Ornithol Sci 18: 205 – 213 (2019)

SHORT COMMUNICATION Dietary habits of wintering Pale Turdus pallidus in the urban green environment of subtropical Okinawa-jima Island, Japan

Shun KOBAYASHI1,#,*, Wakako YOSHIDA1, Hiroaki UI2, Yoko OKAWARA2 and Masako IZAWA1

1 Faculty of Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903–0213, Japan 2 Graduate School of Engineering and Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903–0213, Japan

ORNITHOLOGICAL Abstract Knowledge of the feeding behavior of omnivorous migrant is impor- tant to understand their migration ecology. This study revealed the dietary habits of SCIENCE the Pale Thrush Turdus pallidus overwintering on Okinawa-jima Island, Japan. Food © The Ornithological Society items consumed were determined from the contents of the gizzards of 32 birds; at of Japan 2019 least 24 and eight plant species were identified. The contents of 84.4% of the studied gizzards were dominated by a single species or item. The Pale Thrush for- ages on various and plants, but in its winter habitat it feeds extensively and exclusively on select food items within a short period.

Key words Food habit, Ryukyu Archipelago, Turdus pallidus, Urban, Winter

Approximately 15% of bird species are migratory Tokyo, Japan, the Pale Thrush fed only on fruits, (Kirby et al. 2008), migrating between breeding and although the sample size of observed birds was small. non-breeding ranges in order to maximize energy These observations suggest that the diet of this spe- efficiency (Somveille et al. 2018). However, changes cies varies depending on its winter habitat. in food resources between years can cause annual In order to understand dietary habits, not only food fluctuations in migratory ranges (Newton 2008). Fur- species but also the amount of each species con- thermore, feeding habits can differ among individuals sumed is important. However, previous studies did in some omnivorous birds and individual specializa- not determine the frequency of occurrence or volume tion has been observed in some species (reviewed by of each food item and gizzard content sample sizes Bolnik et al. 2003 and Araújo et al. 2011). Therefore, were too small for analysis. Furthermore, in order to a detailed study of the feeding behavior of omnivo- understand the plasticity of the dietary habits of the rous migrant birds is of interest. species within its broad range, knowledge of its diet The Pale Thrush Turdus pallidus (Passeriformes: in the southern subtropical region where it winters Turdidae) has a body length of 24 cm (Takano 2015). is also desirable. Therefore, in the present study we It is widely distributed across East Asia. It breeds in used gizzard content analysis to clarify the feeding summer in northeast and Russia and winters habits of the Pale Thrush in a subtropical urban green in southern and western Japan, , and southern environment. China (Takano 2015). Previous studies of droppings have shown that this species is omnivorous, with MATERIALS AND METHODS its winter diet including animals such as arthropods and fruits from various plants growing in temperate 1) Study site Kyushu, Japan (Seki 1998). In contrast, Hamao et al. Samples were collected at the University of the (2009) observed that in the urban parks of temperate Ryukyus (Senbaru Campus), which is located in central Okinawa-jima Island (26°14–15′N, 127°45– (Received 26 August 2018; Accepted 17 February 2019) 46′E), the Ryukyu Archipelago, Japan. The campus # Corresponding author, E-mail: [email protected] * Present address: Faculty of Science, University of the Ryukyus, 1 has an area of 100 ha; it is surrounded by human Senbaru, Nishihara, Okinawa 903–0213, Japan residences, contains some scattered buildings, grass-

