). Rodents dance of juveniles which are probably easier to catch [59] have been found to be the most common prey in many and influx of passage migrants. Mediterranean countries (summarized in [28]). Gener- ally, the composition of barn owl diet in Cyprus reflects that of the eastern Mediterranean  area where mammals Temporal and spatial prey use dominate both by number (95.7% in our study vs. 90%, Seasonal trends in the use of the two most important given by [21]) and by composition [similarly constituting prey types suggest a peak in the use of rats in winter and of synanthropic species such as Mus spp., Rattus rattus, a decrease in the other seasons, and an inverse situa- Crocidura suaveolens, Suncus etruscus and birds (Passer tion for Mus peaking in spring and summer. A rat prey domesticus)] [21]. increase in the winter months might be associated to Similarly, to the findings of this study, small mam - increased needs for energy intake by the barn owl [60]. mals comprise the most important prey of the barn owl Relative prey intake may also reflect the availability of worldwide, although the prey composition and diversity the prey species: the reproductive period of mice may varies according to the area [ [1, 2, 19, 20, 41, 47–50]; cease during the colder months [12] whereas this of rats among others]. Among small mammals, two genera of is continuous during most of the year [12, 36]. The activ - rodents were the major prey of the barn owl in Cyprus ity patterns of barn owl and its prey may also play an followed by two genera of insectivores. Kryštufek and important role in its participation in the diet as the barn Vohralík [36] reported only five species of Rodentia owl is mainly a nocturnal predator and its most impor- and two species of Soricidomorpha in Cyprus, being tant prey is active at night. Thus, a low participation of of much lower diversity compared to 15 and 64 spe- species such as Crocidura could be due to their diurnal cies respectively, reported in Turkey. Therefore, the low activity [38]. Nevertheless, shrews constitute of the most mammalian prey diversity in barn owl’s pellets in our important prey types in the transitory Mediterranean cli- study reflects the poor mammal diversity of the island, mate zone of southeastern Bulgaria where also mice and probably explained through the island isolation mecha- rats coexist [48–50]. In this case, most important prey nism [10, 51, 52]. Although rats are considered as the was taken from the predominant dry open cultural land most abundant rodent species on Cyprus [36], in most [48, 50]. The relative importance of shrews may also drop seasons they were less abundant than mice in the diet due to spikes of other small mammal prey such as voles of barn owls. Rats presumably compete with house [49]. Use of rodenticides that cause a decline of the vole mice [53], therefore various factors contributing to the and mice population in farms also caused an increase of local availability of the two species might have resulted shrews as the target prey of barn owls [49]. in their use as prey. Insectivorous mammals have com- An increase in bird use during autumn and summer monly been found as prey for the barn owl [1, 4, 10, may add alternative prey species to compensate for a 48–50, 54]. lower rate of primary prey [7]. It is intriguing that no bats (Chiroptera) were detected In the PCA (Fig.  2), the relationship between habi- in the diet of barn owl in Cyprus. Bats are the second tats and prey types were the most important. The effect most abundant mammalian group in this region (25% of years and seasons was unclear. Mice were important of species, including 17–20 species of bats) [36]. Thus, as prey mostly in lowlands with human activities. This Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 7 of 8 Consent for publication seems to be in accordance with the fact that mice on Not applicable. Cyprus have mostly been recorded in disturbed Medi- terranean shrubby habitat, dominating only areas under Ethics approval and consent to participate During the pellet sampling procedures the birds were not disturbed in their intensive agriculture [36]. The association of shrews natural environment. (and birds) to lowlands reflects inhabitants of various open habitats where the barn owl prefers to hunt [50]. Funding The collection of material in the field was supported by the Game and Fauna Nevertheless, these prey types can be taken from higher Service, Ministry of the Interior, Nicosia, Cyprus and Cyprus Association for latitudes where probably are available. The dominance the Protection of Avifauna, Pafos, Cyprus. The analysis of the material was of rats mostly in the samples from mountainous areas supported by the Department of Zoology, School of Biology, University of Thessaloniki, Greece. seems to reflect the fact that their most important habitat on Cyprus is dense vegetation and plantations while also Publisher’s Note shrub cover is essential [36]. Springer Nature remains neutral with regard to jurisdictional claims in pub- lished maps and institutional affiliations. Conclusions Received: 6 February 2018 Accepted: 23 May 2018 The barn owl prey species diversity in Cyprus was low, with variations in the main rodent prey that could be explained by their abundance, distribution, seasonal activity and habitat preferences. The composition of References prey indicates an opportunistic foraging behavior that is 1. Taylor I. Barn owls. Predator-prey relationships and conservation. Cam- bridge: University Press; 1994. also reported for many of other eastern Mediterranean 2. Bose M, Guidali F. Seasonal and geographic differences in the diet populations studied. Each population seems to respond of the barn owl in an agro-ecosystem in northern Italy. J Raptor Res. accordingly to its unique features and may either adopt 2001;35:240–6. 