Advanced
Diet of yellow bitterns (Ixobrychus sinensis) during the breeding season in South Korea
Diet of yellow bitterns (Ixobrychus sinensis) during the breeding season in South Korea
Journal of Ecology and Environment. 2012. Mar, 35(1): 9-14
Copyright ©2012, The Ecological Society of Korea
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use,distribution, and reproduction in any medium, provided the original work is properly cited.
  • Received : November 07, 2011
  • Accepted : December 22, 2011
  • Published : March 01, 2012
Download
PDF
e-PUB
PubReader
PPT
Export by style
Article
Author
Metrics
Cited by
TagCloud
About the Authors
Miran Kim

Abstract
Yellow bitterns ( Ixobrychus sinensis ) are a small wetland bird common to Asian countries including South Korea, Japan, and China. The aim of this study is to describe diet of yellow bitterns during the breeding season in artificial wetland of northeastern South Korea between May to August 1999-2001. For the purposes of this paper, we observe the frequency of nest visiting by parents during the chick rearing period. A total of 98 boluses regurgitated by 52 chicks aged 1 day to 11 days after hatching form the sample and are shown to contain 323 food items. A bolus contained mean 3.8 items and weighs 0.2 g to 7.7 g. The most regularly occurring food items recorded are fish (63%) and insets (33%). In terms of fish,top mouth minnows ( Pseudorasbora parva ) and crucian carps ( Carassius auratus ) are frequently observed. In terms of insects, there are mosquitoes (Diptera), instars of dragonfly (Libelluidae), damselflies (Coenagrinonidae) and water bugs( Diplonychus japonicus ). Yellow bitterns were also shown to feed on bull frogs ( Rana catesbeiana ), shrimp (Palaemoni-dae), and spiders (Araneae). The size of fish in a bolus ranged from 15.56 mm to 93.73 mm (mean, 37.08 mm). The amount of food can be observed to increase with the age of chicks ( r = 0.279, P = 0.025, N = 64) but parents did not provide larger fish as chicks grew. Parent birds visited nests more frequently when they have a larger brood (F 1,21 = 14.529, P = 0.001). Our results suggest that fish is the most important prey during the breeding season and that age of chicks is related to amount of diet in yellow bitterns.
Keywords
INTRODUCTION
During the breeding season, diet selection often af-fects breeding success (Pierotti and Annett 1991, Wanless et al. 2007). Parent birds have to select appropriate food, which can meet the nutrient requirements of chicks and maximize the efficiency of parental efforts. Experienced parents often select higher quality prey compared to young parents (Limmer and Becker 2009). Parents must also select prey items depending on the age of chicks, as older chicks need more food than younger ones; as such,prey selection changes in terms of composition or size as chicks age (Navarro et al. 2009, Ramos et al. 2009, Mitrus et al. 2010). Yellow-legged gulls ( Larus michahellis ) feed chicks on smaller prey when chicks are young (Ramos et al. 2009), while great bitterns ( Botaurus stellaris ) exhibit no change of prey size as chicks age (Gilbert et al. 2003). Parents may simply choose prey items depending on food availability within habitats. Gull-billed terns ( Sterna ni-lotica ) feed chicks on more aquatic prey in the early part of the breeding season (Dies et al. 2005) and rhinoceros auklets ( Cerorhinca monocerata ) quickly change from Japanese sandlance ( Ammodytes personatus ) to Japanese sea greenling ( Pleurogrammus azonus ) when the warm current reaches their foraging area (Ito et al. 2009). Preys provided to chicks of little terns ( Sterna albifrons ) change-s from year to year, depending on tide and wind speed (Paiva et al. 2006).
Yellow bitterns ( Ixobrychus sinensis ) are small bitterns living in wetlands such as reed beds and rice fields. The population of yellow bitterns is widely distributed from India to South-east Asia. However, their foraging eco-logy has been rarely studied (Ueda 1985, 1992, Kim 2001, Gerlach and Skerrett 2002). This may be due to their cau-tious behavior and concealed habitats. The diet of yellow bitterns during the breeding season has been reported as consisting of aquatic insects and freshwater shrimp (Han-cock and Kushlan 1984).
In this study, we tested whether yellow bittern parents change diet in terms of amount and/or prey size accord-ing to chick development. We also investigated factors af-fecting the frequency of nest visits during the chick rear-ing period in yellow bitterns.
MATERIALS AND METHODS
- Study areas and collecting boluses
This study has been carried out at the artificial swamp (55 ha) in An-san city (126°50´04˝-48˝E, 37°16´ 34˝-43˝N), Republic of Korea from late May to August in 1999 and 2000. To investigate the diet of yellow bitterns during the breeding season, we collected boluses which regurgitated by chicks when they feel stressed, a behavior exhibited by yellow bitterns and other bird species of the family Aredaidae (Kirkpatrick 1940, Olmos et al. 2001). For the purposes of this study, we define a bolus as a food ball re-gurgitated by a chick in one attempt. We visited 21 nests every day during the late incubation period and during the chick rearing period to identify the age of chicks and to collect boluses. Chicks were individually marked with a non-toxic marker pen on their bills or color rings.