205 S. KOBAYASHI et al. land, and trees, and in addition to a 2 ha pond, has DISCUSSION 20 ha of secondary forest, and a 16 ha agricultural experimental field. Pale Thrushes inhabit this area The Pale Thrush was found to feed on a range of each winter from November to April. animal and plant species in winter in the subtropical urban green area. Previous studies have indicated 2) Gizzard contents analysis that Pale Thrushes mainly feed on plants in the tem- We collected dead Pale Thrush specimens from perate urban area (Hamao et al. 2009), or a combi- 2000 to 2017. The main cause of mortality was colli- nation of animal and plant food items at some sites sion with windows. Birds (N=38) were dissected and (Uchida 1913; Chiba et al. 1972; Seki 1998). As the the gizzards extracted and stored in 70% ethanol for abundance of arthropods decreases during winter analysis. The gizzard contents were washed through in urban areas (Galeotti et al. 1991), the probable a 1 mm sieve and the items remaining in the residue reason why thrushes were not observed feeding on were identified wherever possible to species level; animal matter in the temperate urban area was that when we could not do so, we used the label “item.” the abundance of arthropods was low. Our results, The wet weight of each species or item was mea- together with those of previous studies, indicate that sured to an accuracy of 1 mg using a microbalance the Pale Thrush is flexible in its feeding habits and (PG503-S; Mettler Toledo, Switzerland). changes according to food resource availability in their winter habitat. 3) Data analysis Although Pale Thrushes are omnivorous and utilize The frequency of occurrence (FO) of each spe- various food resources, our study showed that single cies or item was calculated, and a binomial test was food species or items tend to dominate the gizzard. In used to compare wet weight among species or items. general, birds have a short digestion time (Ziswiler & Statistical analysis was performed in R ver. 3.4.0 (R Farner 1972; McKechnie 2010). Our results indicate Core Team 2017). that the Pale Thrush intensively consumes specific foods over a short period. Uchida (1913) also showed that gizzard contents were dominated by one to four RESULTS items in this species (N=5). In addition, among Six of the 38 gizzard samples (15.8%) were empty various other omnivorous Turdidae gizzards were and were excluded from the analyses. dominated by one item in 51.4% (N=177) of Dusky From the gizzard samples (N=32), 24 animal Thrushes T. naumanni eunomus wintering in Tokyo, and eight plant species were identified; many items in 56.5% (N=62) of Brown-headed Thrushes T. remained unidentified (Table 1). The mean number chrysolaus resident in Tokyo, and in 37.0% (N=27) of items contained in a single gizzard was 3.4±2.1 of White’s Thrushes Zoothera dauma aurea resident (animal: 2.2±1.9; plant: 1.2±0.6) (N=32, mean±SD). in Tokyo (Uchida 1913). Although the study method Animal species from Gastropoda (FO=53.1%), in the present study differed from that in previous Diplopoda (53.1%), and Insecta (37.5%) frequently studies, the migratory Turdidae may share similar appeared, as did the plant species Bischofia javanica feeding behavior. (fruit/seed; 40.6%) (Table 1). Grit, parasites, and Intra- and interspecific competition, ecological plastics were also observed (Table 1). opportunity, and predation are ecological and evolu- Among the 32 samples analyzed, mean wet weight tionary factors that influence variation in individual was 689.7±802.1 (12–2945) mg. The contents of 10 diets (Araújo et al. 2011). We did not determine what (31.3%) gizzards were dominated (>80% of total wet influences the diet of the Pale Thrush among these weight) by animal species, and 17 (53.1%) gizzards factors. Further research, including identification of were dominated by plant matter (Table 2). Overall, age and sex, study in natural habitat, and long-term the contents of 13 gizzards (40.6%) were found to be surveys, are needed to elucidate the factors deter- dominated by animal food items, while others were mining individual diet variation in omnivorous birds dominated by plant species (binomial test; P=0.38). such as the Pale Thrush so as to understand their The contents of 27 (84.4%) gizzards were dominated effects on migration. (more than 80%) by a single animal item or plant species (Appendix 1 and 2).

206 Dietary habits of Turdus pallidus

Table 1. Frequency of occurrence (FO) of each item.