3. Rasoma J, Goodman SM. Food habits of the barn owl (Tyto alba) in opportunistic feeding habits in response to prey availabil- spiny bush habitat of arid southwestern Madagascar. J Arid Environ. ity or prey selectivity. Further research conducted on the 2007;69:537–43. prey population dynamics and biogeography in Cyprus 4. Bunn DS, Warburton AB, Wilson RDS. The barn owl. Calton: T & AD Poyser; could clarify the seasonal and spatial foraging traits of 5. Tores M, Yom-Tov Y. The diet of the barn owl Tyto alba in the Negev this nocturnal raptor. Desert. Israel J Zool. 2003;49:233–6. 6. Pavey CR, Gorman J, Heywood M. Dietary overlap between the nocturnal letter-winged kite Elanus scriptus and barn owl Tyto alba during a rodent Abbreviations outbreak in arid Australia. J Arid Environ. 2008;72:2282–6. PCA: principal components analysis; asl: above sea level. 7. Carmona ER, Rivadeneira MM. Food habits of the barn owl Tyto alba in the National Reserve Pampa del Tamarugal, Atacama Desert, North Chile. Authors’ contributions J Nat Hist. 2006;40:473–83. MM and MC collected and analyzed the material, data and wrote the paper 8. Capizzi D, Luiselli L. Comparison of the trophic niche of four sympatric being the main part of their B.Sc. dissertations carried out in the School of owls (Asio otus, Athene noctua, Strix aluco and Tyto alba) in Mediterranean Biology, University of Thessaloniki, Greece. VG supervised the planning and central Italy. Ecol Mediterr. 1995;21:13–20. execution of the field and laboratory work and had a major contribution in 9. Marti CD. Raptor food habits studies. In: Giron Pendleton BA, Millsap BA, writing the manuscript. NK and SI guided the field visits and collection of Cline KW, Bird DM, editors. Raptor management techniques manual. the material and contributed to writing of the paper. All authors read and Washington DC: Nat Wildl Fed; 1987. p. 69–80 (Tech Series No 10). approved the final manuscript. 10. Alivizatos H, Goutner V, Zogaris S. Contribution to the study of the diet of four owl species (Aves, Strigiformes) from mainland and island areas of Author details Greece. Belg J Zool. 2005;135:109–18. School of Biology, Aristotle University of Thessaloniki (AUTH), 541 24, Thessa- 11. Leader Z, Yom-Tov Y, Motro U. Diet comparison between two sympatric loniki, Greece. Game and Fauna Service, Ministry of the Interior, 1453 Nicosia, owls -Tyto alba and Asio otus—in the Negev Desert, Israel. Isr J Ecol Evol. Cyprus. Cyprus Association for the Protection of Avifauna, Kalamatas 10 Str., 2010;56:207–16. 8047 Pafos, Cyprus. 12. Nadeem MS, Imran SMK, Mahmood T, Kayani AR, Shah SI. A compara- tive study of the diets of barn owl (Tyto alba) and spotted owlet (Athene Acknowledgements brama) inhabiting Ahmadpur East, Southern Punjab, Pakistan. Anim Biol. The authors thank K. Demetriou, K. Nicolaou, P.Prastides, L. Leantrou and H. 2012;62:13–28. Hadjistylis (Game and Fauna Service) and H. Nicolaou (Forestry Department) 13. Derting TL, Cranford JA. Physical and behavioral correlates of prey vulner- who have contributed in pellet sampling. Also thanks to Robert Patchett ability to barn owl (Tyto alba) predation. Am Midl Nat. 1989;121:11–20. (University of St. Andrews) and Adrian Wright ( Thessaloniki) for checking 14. Muñoz-Pedreros A, Murúa R. Control of small mammals in a pine planta- the spelling and grammar of this article. University Studio Press, Thessaloniki tion (central Chile) by modification of the habitat of predators (Tyto alba, constructed the map included in this paper. Strigiformes and Pseudalopex sp., Canidae). Acta Oecol. 1990;11:251–61. 15. Yom-Tov Y, Wool D. Do the contents of barn owl pellets accurately repre- Competing interests sent the proportion of prey species in the field? Condor. 1997;99:972–6. The authors declare that they have no competing interests. 16. Muñoz-Pedreros A, Gil C, Yáñez J, Rau JR. Raptor habitat management and its implication on the biological control of the Hantavirus. Eur J Wildl Availability of data and materials Res. 2010;56:703–15. Data were adequately presented in the manuscript. For data requests contact 17. Muñoz-Pedreros A, Gil C, Yáñez J, Rau JR, Möller P. Trophic ecology of the authors (MM and MC). two raptors, barn owl (Tyto alba) and white-tailed kite (Elanus leucurus), Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 8 of 8 and possible implications for biological control of Hantavirus reservoir in 42. Hill MO. Diversity and evenness: a unifying notation and its conse- Chile. Wilson J Ornithol. 2016;128:391–403. quences. Ecology. 1973;54:427–32. 18. Tores M, Motro Y, Motro U, Yom-Tov Y. The barn owl—a selective oppor- 43. Alatalo RV. Problems in the measurement of evenness in ecology. Oikos. tunist predator. Israel J Zool. 2005;51:349–60. 1981;37:199–204. 19. Herrera CM. Trophic diversity of the barn owl Tyto alba in continental 44. Peres-Neto PR, Jackson DA, Somers KM. How many principal compo- western Europe. Ornis Scand. 1974;5:181–91. nents? Stopping rules for determining the number of non-trivial axes 20. Álvarez-Castañeda ST, Cárdenas N, Méndez L. Analysis of mammal revisited. Comput Stat Data An. 2005;49:974–97. remains from owl pellets (Tyto alba), in a suburban area in Baja California. 45. Alivizatos H, Goutner V. Winter diet of the barn owl (Tyto alba) and long- J Arid Environ. 2004;59:59–69. eared Owl (Asio otus) in northeastern Greece: a comparison. J Raptor Res. 21. Obuch J, Benda P. Food of the barn owl (Tyto alba) in the eastern Mediter- 1999;33:160–3. ranean. Slovak Rapt J. 2009;3:41–50. 