Nest-Dismantling Behavior of Yellow-Bellied Prinia in Mainland Andislandpopulations

acta ethol https://doi.org/10.1007/s10211-017-0281-4

ORIGINAL PAPER

Nest-dismantling behavior of yellow-bellied prinia in mainland andislandpopulations

Longwu Wang1,2 & Shun-Jen Cheng3 & Yu-Cheng Hsu3 & Wei Liang2

Received: 7 February 2017 /Accepted: 1 December 2017 # Springer-Verlag GmbH Germany, part of Springer Nature and ISPA 2017

Abstract Nest-dismantling behavior in birds is considered a Introduction fitness-maximizing adaptive behavior. Here, we compared nest- dismantling behavior and associated predation rates and nest A nest is a temporary structure in which birds lay and hatch characteristics in yellow-bellied prinia (Prinia flaviventris)on eggs and brood nestlings. Usually, nests are abandoned after mainland China and the island of Taiwan during the breeding chicks fledge or new nests are built (Cavitt et al. 1999; Hansell season from 2010 to 2014. Our results indicated that the pro- 2000, 2007); however, some birds exhibit nest-dismantling portion of individuals showing nest-dismantling behavior was behavior. For example, the hair-crested drongo Dicrurus higher on the island than on the mainland (29.3 vs. 0.8%). Nest- hottentottus removes all nesting materials after a successful dismantling behavior was most frequent at the peak of the reproduction and disposes the materials far from the original breeding season and mainly involved removing the upper nest site (Li et al. 2009). To date, this is the only bird species halves of the nests and reusing the materials to construct new reported to exhibit nest-dismantling behavior after a success- nests. The time taken to dismantle old nests and use the mate- ful reproduction. Nest-dismantling behavior has also been re- rials to build new ones was shorter than the time needed to build ported in other birds, such as the house wren Troglodytes completely new nests. Nest predation, fidelity to the nest site, aedon and sedge wren Cistothorus platensis, which dismantle distance between old and new nests, and the costs of searching nests of conspecifics or other species in their breeding areas to for nest materials could influence nest-dismantling behavior. avoid intraspecific or interspecific competition, respectively Our results suggested that saving time and energy searching (Picman and Picman 1980; Belles-Iisles and Picman 1986; for new nest materials was the primary motivation behind Pribil and Picman 1991). The polygynandrous acorn wood- nest-dismantling behavior in yellow-bellied prinia. pecker Melanerpes formicivorus is a cooperative breeder, and when a group experiences the loss of male helpers, some individuals will dismantle the nests of their partners, forcing Keywords Island effect . Nest-dismantling . Predation . them to rebuild new nests (see Koenig 1990). The blue-gray Yellow-bellied prinia gnatcatcher Polioptila caerulea dismantles old or abandoned nests in its territory and reuses the nesting materials to build new nests. Nest-dismantling behavior can prevent competition * Wei Liang from other nearby breeding pairs and save time and energy [email protected] searching for nesting materials (Picman and Picman 1980;