Order Family Species name Stage/Part FO Animal matters Insecta Hymenoptera Formicidae Pheidole sp. Adult 3.1 Monomorium intrudens Adult 3.1 Ochetellus glaber Adult 3.1 Tetramorium bicarinatum Adult 3.1 Tetramorium sp. Adult 3.1 Anoplolepis gracilipes Adult 6.3 Blattaria Blattellidae Adult 3.1 Coleoptera Unknown – Adult 12.5 Unknown – Larva 3.1 Lepidoptera – Lepidoptera sp. Larva 3.1 Diptera – Diptera sp. Larva 6.3 Psocodea Unknown – Adult 3.1 Unknown – – Adult 12.5 – – Larva 3.1 Insecta Total 37.5 Arachnida Araneae – Unknown Unknown 6.3 Acari – Unknown Adult 3.1 Arachnida Total 6.3 Diplopoda Polydesmida Paradoxosomatidae Unknown Unknown 28.1 Julida Unknown – Unknown 15.6 Unknown – – Unknown 28.1 Diplopoda Total 53.1 Crustacea Isopoda Armadillidae Unknown Adult 3.1 Isopoda Unknown – Larva 3.1 Crustacea Total 6.3 Gastropoda Stylommatophora Bradybaenidae Bradybaena sp. Unknown 6.3 Acusta despecta despecta Unknown 9.4 Unknown – 12.5 Subulinidae Allopeas kyotoense Adult 6.3 Mollusca Achatina fulica Larva 3.1 Unknown – – 3.1 Mesogastropoda Cyclophoridae Cyclophorus turgidus Larva 21.9 Gastropoda Total 53.1 Animal Total 78.1 Plant matters Laurales Lauraceae Machilus thunbergii Fruit/seed 3.1 Poales Poaceae Poaceae spp. Seed 6.3 Malpighiales Phyllanthaceae Bischofia javanica Fruit/seed 40.6 Clusiaceae Garcinia subelliptica Fruit/seed 3.1 Oxalidales Elaeocarpaceae Elaeocarpus zollingeri Fruit/seed 3.1 Rosales Moraceae Ficus sp. Utricle 9.4 Morus australis Fruit/seed 9.4 Sapindales Meliaceae Melia azedarach Fruit/seed 0.0 Solanales Solanaceae Solanaceae sp. Fruit/seed 3.1 Unknown – – Fruit/seed 12.5 – – Leaf/stem 28.1 Fruits/seeds/utricle Total 57.9 Plant Total 90.6 Artificial matters Parts of plastic 3.1 Parts of wood 3.1 Others Parasite 6.3 Feather 18.8 Grit 18.8 Unknown 18.8

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Table 2. Wet weight (%) of each animal class and plant order for each individual.

Animals Plants Individual ID Insecta Arachnida Diplopoda Crustacea Gastropoda Laurales Poales Malpighiales Oxalidales Rosales Solanales Unknown plant 20170124 0 100 20170122 100 20161211 100 20160131 94 1 5 0 20160125 100 20151219 0 12 0 88 20151214B 0 100 20151214A 0 0 100 20151204 4 96 20151203 8 91 1 20151123 0 6 94 20151117A 0 8 92 20150116 90 6 4 20141213 0 69 29 1 20141207 0 100 0 0 20141205 3 2 95 20141128 3 0 0 0 97 0 20141121 99 1 20131224 83 17 20121121 5 0 88 0 7 20110408 0 9 20 71 20101129 6 46 0 44 4 20100410 98 2 20061228 6 36 58 20061218 100 20061204B 100 20061204A 0 0 99 20050314 0 100 0 20021124 40 36 2 21 20021121 7 93 20001120 100 20000322 100

Blank cells indicate nothing appeared.

ACKNOWLEDGMENTS Brambling, Shrike, Thrush, Swallow, Skylark, Fly- catcher, Warbler, Wagtail, Nuthatch, Tree-creeper We are grateful to Mayu Yoshimura, Ryosuke and Tit. Sci Rep Takao Mus Nat Hist (4): 43–77 (in Terada, and Haruhi Soeda for supporting this study, Japanese with English summary). and to various persons who helped us to collect the Galeotti P, Morimando F & Violani C (1991) Feeding samples. We are grateful to two anonymous review- ecology of the Tawny Owls (Strix aluco) in urban ers for their valuable comments. habitats (northern Italy). Ital J Zool 58: 143–150. Hamao S, Miyashita T, Hagiwara S & Mori T (2009) Seed dispersal by wintering birds in an urban space REFERENCES and relationship between gape width and fruit size. Araújo MS, Bolnik DI & Layman CA (2011) The eco- Jpn J Ornithol 59: 139–147 (in Japanese with English logical causes of individual specialization. Ecol Lett summary). 14: 948–958. Kirby JS, Stattersfield AJ, Butchart SHM, Evans MI, Bolnik DI, Svanbäck R, Fordyce JA, Yang LH, Davis Grimmett RFF, Jones VR et al. (2008) Key conserva- JM, Hulsey CD et al. (2003) The ecology of individu- tion issues for migratory land- and waterbird species als: incidence and implications of individual speciali- on the world’s major flyways. Bird Conserv Int 18: sation. Am Nat 161: 1–28. S49–S73. Chiba S, Asabi M, Matsumoto F, Nishihiro S, Asanaka McKechnie A (2010) Feeding and digestion in birds. K & Sakagami E (1972) Stomach analysis of Japanese Afr Bird Birding 15: 46–51.