46. Alivizatos H, Goutner V, Athanasiadis A, Poirazidis K. Comparative tempo- 22. Birdlife International. Data zone; 2015. http://dataz one.birdl ife.org/speci ral prey use by barn owl (Tyto alba) and little owl (Athene noctua) in the es/facts heet/commo n-barn-owl-Tyto-alba. Accessed 20 Nov 2016. Evros Delta, northeastern Greece. J Biol Res Thessalon. 2006;6:177–86. 23. Agrolife Project. http://agrol ife.eu. Accessed 4 Oct 2015. 47. Ali MSA, Santhanakrishnan R. Diet composition of the barn owl Tyto 24. Kassinis N, Roulin A. Reproduction of the barn owl (Tyto alba) in Cyprus alba (Aves: Tytonidae) and spotted owlet Athene brama (Aves: Strigidae) (Aves: strigiformes). Zool Middle East. 2017;63:369–71. coexisting in an urban environment. Podoces. 2012;7:21–32. 25. Angelici FM, Latella L, Luiselli L, Riga F. The summer diet of the little owl 48. Miltschev B, Boev Z, Georgiev V. Food of the Barn Owl (Tyto alba) in south- (Athene noctua) on the island of Astipalaia (Dodecanese, Greece). J Raptor eastern Bulgaria. Egretta. 2004;47:66–77 (in German). Res. 1997;31:280–2. 49. Miltschev B, Georgiev V. Influence of vole population peaks and the use 26. Nature Conservation Unit. Virtual Biodiversity Museum of Cyprus; 2012. of rodenticides on the diet of barn owl Tyto alba (Scopoli 1769) during http://www.natur emuse um.org.cy/lang1 /habit ats.html. Accessed 5 Jan the breeding season in south-east Bulgaria. Egretta. 2009;50:82–7 (in 2017. German). 27. Marti CD. Feeding ecology of four sympatric owls. Condor. 1974;76:45–61. 50. Milchev B. Dietary comparison of coexisting barn owl (Tyto alba) and 28. Goutner V, Alivizatos H. Diet of the barn owl (Tyto alba) and little owl eagle owl (Bubo bubo) during consecutive breeding seasons. Anim Biol. (Athene noctua) in wetlands of northeastern Greece. Belg J Zool. 2016;66:219–28. 2003;133:15–22. 51. Jaksic FM. Trophic structure of some Nearctic, Neotropical and Palearctic 29. Balčiauskienė L. Analysis of tawny owl (Strix aluco) food remains as owl assemblages: potential roles of diet opportunism, interspecific inter - a tool for long-term monitoring of small mammals. Acta Zool Litu. ference and resource depression. J Raptor Res. 1988;22:44–52. 2005;15:85–9. 52. Sommer R, Zoller H, Kock D, Böhme W, Griesau A. Feeding of the barn 30. Andrade A, Saraiva de Menezes JF, Monjeau A. Are owl pellets good owl, Tyto alba with first record of the European free-tailed bat, Tadarida estimators of prey abundance? J King Saud Univ-Sci. 2016;28:239–44. teniotis on the island of Ibiza (Spain, Balearics). Folia Zool. 2005;54:364–70. 31. Iezekiel S, Bakaloudis DE, Vlachos CG. The diet of the Bonelli’s eagle 53. Landová E, Horáček I, Frynta D. Have black rats evolved a culturally-trans- Hieraaetus fasciatus in Cyprus. In: Chancellor RD, Meyburg BU, editors. In: mitted technique of pinecone opening independently in Cyprus and Raptors worldwide: proceedings of the VI world conference on birds of Israel? Isr J Ecol Evol. 2006;52:151–8. prey and owls. Berlin: World Working Group on Birds of Prey/MME; 2004. 54. Purger JJ. Survey of the small mammal fauna in north-western Somogy p. 581–87. county (Hungary), based on barn owl Tyto alba (Scopoli, 1769) pellet 32. Seçkin S, Coşkun Y. Mammalian remains in the pellets of long-eared owls analysis. Nat Somogy. 2014;24:293–304. (Asio otus) in Diyarbakır province. Turk J Zool. 2006;30:271–8. 55. Pieper H. Fledermäuse aus Schleiereulen-Gewöllen von der Insel Kreta. Z 33. Marchesi L, Sergio F, Pedrini P. Costs and benefits of breeding in human- Säugetierkd. 1977;42:7–12. altered landscapes for the eagle owl Bubo bubo. Ibis. 2002;144:164–77. 56. Benda P, Andreas M, Kock D, Lučan RK, Munclinger P, Nová P, et al. 34. Lawrence MJ, Brown RW. Mammals of Britain: their tracks, trails and signs. Bats (Mammalia: Chiroptera) of the eastern Mediterranean Part 4: bat London: Blandford Press; 1967. fauna of Syria: distribution, systematics, ecology. Acta Soc Zool Bohem. 35. Brown R, Ferguson J, Lawrence M, Lees D. Track and signs of the birds of 2006;70:1–329. Britain and Europe. London: Helm; 1987. 57. Santhanakrishnan R, Ali AHMS, Anbarasan U. Diet variations of the barn 36. Kryštufek B, Vohralík V. Mammals of Turkey and Cyprus: Rodentia II: owl Tyto alba (Scopoli, 1769) in Madurai District, Tamil Nadu, southern Cricetinae, Muridae, Spalacidae, Calomyscidae, Capromyidae, Hystricidae, India. Podoces. 2010;5:95–103. Castoridae. Koper: Založba Annales; 2009. 58. Obuch J, Khaleghizadeh A. Spatial variation in the diet of the barn owl 37. Perrins C. Birds of Britain and Europe (New Generation Guides). London: Tyto alba in Iran. Podoces. 2011;6:103–16. Collins; 1987. 59. Kafkaletou-Diez A, Tsachalidis EP, Poirazidis K. Seasonal variation in the 38. MacDonald D, Barret P. Mammals of Britain and Europe. London: Collins; diet of the long-eared owl (Asio otus) in a northeastern agricultural area 1993. of Greece. J Biol Res Thessalon. 2008;10:181–9. 39. R Core Team. R: a language and environment for statistical computing. 60. Bontzorlos VA, Peris SJ, Vlachos CG, Bakaloudis DE. Barn owl Tyto alba prey Vienna: R Foundation for Statistical Computing. Computing; 2015. in Thessaly, and evaluation of barn owl diets throughout Greece. Ardea. 40. Shannon CE, Weaver W. The mathematical theory of communications. 2009;97:625–30. Urbana: University of Illinois Press; 1963. 41. Marks JS, Marti CD. Feeding ecology of sympatric barn owls and long- eared owls in Idaho. Ornis Scand. 1984;15:135–43. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Biological Research-Thessaloniki Springer Journals

Spatial and temporal patterns in the diet of barn owl (Tyto alba) in Cyprus

Free
8 pages
Loading next page...
 
/lp/springer_journal/spatial-and-temporal-patterns-in-the-diet-of-barn-owl-tyto-alba-in-C4LnJeFSyF
Publisher
BioMed Central
Copyright
Copyright © 2018 by The Author(s)
Subject
Life Sciences; Life Sciences, general
eISSN
2241-5793
D.O.I.