1 Belles-Iisles and Picman 1986). Some birds such as the Key Laboratory of Plant Physiology and Development Regulation, ochre-bellied flycatcher Mionectes oleaginea, Hawai‘icreeper School of Life Sciences, Guizhou Normal University, Guiyang 550001, China Oreomystis mana, and cerulean warbler Dendroica cerulea save time and energy in nest building by stealing other birds’ 2 Ministry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, nesting materials (Snow and Snow 1979; VanderWerf 1998; Haikou 571158, China Jones et al. 2007). 3 Department of Natural Resources and Environmental Studies, The following hypotheses have been proposed for the evo- National Dong Hwa University, Hualien 97401, Taiwan lutionary origins and adaptation of bird nest-dismantling acta ethol behavior: (1) the Bpredation hypothesis^ states that by remov- open plains with a subtropical monsoon climate (for details, ing the nest materials, local predators cannot easily find newly see Yang et al. 2014). fledged chicks around the nests, thereby increasing the surviv- Yellow-bellied prinia belongs to the Passeriformes: al rates of chicks. In addition, removing nest materials from Cisticolidae. They build their nests in low bushes or small the old nest may reduce the predation risk for adult birds while shrubs, and both male and female birds are involved in the gathering new nesting materials elsewhere (Li et al. 2009; nest building process. The nests are mostly spherical, with Slager et al. 2012); (2) the Bnest site competition hypothesis^ side openings in the upper half (Lo and Cheng 2007;Ding states that birds dismantle old nests to conceal successful nest et al. 2008, 2017). Yellow-bellied prinia is a suitable host for sites that can be used in the next breeding season (Li et al. the Oriental cuckoo Cuculus optatus (see Xia et al. 2016)and 2009;Cantrelletal.2016). This hypothesis also states that the brood parasitism has been observed in the field (La Touche cost of building a new nest in a new territory is greater than the 1931, 1932, 1933, 1934; Zhang 1980;Yangetal.2014). cost of building a new nest at the old site after dismantling the old nest; therefore, birds usually choose the latter to avoid intense competition for territories (Belles-Iisles and Picman Field data collection 1986; Pribil and Picman 1991); (3) the Bevolutionary relic hypothesis^ states that nest-dismantling behavior was benefi- KOWA (8 × 30) Binoculars (Kowa Company, Ltd., cial to the breeding success of parent birds in the past, so nest- Nagoya, Japan) were used to systematically search for dismantling behavior is an adaptive reproductive strategy (Li nest habitats in the field. Located nests were marked and et al. 2009); (4) the Btime and energy hypothesis^ states that observed over the entire breeding season and the output of dismantling nests of conspecifics or other species and reusing each nest was recorded from the start of nest building to the nest materials to build new nests save time and reduce the the successful fledging of the young birds. We began re- energetic costs of searching for new nest materials (Jones et al. cording observations when the birds began to dismantle 2007). their nests and continued until the nests were completely The yellow-bellied prinia Prinia flaviventris is a small, dismantled or until the dismantling behavior ceased. The passerine bird that is widely distributed in Southern China extent of nest dismantling was quantified in increments of (MacKinnon and Phillipps 1999;Zhao2001). During the 10% from 10 to 100%. We divided the nest into ten equal breeding season, male and female birds build nests together portions from the top to the bottom, and each portion and males reduce the lengths of their tails, which are longer in equivalent to 10% was considered one unit. If the birds the wintering period (Ding et al. 2007; Zhang et al. 2007;Ding used materials from old nests to build new nests, the dis- et al. 2008). We found that the proportion of nest-dismantling tance between the two nests was measured using a laser behavior in yellow-bellied prinia was high and inconsistent rangefinder (TAJIMA LKT-F03, TJM Design between populations on mainland China and the island of Corporation, Tokyo, Japan; range 0–30 m, precision Taiwan. Therefore, we compared the nest-dismantling behav- 0.001 m). To compare the nest size and nest materials ior of yellow-bellied prinia in two study areas representing between the two study areas, we randomly selected 30 these two regions and investigated the adaptation of nest- nests from each area and measured the height, width, dismantling behavior of yellow-bellied prinia. and diameter of the opening and depth of the nests and recorded the type of nest material (Table 1).

Methods Data analysis Study areas A one-sample Kolmogorov-Smirnov test was used to analyze This study was conducted on mainland China and the island of the normality of the data. When the data were normally dis- Taiwan. In mainland China, the study was conducted in tributed, a t test or one-way analysis of variance (ANOVA) Nonggang National Nature Reserve (23°39′ N, 107°04′ E) in was used to compare the mean values; Welch’s t test was used Guangxi Province from April to July, 2010–2014. The area when variance was heterogenous. If the data were not normal- had a wide-open terrain with sugarcane Saccharum ly distributed, a non-parametric Mann-Whitney U test was officinarum as the main crop. The study area in Taiwan was conducted. All tests were two-tailed; differences were consid- in Shoufeng Township, Hualien County (23°51′ N, 121°31′ ered significant at P < 0.05, highly significant at P < 0.01, and E), and was studied during the same time as the area in main- not significant at P > 0.05. Statistical analysis was conducted land China. The area was mainly wild, weedy wasteland, and using IBM SPSS Version 21.0 (IBM Corp., Armonk, NY, the main plant species included Miscanthus floridulus, Bidens USA), and unless otherwise specified, all results are presented pilosa, and Pennisetum purpureum. Both study areas were as mean ± SD. acta ethol