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Newton I (2008) The ecology of bird migration. Aca- Takano S (2015) A field guide to the birds of Japan- demic Press, London. revised and with supplements. Wild Bird Society of R Core Team (2017) R: A language and environment Japan, Tokyo (in Japanese). for statistical computing. R Foundation for Statisti- Uchida S (1913) Honpou-san chorui to nogyo tono cal Computing. Available at http://www.R-project.org kankei chosa seiseki (Results of the survey for (accessed on 18 May 2017). relationships between Japanese birds and agriculture). Seki S (1998) Territorial behavior of the Pale Thrush Nouji sikenjo tokubetsu houkoku (29): 1–54 (in Jap- (Turdus pallidus) wintering in the temperate ever- anese). green broad-leaved forest. Trans Jpn For Soc 109: Ziswiler V & Farner DS (1972) Digestion and the 393–394 (in Japanese). digestive system. In: Farner DS & King JR (eds) Somveille M, Rodrigues ASL & Manica A (2018) Avian biology volume II. pp 343–430. Academic Energy efficiency drives the global seasonal distribu- Press, London. tion of birds. Nat Ecol Evol 2: 962–969.

209 S. KOBAYASHI et al. 0 Insecta Coleoptera – 0 0 0 0 – Coleoptera sp. (adult) Coleoptera sp. (larva) 0 0 InsectaHymenoptera Blattaria Insecta Coleoptera Insecta Formicidae Blattellidae sp.Tetramorium Blattellidae sp. 0 Tetramorium bicarinatum Tetramorium sp. 0 Insecta Insecta Pheidole 0 Insecta Formicidae Formicidae Formicidae Appendix 1. weight Wet (mg) of animal items. 0 Insecta Formicidae 0 0 Insecta HymenopteraFormicidae Hymenoptera Hymenoptera Hymenoptera Hymenoptera Anoplolepis gracilipes Monomorium intrudens Ochetellus glaber 24-Jan 22-Jan 11-Dec 18-Dec 4-Dec 4-Dec 21-Nov 24-Dec 21-Nov 25-Jan 19-Dec 3-Dec 23-Nov 17-Nov 16-Jan 13-Dec 7-Dec 28-Nov 29-Nov 28-Dec 24-Nov 21-Nov 20-Nov 2005 14-Mar 2015 2015 2015 2015 2015 2014 2014 2010 2000 22-Mar ID Year Date 20170124 2017 20170122 2017 20161211 2016 20160131 2016 31-Jan 20061218 2006 20061204B 2006 20061204A 2006 20050314 20141121 2014 20131224 2013 20121121 2012 20110408 2011 8-Apr 20160125 2016 20151219 20151214C 201520151214B 14-Dec 201520151204A 14-Dec 201520151203 4-Dec 20151123 20151117A 20150116 20141213 20141207 20141205 201420141128 5-Dec 2014 20101129 20100410 201020061228 10-Apr 2006 20021124 2002 20021121 2002 20001120 2000 20000322

210 Dietary habits of Turdus pallidus 30 Isopoda Armadillidae Armadillidae sp. 3 6 0 47 19 31 64 111 205 – – Diplopoda sp. 7 3 36 10 280 Diplopoda Diplopoda Crustacea 0 8 2 9 27 53 40 173 300 Paradoxosomatidae Julidae Paradoxosomatidae sp. Julidae sp. – 0 0 0 Arachnida Arachnida Diplopoda Araneae Acari Polydesmida Julida – Araneae sp. Acari sp. 7 Insecta – – Appendix 1. (continued). 0 0 10 288 – – Insecta sp. (adult) Insecta sp. (larva) 0 Psocodea sp. 0 26 Insecta Insecta Insecta Diptera Psocodea –– Diptera sp. Insecta Lepdoptera – Lepdoptera sp. (larva) 24-Jan 22-Jan 11-Dec 25-Jan 19-Dec 3-Dec 23-Nov 17-Nov 7-Dec 16-Jan 13-Dec 21-Nov 24-Dec 21-Nov 29-Nov 28-Dec 28-Nov 32 18-Dec 4-Dec 4-Dec 24-Nov 21-Nov 20-Nov 2015 2015 2015 2015 2014 2015 2014 2010 2005 14-Mar 2000 22-Mar ID Year Date 20170124 2017 20170122 2017 20161211 2016 20160131 201620160125 31-Jan 2016 20151219 20151214C 201520151214B 14-Dec 201520151204A 14-Dec 201520151203 4-Dec 20151123 20151117A 20141207 20150116 20141213 20141205 2014 5-Dec 20141121 2014 20131224 2013 20121121 2012 20110408 201120101129 8-Apr 20100410 201020061228 10-Apr 2006 20141128 2014 20061218 2006 20061204B 2006 20061204A 2006 20050314 20021124 2002 20021121 2002 20001120 2000 20000322