Once chicks regurgitated boluses, we measured the wet weight of a bolus and retrieved them from nests to identi-fy prey items and to record the number of items. Because heads of fish in a bolus are slowly digested compared to other part of the fish (Barrett et al. 2007), we counted the number of fish heads to avoid over-counting. Food items in a bolus were identified based on the guide book of fish (Kim and Kang 1993), insects (Youn 1995) and aquatic insects (Bae 1998). Prey items in a bolus were identified at species level or at family level and the number of food items in a bolus were counted. Body size of a fish in a bo-lus was measured from mouth to tail to the nearest 0.01 mm using vernier calipers. Boluses were preserved in 60% ethanol for weighing the ash-free dry weight in the labo-ratory.
For the analysis of the relationship between age of chicks and prey size, only fish of known size were includ-ed in the study. The proportion of prey items was estimat-ed as a percentage of the total number of prey in a bolus.
In the laboratory, we used ash-free dry weight (AFDW) to estimate the energy of regurgitated prey. AFDW has been used to estimate actual energy intake of prey in many previous studies of geese (Therkildsen and Mad-sen 2000) and shorebirds (Ge et al. 2009). Non-prey items such as pieces of reeds were removed to estimate AFDW of regurgitated prey. Boluses were dried at a temperature of 55°C and burnt in a 550°C oven for 5 h. AFDW was esti-mated in 62 boluses collected from 1999.
- Frequency of visiting nests by parents
We estimated the frequency of visiting nests by par-ent birds from June to August. This estimate is in terms of nest visits per h, based on recordings made with a video camera. We recorded nests with chicks for approximately 2 h per a day between 8.30 and 17.00. A video camera was camouflaged with reeds and placed 2 to 3 m away from the nest. Items of interest in these recordings are age of the oldest chicks in a brood, date of observation, and brood size.
- Statistical analysis
All data analysis was performed using SPSS ver. 18.0 (SPSS Inc., Chicago, IL, USA). ANOVA was used to inves-tigate the relationship between food amount and other factors. All biologically relevant two-way interactions between explanatory variables were included in the ini-tial model and we removed the stepwise least significant term. Statistics are shown for the last step variables in-cluded in the model. The correlation between amount of food and age of chicks was examined using Pearson’s rank correlation test. This is significant when the P -value is less than 0.05. Mean values are presented with ± 1 SE.
RESULTS
- Regurgitated prey items
A total of 98 boluses were collected from 52 chicks aged from one day to eleven days after hatching. A mean of two boluses per a chick were taken (range, one to six boluses per a chick). Boluses were collected from June to August, 1999-2001.
Yellow bitterns were observed to feed chicks primar-ily on fish (63%) and insects (33%) ( Table 1 ). A bolus in-
Lager Image
Composition of prey items in 98 boluses regurgitated by chicks of yellow bitterns during the breeding season. Total amounts of prey items collected were 154 188 and 29 in June July and August respectively.
Prey items (%) in 98 boluses regurgitated by 52 chicks of yellow bitterns in 1999 and 2000Values are presented as number (%). Occupancy was estimated as the number of each item with regard to total items.
Lager Image
Prey items (%) in 98 boluses regurgitated by 52 chicks of yellow bitterns in 1999 and 2000 Values are presented as number (%). Occupancy was estimated as the number of each item with regard to total items.
cluded a mean of 3.8 individual items. With regard to fish in boluses, top mouth minnows ( Pseudorasbora parva ) were the most common (29.1%). Other fish species in re-gurgitates were crucian carps ( Carassius auratus ) (22.9%), loaches (Misgurnus) (9.2%), and round-tailed paradise fishes ( Macropodus chinenesis ) (1.2%). With regard to insects in boluses, mosquitoes (Diptera) were frequently observed (17.9%). Chicks of yellow bitterns were also fed on instars of dragonflies, damselflies (Coenagrinonidae), and water bugs ( Diplonychus japonicus ). Other prey items include bullfrogs, shrimp, and spiders ( Table 1 ). The com-position of prey items in boluses is observed to change as the breeding season progresses. In June, yellow bitterns feed their chicks a diet of equal parts fish and insects, while through the rest of the breeding season more fish than insects are fed to chicks (July, 74% of fish; August, 69% of fish) ( Fig.1 ).