Table 1 Comparison of nest parameters between mainland and Study Height (mm) Width (mm) Hole diameter Depth (mm) Number of plant N island prinia populations. Values area (mm) species are means ± SD Mainland 134.95 ± 6.71 70.05 ± 3.83 51.67 ± 2.08 51.96 ± 2.47 1 30 Island 136.32 ± 3.18 71.76 ± 4.35 52.03 ± 2.23 52.47 ± 2.75 9 30 t − 1.013 − 1.621 df 58 58 58 58 P 0.315 0.110 0.523 0.451

Results simple. The nest sizes did not differ between the two study areas (Table 1). Reproductive biology Nest-dismantling behavior Yellow-bellied prinias were common in both the study areas. The island population began nesting and laying eggs in early Parent birds removed nest material and built new nests in the April. In 2010, the first egg was laid on April 24 and on April vicinity usually after a failed reproduction due to predation 22 in 2011. During the 2 years, a total of 242 yellow-bellied (see Fig. 1 for examples of nest dismantling). In the island prinia nests were found. The mean time taken to build a new population, 71 dismantled nests were observed in the field, nest was 3.0 ± 0.5 days (n = 10). The nests were built in the accounting for 29.3% of the total nests (71/242). There was lower layers of Miscanthus or Pennisetum purpureum plants. no difference in the proportion of dismantled nests between – The birds laid 2 5 eggs, with an average of 3.3 ± 0.6 eggs per the years (chi-square test, χ2 = 0.391, df =1, P = 0.532; the nest (n = 100). The mean egg volume (Hoyt, 1979)was proportion of dismantled nests in 2010 (25.9%, 14/54) vs. 3 994.51 ± 81.27 mm . In the mainland population, a total of 2011 (30.3%, 57/188)), indicating that nest-dismantling be- 371 nests were found from 2010 to 2014, and nesting began havior was not due to chance in the island population, but a — in early April 14 days earlier than the island population. The common phenomenon in this area. The nest-dismantling be- – mean time taken to build a nest was 3.0 ± 0.5 days (n =12);3 havior mainly occurred during the peak of the breeding season 7 eggs were laid per nest, with an average of 4.6 ± 0.6 per nest (Fig. 2). Of the dismantled nests, 97.2% (69/71) followed a 3 (n = 100). The mean egg volume was 1042.24 ± 78.86 mm failed breeding, another 2.8% (2/71) were dismantled after a and the main nesting plant was Saccharum officinarum. successful breeding, of which one nest was completely dis- ’ Overall, the number of eggs per nest (Student s t test, t = mantled, and the other was half dismantled. − 15,139, df = 198, P < 0.001) and the egg volumes (t = Prinias removed the nest materials beginning at the top and 4.197, df =198, P < 0.001) in nests of the island population working towards the bottom of the nest. Some nests were were significantly smaller than in nests of the mainland completely dismantled, while others were only partially dis- population. mantled (Fig. 2). The nest materials from dismantled nests Yellow-bellied prinias on the island had a higher breeding were used to build new nests. Yellow-bellied prinias have very failure rate. Of 100 nests observed in 2010, 87% were strong territorial behavior; they usually built new nests close predated or damaged by humans and only 7% of nests were to the original nesting sites (Ding et al. 2008; Yang et al. confirmed to fledge young birds. In contrast, the predation rate 2014). Twenty-five nests found in the field were newly built in the mainland population was lower and the successful on plants very close to the old nest sites. The distance between fledging rate was 53.5% (31 out of 58 nests) in 2010. the old and the new nests was on average 3.66 ± 1.59 m (n = Comparison of the nest materials (Table 1)showedthatthe 25). Field observations showed that the mean time taken to island birds used only the top inflorescence of Miscanthus as a dismantle old nests and build new nests was 2.5 ± 0.5 days nest material, whereas the mainland birds used ten different (n =10),whichwas0.5–1.0 days shorter than the first nest types of materials, including sugarcane root, inflorescences of building time. Crassocephalum crepidioides and Miscanthus spp., elephant There was some variation in the extent of nest-dismantling grass Pennisetum purpureum and Imperata spp. leaves, plastic behavior among different pairs of adult birds. The majority debris, chicken feathers, rags, spider silk, and fine grass roots. (78.9%) of pairs dismantled only 10–50% of the nesting ma- The difference between the nesting materials used in each terial (Fig. 3); thus, nest-dismantling behavior was focused on χ2 population was highly significant ( = 123.200, df =9, the upper half of the nest, whereas the nesting material of the P < 0.001). The mainland birds used more diverse nesting lower part remained in its original position. In addition, we did materials, whereas that used by island birds was relatively not observe any yellow-bellied prinia reusing old nests. acta ethol