211 S. KOBAYASHI et al. 0 0 0 0 6 0 0 8 0 0 0 0 27 24 47 32 19 98 50 15 23 305 461 448 234 127 193 231 123 634 541 154 Total 0 0 14 61 23 234 154 Cyclophoridae Cyclophorus turgidus 0 – Stylommatophora sp. 67 3 8 Allopeas kyotoense Achatina fulica 0 0 123 293 Bradybaenidae sp. Appendix 1. (continued). 43 501 Gastropoda Gastropoda Gastropoda Gastropoda Gastropoda Gastropoda Bradybaenidae Bradybaenidae Subulinidae Mollusca Bradybaena sp. 0 24 425 Gastropoda Bradybaenidae Acusta despecta 0 Crustacea Isopoda Stylommatophora Stylommatophora Stylommatophora Stylommatophora Stylommatophora Stylommatophora Mesogastropoda – Isopoda sp. 24-Jan 22-Jan 11-Dec 25-Jan 19-Dec 3-Dec 23-Nov 17-Nov 16-Jan 13-Dec 7-Dec 28-Nov 21-Nov 24-Dec 21-Nov 29-Nov 28-Dec 18-Dec 4-Dec 4-Dec 24-Nov 21-Nov 20-Nov 2015 2015 2015 2015 2015 2014 2014 2010 2005 14-Mar 2000 22-Mar ID Year Date 20170124 2017 20170122 2017 20161211 2016 20160131 2016 31-Jan 20160125 2016 20151219 20151214C 2015 14-Dec 20151214B 2015 14-Dec 20151204A 2015 4-Dec 20151203 20151123 20151117A 20150116 20141213 20141207 20141205 2014 5-Dec 20141128 2014 20141121 2014 20131224 2013 20121121 2012 20110408 2011 8-Apr 20101129 20100410 2010 10-Apr 20061228 2006 20061218 2006 20061204B 2006 20061204A 2006 20050314 20021124 2002 20021121 2002 20001120 2000 20000322

212 Dietary habits of Turdus pallidus 0 0 0 0 68 15 98 12 52 196 213 336 238 105 205 651 223 180 1132 1094 2913 2386 1663 2945 1249 Total 0 0 4 4 0 0 0 7 7 27 1243 18 14 1025 17 17 5 15 98 177 –– –– 238 Solanaceae sp. Plant sp. Plant sp. 100 1011 1132 Fruit/Seed Fruit/Seed Fruit/Seed Fruit/Seed Leaf/Branch Morus australis Melia azedarach sp. 0 19 223 Utricle Ficus 1176 2386 Garcinia subellipticaGarcinia Elaeocarpus zollingeri Appendix 2. weight Wet (mg) of plant items. 68 73 52 12 336 195 651 205 180 1094 2913 1663 2945 Fruit/Seed Fruit/Seed Fruit/Seed Bischofia javanica 0 0 Seed Poaceae spp. 1216 Fruit/Seed Lauraceae Poaceae Phyllanthaceae Clusiaceae Elaeocarpaceae Moraceae Moraceae Meliaceae Solanaceae Laurales Poales Malpighiales Malpighiales Oxalidales Rosales Rosales Sapindales Solanales Machilus thunbergii 21-Nov 20-Nov 28-Dec 18-Dec 4-Dec 4-Dec 29-Nov 24-Nov 24-Dec 21-Nov 21-Nov 7-Dec 28-Nov 3-Dec 23-Nov 17-Nov 16-Jan 13-Dec 25-Jan 19-Dec 22-Jan 11-Dec 24-Jan 2000 22-Mar 2005 14-Mar 2010 2014 2015 2015 2015 2015 2014 2015 ID Year Date 2002112120001120 2002 20000322 2000 2010041020061228 2010 10-Apr 20061218 2006 20061204B 2006 2006 20061204A 2006 20050314 20101129 20021124 2002 2013122420121121 2013 20110408 2012 2011 8-Apr 20141121 2014 20141207 2014120520141128 2014 5-Dec 2014 20151214C 201520151214B 14-Dec 201520151204A 14-Dec 201520151203 4-Dec 20151123 20151117A 20150116 20141213 2016012520151219 2016 2017012220161211 2017 20160131 2016 2016 31-Jan 20170124 2017

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