10.1186/s40709-018-0080-8
Publisher site
See Article on Publisher Site

Abstract

Background: The barn owl, a nocturnal raptor with cosmopolitan distribution, shows a great adaptability to differ - ent environments. Regarding prey, the barn owl is a rather selective species, but if changes in the abundance of the selected prey occur, it becomes an opportunistic predator and easily incorporates other prey in its diet, using a wide range of prey species and foraging habitats. Small rodents are usually the prey mostly used. Compared to the popula- tions of north and eastern Europe, barn owl populations in the Mediterranean area have been the least studied. In Cyprus, where barn owl is a common bird species, there are no studies on its diet and feeding ecology. This study was carried out to contribute to the spatial and temporal patterns barn owl diet in Cyprus also providing information on small mammals’ presence and species composition on the island. Methods: This study was based on 1407 regurgitated pellet analysis that were collected from 26 sites representing six major habitat types on central and southern Cyprus from summer 2013 to summer 2014. The diet of the barn owl was described in terms of seasonal average biomass and numerical percentages of each prey species and com- pared by Kruskal–Wallis test. Seasonal prey diversity and evenness indices were also calculated. Principal component analysis (PCA) was performed on the prey biomass proportion data assigned to six major habitat types with regard to elevation, vegetation and human uses. Results: Low prey diversity was found comprised mainly of rodents (overall means 96.2 and 95.7% by number and biomass, respectively). Mice followed by rats were most important prey whereas insectivores, birds and insects were minor components of the owl’s diet. Evenness and diversity values were relatively similar among seasons. PCA differentiated mainly between lowland areas where mice were more abundant prey and mountainous areas where rats dominated in the diet. Insectivores correlated with birds, prey types characterizing several lowland and highland habitats. Conclusions: The barn owl prey composition in Cyprus suggests an opportunistic foraging behavior, low prey spe- cies diversity with variations in the main rodent prey that could be explained by their distribution, seasonal activity and habitat preferences. Keywords: Barn owl, Cyprus, Feeding ecology, Tyto alba Background food supply and refuge and enables it to inhabit areas The barn owl ( Tyto alba (Scopoli, 1769); order Strigi- such as Negev desert, Israel [5], Simpson desert, Aus- formes) is a nocturnal raptor with cosmopolitan dis- tralia [6] and Atacama desert, Chile [7]. The barn owl tribution, being common in the temperate and tropical shows a great adaptability to different environments zones of the world [1–3]. It exhibits low resistance to explaining its cosmopolitan distribution [7]. As a con- cold [4]. Its presence in arid environments depends on sequence, use of a wide range of prey species [1, 2] and foraging habitats [8] have been reported. Although for- aging opportunism, that is use of a wide range of prey *Correspondence: vgoutner@bio.auth.gr 1 species depending on their availability, has been sug- School of Biology, Aristotle University of Thessaloniki (AUTH), 541 24, Thessaloniki, Greece gested as a common behaviour exhibited by the species Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 2 of 8 [7, 9–12], it has also been indicated that barn owl is an The locations sampled are presented below. The respec - A selective predator, so its diet does not represent the tive names are indicated in Fig. 1. true abundance of prey in the wild [13–17]. According to Tores et  al. [18] and Muñoz-Pedreros et  al. [17] the Group 1. Mountain with Pinus brutia pine forests barn owl cannot be defined as a pure opportunist or a and maquis pure selective hunter. This strategy of flexible hunting Apliki makes the barn owl a very successful predator, explain- A nest was found in a Quercus alnifolia zone, with pines ing its wide cosmopolitan distribution and the ability and maquis (1000 m asl). to colonize new environments, a plastic diet strategy much greater than that of most other species of raptors. Potamitissa In conclusion, barn owl is a rather selective species, but A natural nest was found in a cavity of an oriental plane if changes in the abundance of the selected prey occur, tree in a clump of trees (alders, plane, pine and olive it becomes an opportunistic predator and easily incor- trees) and scattered low vegetation of thorny shrubs porates other prey to its diet even prey of low energy (820 m asl). value [19], remaining in its territory even when the selected prey types decrease [17]. The barn owl feeds Athrakos mainly on small mammals (7–24  g), probably without An artificial nest placed on a pine tree was in use and pel - discriminating between large and small prey [20]. In lets were collected from a nearby roost. Sparse vegetation the Mediterranean region, a combination of suitable with Cistus shrubs and some arable land surrounded the climatic conditions and long-term human presence has sites (676 m asl). favoured the establishment of this species, supporting relatively high population densities [21]. Compared to Prastio Kellakiou the populations in north and eastern Europe, those in An artificial nest was in use placed in a hilly area covered the Mediterranean area have been the least studied [8]. with a variety of natural vegetation, such as Quercus alni- Barn owl is a common resident in Cyprus and its folia, Cistus sp., Eucalyptus sp., fruit and pine trees, and population is estimated at 250–750 breeding pairs cypress trees (490 m asl). (these estimates are conservative) [22]. AGROLIFE project [23] in cooperation with Game and Fauna Pelentri Service explored an alternative to rodenticide rodent An artificial nest was in use situated on a pine tree in an control via use of barn owl nesting boxes. In Cyprus, area of scarce pine trees, Quercus alnifolia, Cistus sp. and information on the breeding ecology and trends of the fruit trees (800 m asl). barn owl is limited [24], whereas there are no studies on its diet and feeding ecology. Similarly, very few such Lefkara studies occur in the eastern Mediterranean [10, 25]. An artificial nest was in use situated under a bridge in The aim of the present study was (a) to contribute an area surrounded with pine trees, cypresses trees and to the spatial and temporal patterns barn owl diet in reedbeds (430 asl). Cyprus, providing information lacking so far; (b) based on prey use of the owl, to provide data on the presence Group 2. Lowlands with agricultural crops and species composition of small mammals on the Avdimou island, where relevant information is scarce. An artificial nest on a pine tree in a lowland area was in use. Reedbeds surrounded the area (380 m asl). Another Methods artificial nest placed in the same area on an electric The study area power pole was also in use. Cyprus (35°00′N, 33°00′E), is the third largest island in the Mediterranean Sea  covering an area of 9250  km Paramali (Fig.  1). The location of the island, with Africa to the An artificial nest in use was situated on a cypress tree on south, Turkey and central Europe to the north and the cultivated land (20 m asl). Middle East to the east, is very important for the avifauna of the island. Cyprus includes a diversity of habitats such Agios Dimitrianos (Episkopi) as sand dunes and rocky coastline, wetlands, streams Two nests were located on pine trees surrounded by cul- and lakes, scrubland, agricultural land (e.g. cereal fields, tivations, scattered pines and fruit trees (23 m asl). orchards, vineyards), desert-like uncultivated or rocky land, and forests (mostly pine forests) [26]. Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 3 of 8 Fig. 1 Map of Cyprus indicating the sampling sites of barn owl pellets. Sampling sites have been assigned to groups according to habitat type (1–6) Pareklisia Group 3. Hilly areas with crops and livestock facilities A roost site was found in a rocky area near habitations, Kofinou sparse vegetation and cultivations with Pistacia lenticus. An artificial nest in use was placed near livestock areas. The surrounding vegetation was composed of culti - vated trees (mainly almond) and low shrubs (169 m asl). Avdellero A nest was placed under a bridge within a livestock graz- ing area (135 m asl). Anglisides An artificial nest and roost sites in use were under a Achelia stone-built bridge. Reedbeds, acacias and olive trees Four artificial nests placed on cultivated land were in use were the most important vegetation around this site (35 asl). (174 m asl). Timi Klavdia An artificial nest in use was situated in a forest sur - An artificial nest was in use was placed under a bridge. rounded by cultivations and low vegetation at about sea The surrounding habitat was similar to Anglisides (170 m level. asl). Kellia Makounta An artificial nest in use was placed under a bridge in an A nest was found in a craggy mountainous area. The area with riparian vegetation of reedbeds and acacias surrounding habitat was dominated by agricultural and (55 m asl). tree cultivations (100 m asl). Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 4 of 8 Panagia Aimatousa Data analysis A roost site was located near livestock facilities in an area The pellets were analyzed using reference books [34– surrounded by olive trees. 36], but excluding those that contained only hair. Mean weight of each prey taxon was taken from the literature [37, 38]. Mice of the genus Mus and rats Rattus were not Group 4. Areas with dry vegetation identified at the species level because it was impossible One roost site was found near Zodia (85 asl) and three to distinguish them by cranial characters. Although their at Pano Koutrafas (241  m asl), in dry craggy areas with identification could be possible through DNA analysis of bushes, acacias and some fruit tree cultivations. hair found in the pellets, this approach was beyond the scope of the present study. Rats most likely belonged to Group 5. Mountainous areas with vineyards and olive trees the species Rattus rattus as the presence of Rattus nor- Trachypedoula vegicus on Cyprus is dubious [36]. Insects were iden- A roost was found on a stone-built bridge. The surround - tified at the level of family due to the poor condition ing area included vineyards, olive cultivations and bush- of their remains in the pellets. The diet of the barn owl land (500 m asl). was described in terms of seasonal average biomass and numerical percentages of each prey species. Average prey Vretsia weight of each species in each period was estimated by Two nests were located in deserted buildings in a village. multiplying the numbers of each prey item by its mean Nearby areas were covered with vineyards and citrus weight, adding the weights produced and dividing the fruit cultivations (500 m asl). sum by the total numbers of prey in each sample. The diet of barn owl was analysed for each field sample in terms of Group 6. Lowlands with maquis vegetation numbers and biomass. Median prey weights were com- Kouklia pared among different seasons by Kruskal–Wallis test. Roosts were located on a bridge and nearby areas sur- These tests were performed using R [39] and Statistica rounded with maquis and olive and carob trees. version 7.0 (StatSoft, Tulsa, USA) softwares. The prey diversity was estimated at a class level (mammals, birds, Pellet collection insects) by using the antilog of the Shannon-Weiner Available evidence indicates that pellet analysis is still index [40, 41], while the evenness index for the mammals the most suitable method for studying the diet of owls was calculated by using the Hill’s ratio [42, 43]. especially the medium sized ones [9, 27, 28]. Analys- The prey types were assigned to six major habitat types ing a small sample of pellets can give adequate informa- with regard to elevation, vegetation and human uses tion about prey composition in the field and it takes less (Fig.  1). Principal component analysis was performed on working hours than mammal trapping [29, 30]. Despite the prey biomass proportions data from the six habitat the controversy whether pellets represent the true com- types. The analysis showed that 99.6% of the variation in munity structure of the prey [15], pellets can give infor- the dataset was explained by the first three components mation about prey-species communities and other while the first two components explain 77.9% of the vari - biogeographic data [1, 31, 32]. Pellets are relatively easy ance in the data. Only the first 2 components were con - to find and small bones remain well preserved within sidered in the analysis based on the Kaiser stopping rule, them [2]. Pellet analysis is a useful tool for the manage- i.e. the number of components with eigenvalues over 1 ment and protection of owl species and their habitats [1] [44]. while the outcome from the analysis can be used to assess ecosystem health [2, 33]. Results Pellets were collected at the end of every season for Prey composition and seasonal variation in barn owl’s diet 1  year, from summer 2013 to summer 2014. They were In a total of 1407 pellets analyzed during the study, 3312 collected from natural nests (situated at old buildings, prey items were identified (mean 2.35 prey items per pel - tree cavities and under bridges) and nesting boxes placed let, ranging from 1 to 8). The diet of the species was made and monitored by the Game and Fauna Service. The nests up almost exclusively of small mammals, both in num- were located at a variety of habitats, including coastal ber and biomass (overall means 96.2 and 95.7%, respec- areas, lowlands (0–500 m elevation) and mountain areas tively) (Table 1). Of the small mammals, mice (Mus spp.) (above 500 m elevation) with different types of vegetation dominated the owl’s diet both by numbers and biomass (see above for a detailed presentation of the localities). in most seasons, followed by rats (Rattus spp.) with their relative proportions varying seasonally (Table 1). Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 5 of 8 Lesser White-toothed shrew (Crocidura suaveo- lens), though numerically higher than rats in summer and autumn of 2013, were much less important by bio- mass due to their small size. The numerical distribution of these three major prey types differed significantly through the study period (Kruskal–Wallis χ = 69.638, df = 13, p < 0.0001). Etruscan shrew (Suncus etruscus) was of minor importance among the mammalian prey present in proportions being highest in summer 2013 and relatively similar in the other seasons (Table 1). Βirds were found in low proportions in the diet (2.6–6.0% by biomass) whereas insects were unimportant as prey (Table  1). Evenness and diversity values were relatively similar among seasons with spring and summer 2014 evenness values being lowest (Table 1). Spatial variation in barn owl’s diet PCA biplot (Fig.  2) shows the correlations among prey types and also the habitat and temporal variation in barn owl’s diet. Mice showed a positive correlation with insects and slight to negative correlations to other prey types, particularly rats that were slightly positively cor- related only to birds. Etruscan and lesser white-toothed Fig. 2 Biplot containing the first two principal components presenting the differentiation of barn owl prey according to shrews and birds were very highly positively correlated habitat. Symbol meaning: 1: Mountain with pine trees and maquis; with each other and negatively correlated with insects. 2: Lowlands with agricultural crops; 3: Hilly areas with crops and Mice and insects were mostly involved in the owl’s diet in livestock facilities; 4: Areas with dry vegetation; 5: Mountain hilly areas with crops and livestock facilities, areas with areas with vineyards and olive trees; 6: Lowlands with maquis dry vegetation, and lowlands with agricultural crops in vegetation. Different colours denote the 5 different sampling periods during 2013–2014. A Autumn, W Winter, S Spring, U Summer (i.e. both years and across seasons. Nevertheless, insects were 2A13 = Samples from lowlands with agricultural crops during autumn not an important prey category (as shown in Table  1). of 2013) Shrews and birds were more important in lowlands with Table 1 Seasonal diet of barn owl in Cyprus in % numbers (N) and % biomass (B), from summer 2013 to summer 2014 Prey type Summer 2013 Autumn 2013 Winter 2013–2014 Spring 2014 Summer 2014 N B N B N B N B N B Insects 2.7 0.1 1.3 0.1 0.4 0.1 0.4 0.1 – – Birds 1.8 3.0 4.2 5.8 3.0 3.8 1.7 2.6 3.5 6.0 Mammals 95.5 96.9 94.5 94.1 96.6 96.1 97.9 97.3 96.5 94.0 Mice (Mus spp.) 64.6 52.0 70.4 48.8 72.2 44.2 76.9 57.2 76.9 62.3 Rats (Rattus spp.) 9.1 36.4 11.9 41.4 16.2 49.5 9.7 36.3 6.6 27.0 Lesser White-toothed shrew (Croci- 20.8 8.4 10.7 3.7 7.5 2.3 9.6 3.6 11.0 4.4 dura suaveolens) Etruscan shrew (Suncus etruscus) 0.9 0.1 1.5 0.2 0.7 0.1 1.7 0.2 2.0 0.3 Total number of prey 331 – 1063 – 759 – 934 – 225 – Prey diversity 1.24 1.28 1.18 1.12 1.16 Evenness 0.69 0.71 0.70 0.58 0.60 Median prey weight (g) 4.86 3.73 2.45 2.30 1.49 Interquartile range: 25–75% 22.93 26.74 30.40 24.19 21.9 Average prey weight (g) 14.93 17.29 19.61 16.1 14.8 Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 6 of 8 agricultural crops, lowlands with maquis vegetation and although potentially available for predation, bats were mountain areas with vineyards and olive trees. Rats con- not taken, and this was probably due to a greater diffi - tributed to the owl’s diet in a variety of habitats, more culty in capturing them compared to other mammalian importantly in mountain areas with pine trees, maquis, prey. Bats have been found in barn owl pellets in the vineyards and olive trees and lowlands with agricultural Mediterranean but Obuch and Benda [21] suggested that crops. there was no specialization to bat hunting by the barn owl in this region although some studies would suggest specialization [52, 55, 56]. Birds were a minor constitu- Discussion ent in barn owl’s diet. Some studies showed an increase Prey diversity and variability in bird predation when other prey species were rare [2, This paper constitutes a novel study of the spatial and 10, 57]. In this study, birds were relatively small-sized temporal feeding habits of the barn owl on Cyprus. Simi- species (Turdus sp., Sturnus sp., Passer sp., Fringillidae), lar studies in the eastern Mediterranean  region have roosting mostly in communal perches [58]. An increased only been known for some islands and terrestrial eco- bird proportion in the diet during the autumn and sum- systems of Greece [10, 28, 45, 46] and a limited number mer months may have reflected an increased availability of sites sampled from Turkey, NW Syria, SW Lebanon, of this prey type, presumably due to the seasonal abun- N Israel, and N Egypt (summarized in [21]). Rodents dance of juveniles which are probably easier to catch [59] have been found to be the most common prey in many and influx of passage migrants. Mediterranean countries (summarized in [28]). Gener- ally, the composition of barn owl diet in Cyprus reflects that of the eastern Mediterranean  area where mammals Temporal and spatial prey use dominate both by number (95.7% in our study vs. 90%, Seasonal trends in the use of the two most important given by [21]) and by composition [similarly constituting prey types suggest a peak in the use of rats in winter and of synanthropic species such as Mus spp., Rattus rattus, a decrease in the other seasons, and an inverse situa- Crocidura suaveolens, Suncus etruscus and birds (Passer tion for Mus peaking in spring and summer. A rat prey domesticus)] [21]. increase in the winter months might be associated to Similarly, to the findings of this study, small mam - increased needs for energy intake by the barn owl [60]. mals comprise the most important prey of the barn owl Relative prey intake may also reflect the availability of worldwide, although the prey composition and diversity the prey species: the reproductive period of mice may varies according to the area [ [1, 2, 19, 20, 41, 47–50]; cease during the colder months [12] whereas this of rats among others]. Among small mammals, two genera of is continuous during most of the year [12, 36]. The activ - rodents were the major prey of the barn owl in Cyprus ity patterns of barn owl and its prey may also play an followed by two genera of insectivores. Kryštufek and important role in its participation in the diet as the barn Vohralík [36] reported only five species of Rodentia owl is mainly a nocturnal predator and its most impor- and two species of Soricidomorpha in Cyprus, being tant prey is active at night. Thus, a low participation of of much lower diversity compared to 15 and 64 spe- species such as Crocidura could be due to their diurnal cies respectively, reported in Turkey. Therefore, the low activity [38]. Nevertheless, shrews constitute of the most mammalian prey diversity in barn owl’s pellets in our important prey types in the transitory Mediterranean cli- study reflects the poor mammal diversity of the island, mate zone of southeastern Bulgaria where also mice and probably explained through the island isolation mecha- rats coexist [48–50]. In this case, most important prey nism [10, 51, 52]. Although rats are considered as the was taken from the predominant dry open cultural land most abundant rodent species on Cyprus [36], in most [48, 50]. The relative importance of shrews may also