- Amount of food and prey size
The fish size in boluses was measured in 48 fish, of which the entire body length is estimated. The mean ob-served length of fish in boluses was 35.8 ± 2.65mm (range, 15.56 to 93.79 mm). The wet weight of a bolus ranged from 0.2 g to 7.7 g and AFDW was from 0.032 g to 1.421 g. AFDW of a bolus was observed to increase with the age of chicks ( r = 0.279, P = 0.025, N = 64) ( Fig.2 ). The fish size in bo-luses is not observed to be related to the age of chicks ( r = -0.073, P = 0.623, N = 48).
Lager Image
Relationships between ash-fee dry weight (AFDW) (g) per a bolus in 1999 and the age of chicks.
Lager Image
Relationships between frequency of nest visits by parents and brood size in yellow bitterns
Frequency of nest visits by parents for feeding chicks in eight nests related to brood size age of the oldest chicks in a brood and date of observationTwenty-three observations are made via video recording for a total of 22 h 10 min and 5 s during the breeding season.
Lager Image
Frequency of nest visits by parents for feeding chicks in eight nests related to brood size age of the oldest chicks in a brood and date of observation Twenty-three observations are made via video recording for a total of 22 h 10 min and 5 s during the breeding season.
- Frequency of visiting nests
In this study, we recorded eight nests containing chicks aged three to ten days after hatching. A total of 23 obser-vations were made for a total recorded time period of 22 h 10 min 5 s. Chicks are not disturbed for more than 10 min after placing a video camera. Parents visited nests 1.39 ± 0.09 times per h (range, 0.27 to 2.12 times per h) during the chick rearing period. Parents visited more frequently when they had a larger brood in a nest ( F 1,21 = 14.529, P = 0.001) ( Fig.3 ). However, the age of the oldest chicks in a brood ( F 1,20 = 0.702, P = 0.412) and date of observation ( F 1,19 = 0.483, P = 0.405) did not affect the frequency of nests visits by parents ( Table 2 ).
DISCUSSION
In the results of this study, food items fed to chicks by yellow bittern parents are observed to vary throughout the breeding season. In the early breeding season, yellow bitterns feed their young on similar proportions of fish and insects, but later in the breeding season more fish are consumed than insects. This may be related to the change of food availability in the study area over time. As the fries of top mouth minnows and crucian carps, which form the main prey of yellow bitterns, hatch in April (Kim and Kang 1993), small sized fish may become more abundant later in the breeding season. In Japan, yellow bitterns are op-portunistic predators (Ueda 1992). They mainly feed fish and insects, but also reptiles and amphibians under poor food conditions (Ueda 1985, 1992).
The diet fed by yellow bitterns to chicks thus consisted of varied items such as fish, insects, and frogs. Fish form the most important prey item during the chick rearing period. In Malaysia, yellow bitterns breeding in rice fields are shown to prey more on invertebrates such beetle lar-va, blue-bottle flies, and damselflies than fish (Lansdown and Rajanathan 1993). In our results, mosquitoes were observed to be the most frequent insect prey of yellow bitterns. However, it is observed through video recording that parents usually catch mosquitoes when they are with chicks in the nest. Parent birds might catch mosquitoes to protect chicks in the nests.
The rate of food provision by parents varies with chick age and brood size (Adler and Ritchison 2011). The fre-quency of nest visits by parents in yellow bitterns is re-lated to brood size. Parent birds are observed to visit nests more frequently when they have a larger brood. This may be due to increased food requirements when bitterns have a large brood. The age of the oldest chick in a brood did not exert an observable influence on the frequency of nest visits by parents.
The wet weight of a bolus increases with a chick’s age. The parents of yellow bittern brought more food, but did not alter the frequency of nest visits as chicks grew. One possible explanation is that higher rates of nest visi-tation may increase predation risk (Eggers et al. 2005). Parents may bring larger numbers of fish in a food-load rather than visit nests more frequently in order to meet increased food demands of chicks. However, parents with larger broods may have to work harder and visit nests more frequently to maximize food quantity for chicks.
To conclude, yellow bitterns are observed to forage op-portunistically depending on food availability in habitats. The age of chicks and brood size is shown to affect the amount of food and the number of nest visits, respec-tively.
Acknowledgements
We thank Dr. Ki-sup Lee, Mr. Byong-soon Jang, Dr. Young-soo Kwon, Dr. Hwa-jeong Kim, Ms. Ji-young Ahn, and Dr. Sin-yeon Kim for their help in fieldwork.
References
Adler J , Ritchison G 2011 Provisoning behaviour of male and female grasshopper sparrows. Wilson J Ornithol 123 515 - 520    DOI : 10.1676/10-150.1
Bae Y 1998 A Picture Guide Book of Korean Insects. Korea University Seoul.