drop seasons they were less abundant than mice in the diet due to spikes of other small mammal prey such as voles of barn owls. Rats presumably compete with house [49]. Use of rodenticides that cause a decline of the vole mice [53], therefore various factors contributing to the and mice population in farms also caused an increase of local availability of the two species might have resulted shrews as the target prey of barn owls [49]. in their use as prey. Insectivorous mammals have com- An increase in bird use during autumn and summer monly been found as prey for the barn owl [1, 4, 10, may add alternative prey species to compensate for a 48–50, 54]. lower rate of primary prey [7]. It is intriguing that no bats (Chiroptera) were detected In the PCA (Fig.  2), the relationship between habi- in the diet of barn owl in Cyprus. Bats are the second tats and prey types were the most important. The effect most abundant mammalian group in this region (25% of years and seasons was unclear. Mice were important of species, including 17–20 species of bats) [36]. Thus, as prey mostly in lowlands with human activities. This Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 7 of 8 Consent for publication seems to be in accordance with the fact that mice on Not applicable. Cyprus have mostly been recorded in disturbed Medi- terranean shrubby habitat, dominating only areas under Ethics approval and consent to participate During the pellet sampling procedures the birds were not disturbed in their intensive agriculture [36]. The association of shrews natural environment. (and birds) to lowlands reflects inhabitants of various open habitats where the barn owl prefers to hunt [50]. Funding The collection of material in the field was supported by the Game and Fauna Nevertheless, these prey types can be taken from higher Service, Ministry of the Interior, Nicosia, Cyprus and Cyprus Association for latitudes where probably are available. The dominance the Protection of Avifauna, Pafos, Cyprus. The analysis of the material was of rats mostly in the samples from mountainous areas supported by the Department of Zoology, School of Biology, University of Thessaloniki, Greece. seems to reflect the fact that their most important habitat on Cyprus is dense vegetation and plantations while also Publisher’s Note shrub cover is essential [36]. Springer Nature remains neutral with regard to jurisdictional claims in pub- lished maps and institutional affiliations. Conclusions Received: 6 February 2018 Accepted: 23 May 2018 The barn owl prey species diversity in Cyprus was low, with variations in the main rodent prey that could be explained by their abundance, distribution, seasonal activity and habitat preferences. The composition of References prey indicates an opportunistic foraging behavior that is 1. Taylor I. Barn owls. Predator-prey relationships and conservation. Cam- bridge: University Press; 1994. also reported for many of other eastern Mediterranean 2. Bose M, Guidali F. Seasonal and geographic differences in the diet populations studied. Each population seems to respond of the barn owl in an agro-ecosystem in northern Italy. J Raptor Res. accordingly to its unique features and may either adopt 2001;35:240–6. 3. Rasoma J, Goodman SM. Food habits of the barn owl (Tyto alba) in opportunistic feeding habits in response to prey availabil- spiny bush habitat of arid southwestern Madagascar. J Arid Environ. ity or prey selectivity. Further research conducted on the 2007;69:537–43. prey population dynamics and biogeography in Cyprus 4. Bunn DS, Warburton AB, Wilson RDS. The barn owl. Calton: T & AD Poyser; could clarify the seasonal and spatial foraging traits of 5. Tores M, Yom-Tov Y. The diet of the barn owl Tyto alba in the Negev this nocturnal raptor. Desert. Israel J Zool. 2003;49:233–6. 6. Pavey CR, Gorman J, Heywood M. Dietary overlap between the nocturnal letter-winged kite Elanus scriptus and barn owl Tyto alba during a rodent Abbreviations outbreak in arid Australia. J Arid Environ. 2008;72:2282–6. PCA: principal components analysis; asl: above sea level. 7. Carmona ER, Rivadeneira MM. Food habits of the barn owl Tyto alba in the National Reserve Pampa del Tamarugal, Atacama Desert, North Chile. Authors’ contributions J Nat Hist. 2006;40:473–83. MM and MC collected and analyzed the material, data and wrote the paper 8. Capizzi D, Luiselli L. Comparison of the trophic niche of four sympatric being the main part of their B.Sc. dissertations carried out in the School of owls (Asio otus, Athene noctua, Strix aluco and Tyto alba) in Mediterranean Biology, University of Thessaloniki, Greece. VG supervised the planning and central Italy. Ecol Mediterr. 1995;21:13–20. execution of the field and laboratory work and had a major contribution in 9. Marti CD. Raptor food habits studies. In: Giron Pendleton BA, Millsap BA, writing the manuscript. NK and SI guided the field visits and collection of Cline KW, Bird DM, editors. Raptor management techniques manual. the material and contributed to writing of the paper. All authors read and Washington DC: Nat Wildl Fed; 1987. p. 69–80 (Tech Series No 10). approved the final manuscript. 10. Alivizatos H, Goutner V, Zogaris S. Contribution to the study of the diet of four owl species (Aves, Strigiformes) from mainland and island areas of Author details Greece. Belg J Zool. 2005;135:109–18. School of Biology, Aristotle University of Thessaloniki (AUTH), 541 24, Thessa- 11. Leader Z, Yom-Tov Y, Motro U. Diet comparison between two sympatric loniki, Greece. Game and Fauna Service, Ministry of the Interior, 1453 Nicosia, owls -Tyto alba and Asio otus—in the Negev Desert, Israel. Isr J Ecol Evol. Cyprus. Cyprus Association for the Protection of Avifauna, Kalamatas 10 Str., 2010;56:207–16. 8047 Pafos, Cyprus. 12. Nadeem MS, Imran SMK, Mahmood T, Kayani AR, Shah SI. A compara- tive study of the diets of barn owl (Tyto alba) and spotted owlet (Athene Acknowledgements brama) inhabiting Ahmadpur East, Southern Punjab, Pakistan. Anim Biol. The authors thank K. Demetriou, K. Nicolaou, P.Prastides, L. Leantrou and H. 2012;62:13–28. Hadjistylis (Game and Fauna Service) and H. Nicolaou (Forestry Department) 13. Derting TL, Cranford JA. Physical and behavioral correlates of prey vulner- who have contributed in pellet sampling. Also thanks to Robert Patchett ability to barn owl (Tyto alba) predation. Am Midl Nat. 1989;121:11–20. (University of St. Andrews) and Adrian Wright ( Thessaloniki) for checking 14. Muñoz-Pedreros A, Murúa R. Control of small mammals in a pine planta- the spelling and grammar of this article. University Studio Press, Thessaloniki tion (central Chile) by modification of the habitat of predators (Tyto alba, constructed the map included in this paper. Strigiformes and Pseudalopex sp., Canidae). Acta Oecol. 1990;11:251–61. 15. Yom-Tov Y, Wool D. Do the contents of barn owl pellets accurately repre- Competing interests sent the proportion of prey species in the field? Condor. 1997;99:972–6. The authors declare that they have no competing interests. 16. Muñoz-Pedreros A, Gil C, Yáñez J, Rau JR. Raptor habitat management and its implication on the biological control of the Hantavirus. Eur J Wildl Availability of data and materials Res. 2010;56:703–15. Data were adequately presented in the manuscript. For data requests contact 17. Muñoz-Pedreros A, Gil C, Yáñez J, Rau JR, Möller P. Trophic ecology of the authors (MM and MC). two raptors, barn owl (Tyto alba) and white-tailed kite (Elanus leucurus), Moysi et al. J of Biol Res-Thessaloniki (2018) 25:9 Page 8 of 8 and possible implications for biological control of Hantavirus reservoir in 42. Hill MO. Diversity and evenness: a unifying notation and its conse- Chile. Wilson J Ornithol. 2016;128:391–403. quences. Ecology. 1973;54:427–32. 18. Tores M, Motro Y, Motro U, Yom-Tov Y. The barn owl—a selective oppor- 43. Alatalo RV. Problems in the measurement of evenness in ecology. Oikos. tunist predator. Israel J Zool. 2005;51:349–60. 1981;37:199–204. 19. Herrera CM. Trophic diversity of the barn owl Tyto alba in continental 44. Peres-Neto PR, Jackson DA, Somers KM. How many principal compo- western Europe. Ornis Scand. 1974;5:181–91. nents? Stopping rules for determining the number of non-trivial axes 20. Álvarez-Castañeda ST, Cárdenas N, Méndez L. Analysis of mammal revisited. Comput Stat Data An. 2005;49:974–97. remains from owl pellets (Tyto alba), in a suburban area in Baja California. 45. Alivizatos H, Goutner V. Winter diet of the barn owl (Tyto alba) and long- J Arid Environ. 2004;59:59–69. eared Owl (Asio otus) in northeastern Greece: a comparison. J Raptor Res. 21. Obuch J, Benda P. Food of the barn owl (Tyto alba) in the eastern Mediter- 1999;33:160–3. ranean. Slovak Rapt J. 2009;3:41–50. 46. Alivizatos H, Goutner V, Athanasiadis A, Poirazidis K. Comparative tempo- 22. Birdlife International. Data zone; 2015. http://dataz one.birdl ife.org/speci ral prey use by barn owl (Tyto alba) and little owl (Athene noctua) in the es/facts heet/commo n-barn-owl-Tyto-alba. Accessed 20 Nov 2016. Evros Delta, northeastern Greece. J Biol Res Thessalon. 2006;6:177–86. 23. Agrolife Project. http://agrol ife.eu. Accessed 4 Oct 2015. 47. Ali MSA, Santhanakrishnan R. Diet composition of the barn owl Tyto 24. Kassinis N, Roulin A. Reproduction of the barn owl (Tyto alba) in Cyprus alba (Aves: Tytonidae) and spotted owlet Athene brama (Aves: Strigidae) (Aves: strigiformes). Zool Middle East. 2017;63:369–71. coexisting in an urban environment. Podoces. 2012;7:21–32. 25. Angelici FM, Latella L, Luiselli L, Riga F. The summer diet of the little owl 48. Miltschev B, Boev Z, Georgiev V. Food of the Barn Owl (Tyto alba) in south- (Athene noctua) on the island of Astipalaia (Dodecanese, Greece). J Raptor eastern Bulgaria. Egretta. 2004;47:66–77 (in German). Res. 1997;31:280–2. 49. Miltschev B, Georgiev V. Influence of vole population peaks and the use 26. Nature Conservation Unit. Virtual Biodiversity Museum of Cyprus; 2012. of rodenticides on the diet of barn owl Tyto alba (Scopoli 1769) during http://www.natur emuse um.org.cy/lang1 /habit ats.html. Accessed 5 Jan the breeding season in south-east Bulgaria. Egretta. 2009;50:82–7 (in 2017. German). 27. Marti CD. Feeding ecology of four sympatric owls. Condor. 1974;76:45–61. 50. Milchev B. Dietary comparison of coexisting barn owl (Tyto alba) and 28. Goutner V, Alivizatos H. Diet of the barn owl (Tyto alba) and little owl eagle owl (Bubo bubo) during consecutive breeding seasons. Anim Biol. (Athene noctua) in wetlands of northeastern Greece. Belg J Zool. 2016;66:219–28. 2003;133:15–22. 51. Jaksic FM. Trophic structure of some Nearctic, Neotropical and Palearctic 29. Balčiauskienė L. Analysis of tawny owl (Strix aluco) food remains as owl assemblages: potential roles of diet opportunism, interspecific inter - a tool for long-term monitoring of small mammals. Acta Zool Litu. ference and resource depression. J Raptor Res. 1988;22:44–52. 2005;15:85–9. 52. Sommer R, Zoller H, Kock D, Böhme W, Griesau A. Feeding of the barn 30. Andrade A, Saraiva de Menezes JF, Monjeau A. Are owl pellets good owl, Tyto alba with first record of the European free-tailed bat, Tadarida estimators of prey abundance? J King Saud Univ-Sci. 2016;28:239–44. teniotis on the island of Ibiza (Spain, Balearics). Folia Zool. 2005;54:364–70. 31. Iezekiel S, Bakaloudis DE, Vlachos CG. The diet of the Bonelli’s eagle 53. Landová E, Horáček I, Frynta D. Have black rats evolved a culturally-trans- Hieraaetus fasciatus in Cyprus. In: Chancellor RD, Meyburg BU, editors. In: mitted technique of pinecone opening independently in Cyprus and Raptors worldwide: proceedings of the VI world conference on birds of Israel? Isr J Ecol Evol. 2006;52:151–8. prey and owls. Berlin: World Working Group on Birds of Prey/MME; 2004. 54. Purger JJ. Survey of the small mammal fauna in north-western Somogy p. 581–87. county (Hungary), based on barn owl Tyto alba (Scopoli, 1769) pellet 32. Seçkin S, Coşkun Y. Mammalian remains in the pellets of long-eared owls analysis. Nat Somogy. 2014;24:293–304. (Asio otus) in Diyarbakır province. Turk J Zool. 2006;30:271–8. 55. Pieper H. Fledermäuse aus Schleiereulen-Gewöllen von der Insel Kreta. Z 33. Marchesi L, Sergio F, Pedrini P. Costs and benefits of breeding in human- Säugetierkd. 1977;42:7–12. altered landscapes for the eagle owl Bubo bubo. Ibis. 2002;144:164–77. 56. Benda P, Andreas M, Kock D, Lučan RK, Munclinger P, Nová P, et al. 34. Lawrence MJ, Brown RW. Mammals of Britain: their tracks, trails and signs. Bats (Mammalia: Chiroptera) of the eastern Mediterranean Part 4: bat London: Blandford Press; 1967. fauna of Syria: distribution, systematics, ecology. Acta Soc Zool Bohem. 35. Brown R, Ferguson J, Lawrence M, Lees D. Track and signs of the birds of 2006;70:1–329. Britain and Europe. London: Helm; 1987. 57. Santhanakrishnan R, Ali AHMS, Anbarasan U. Diet variations of the barn 36. Kryštufek B, Vohralík V. Mammals of Turkey and Cyprus: Rodentia II: owl Tyto alba (Scopoli, 1769) in Madurai District, Tamil Nadu, southern Cricetinae, Muridae, Spalacidae, Calomyscidae, Capromyidae, Hystricidae, India. Podoces. 2010;5:95–103. Castoridae. Koper: Založba Annales; 2009. 58. Obuch J, Khaleghizadeh A. Spatial variation in the diet of the barn owl 37. Perrins C. Birds of Britain and Europe (New Generation Guides). London: Tyto alba in Iran. Podoces. 2011;6:103–16. Collins; 1987. 59. Kafkaletou-Diez A, Tsachalidis EP, Poirazidis K. Seasonal variation in the 38. MacDonald D, Barret P. Mammals of Britain and Europe. London: Collins; diet of the long-eared owl (Asio otus) in a northeastern agricultural area 1993. of Greece. J Biol Res Thessalon. 2008;10:181–9. 39. R Core Team. R: a language and environment for statistical computing. 60. Bontzorlos VA, Peris SJ, Vlachos CG, Bakaloudis DE. Barn owl Tyto alba prey Vienna: R Foundation for Statistical Computing. Computing; 2015. in Thessaly, and evaluation of barn owl diets throughout Greece. Ardea. 40. Shannon CE, Weaver W. The mathematical theory of communications. 2009;97:625–30. Urbana: University of Illinois Press; 1963. 41. Marks JS, Marti CD. Feeding ecology of sympatric barn owls and long- eared owls in Idaho. Ornis Scand. 1984;15:135–43.

Journal

Journal of Biological Research-ThessalonikiSpringer Journals

Published: May 31, 2018

References

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off