Barrett RT , Camphuysen K , Anker-Nilssen T , Chardine JW , Furness RW , Garthe S , Hüppop O , Leopold MF , Mon-tevecchi WA , Veit RR 2007 Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64 1675 - 1691    DOI : 10.1093/icesjms/fsm152
Dies JI , Marin J , Perez C 2005 Diet of nesting gull-billed terns in eastern Spain. Waterbirds 28 106 - 109    DOI : 10.1675/1524-4695(2005)028[0106:DONGTI]2.0.CO
Eggers S , Griesser M , Ekman J 2005 Predator-induced plas-ticity in nest visitation rates in the Siberian jay (Perisore-us infaustus). Behav Ecol 16 309 - 315    DOI : 10.1093/beheco/arh163
Ge ZM , Zhou X , Wang TH , Wang KY , Pei E , Yuan X 2009 Ef-fects of vegetative cover changes on the carrying capac-ity of migratory shorebirds in a newly formed wetland Yangtze River Estuary China. Zool Stud 48 769 - 779
Gerlach J , Skerrett A 2002 The distribution ecology and status of the yellow bittern Ixobrychus sinensis in Sey-chelles. Afr J Ecol 40 194 - 196    DOI : 10.1046/j.1365-2028.2002.00346.x
Gilbert G , Tyler G , Smith KW 2003 Nestling diet and fish preference of bitterns Botaurus stellaris in Britain. Ardea 91 35 - 44
Hancock J , Kushlan J 1984 The Heron's Handbook. Harper and Row London.
Ito M , Minami H , Tanaka Y , Watanuki Y 2009 Seasonal and inter-annual oceanographic changes induce diet switching in a piscivorous seabird. Mar Ecol Prog Ser 393 273 - 284    DOI : 10.3354/meps08192
Kim I , Kang H 1993 A Picture Guide Book of Korean Fish. Academic Books Seoul.
Kim M 2001 Breeding ecology of yellow bitterns. Kyunghee University Seoul Korea.
Kirkpatrick CM 1940 Some foods of young great blue her-ons. Am Midl Nat 24 594 - 601    DOI : 10.2307/2420861
Lansdown RV , Rajanathan R 1993 Some aspects of the ecol-ogy of Ixobrychus bitterns nesting in Malaysia ricefields. Colon Waterbirds 16 98 - 101    DOI : 10.2307/1521564
Limmer B , Becker PH 2009 Improvement in chick provi-sioning with parental experience in a seabird. Anim Be-hav 77 1095 - 1101    DOI : 10.1016/j.anbehav.2009.01.015
Mitrus C , Mitrus J , Sikora M 2010 Changes in nestling diet composition of the red-breasted flycatcher Ficedula parva in relation to chick age and parental sex. Anim Biol 60 319 - 328    DOI : 10.1163/157075610X516529
Navarro J , Louzao M , Igual JM , Oro D , Delgado A , Arcos JM , Genovart M , Hobson KA , Forero MG 2009 Seasonal changes in the diet of a critically endangered seabird and the importance of trawling discards. Mar Biol 156 2571 - 2578    DOI : 10.1007/s00227-009-1281-3
Olmos F , Silva RS , Prando A 2001 Breeding season diet of Scarlet ibises and little blue herons in a Brazilian mangrove swamp. Waterbirds 24 50 - 57
Paiva VH , Ramos JA , Catry T , Pedro P , Medeiros R , Palma J 2006 Influence of environmental factors and ener-getic value of food on Little Tern Sterna albifrons chick growth and food delivery. Bird Stud 53 1 - 11    DOI : 10.1080/00063650609461410
Pierotti R , Annett CA 1991 Diet choice in the herring gull: constraints imposed by reproductive and ecological fac-tors. Ecology 72 319 - 328    DOI : 10.2307/1938925
Ramos R , Ramírez F , Sanpera C , Jover L , Ruiz X 2009 Diet of Yellow-legged Gull (Larus michahellis) chicks along the Spanish Western Mediterranean coast: the relevance of refuse dumps. J Ornithol 150 265 - 272    DOI : 10.1007/s10336-008-0346-2
Therkildsen OR , Madsen J 2000 Assessment of food intake rates in pink-footed geese Anser brachyrhynchus based on examination of oesophagus contents. Wildl Biol 6 167 - 172
Ueda K 1985 The birds of Kusukdo. Wild Bird Rep 76 30 - 36
Ueda K 1992 Food of the yellow bittern Ixobrychus sinensis in boluses regurgitated by nestlings. J Yamashina Inst Ornithol 24 13 - 17    DOI : 10.3312/jyio1952.24.13
Wanless S , Frederiksen M , Daunt F , Scott BE , Harris MP 2007 Black-legged kittiwakes as indicators of environ-mental change in the North Sea: evidence from long-term studies. Prog Oceanogr 72 30 - 38    DOI : 10.1016/j.pocean.2006.07.007
Youn IB 1995 Aquatic Insects of Korea. Jeonghangsa Seoul.