Fig. 1 Yellow-bellied prinia dismantling their nests in a Taiwanese field. a Four eggs in the nest on May 18, 2011. b Most of the nest material was removed after predation on May 25, 2011. c Nest dismantling process was completed by May 27, 2011

In the mainland population, only three dismantled nests Discussion were observed in 2013, with a nest-dismantling ratio of 0.81% (3/371). This was significantly lower than in the island The proportion of prinia pairs showing nest-dismantling be- population (chi-square test, χ2 = 112.315, df =1, P <0.001). havior on the island of Taiwan was higher than that on main- The nest material from all three of the dismantled nests was land China. Nest-dismantling behavior in birds has been re- reused to build new nests; the mean distance between the old ported previously (Root 1969; Snow and Snow 1979; and new nests was 3.59 ± 2.08 m (n =3). Sedgwick and Knopf 1988; VanderWerf 1998; Jones et al.

Fig. 2 The number of dismantled nests across the seasons in 2010 (total = 14/54) and 2011 (total = 57/188) in Taiwan acta ethol

(Hansell 2000). Therefore, the removal and reuse of suitable nesting materials from old nests saves kinetic energy and time that would otherwise be spent searching for new nesting materials of a similar type. The level of difficulty involved in searching for nest materials also influences the amount of energy invested by the parent birds. Nesting materials used by birds on the island were relatively simple compared to those used by birds on the mainland. Thus, over a short distance, it might have been more beneficial to reuse materials from the old nest. This may also explain why most yellow- bellied prinia did not leave the nest site following a failed breeding, but built a new nest close to the old site. Possible explanations for nest-dismantling behavior in yellow-bellied prinia might be to save time and energy in Fig. 3 The frequency histogram of the extent of nest dismantling in the searching for nesting materials. The time taken to build a Taiwan population (n =71) completely new nest was 3.0 ± 0.5 days, while the time taken to build a new nest using old nesting material was 2.5 days, which saved 0.5–1.0 days compared to the usual construction 2007;Lietal.2009;Slageretal.2012). The breeding ecology time. Dismantling of old nests and reusing the nesting material of yellow-bellied prinia has also been studied previously might be an adaptive strategy if it reduces the costs of nest (Ding et al. 2007, 2008; Lo and Cheng 2007; Zhang et al. building for parent birds (Gauthier and Thomas 1993; Nores 2007;Dingetal.2017). A recent study of the mainland pop- and Nores 1994; Jones et al. 2007). The clutch sizes of yellow- ulation showed that the brood sex ratio of the yellow-bellied bellied prinia on the island were significantly smaller than prinia was 1:1, and sex ratios of different nests were evenly those on the mainland, while egg volumes were bigger on distributed within the study area; however, nest-dismantling the island. This not only demonstrates Bisland syndrome^ behavior was not reported (Ding et al. 2017). From the field (MacArthur and Wilson 1967; Adler and Levins 1994; observations, we concluded that both male and female indi- Losos and Ricklefs 2009;Covas2012), but could also reflect viduals participated in nest dismantling and building of the a trade-off (Roff 1992). Reducing the number of eggs, allo- new nests, which was consistent with previous observations cating more resources and energy to somatic maintenance, and that males and females collaborate to build nests (Lo and potentially increasing the quality of future generations is a Cheng 2007; Ding et al. 2008). Nest-dismantling behavior good strategy to maximize individual fitness (Goodman was observed, albeit unequally, in both populations, which 1974; Barbraud and Weimerskirch 2001;Yangetal.2012). indicated the universality of this behavior in yellow-bellied Nest-dismantling behavior of parent birds was undoubtedly a prinia. It is likely that the local environmental factors result of the balance between saving energy and maximizing prompted the nest-dismantling behavior in the populations. individual fitness. Yellow-bellied prinias have strong territorial behavior and Yellow-bellied prinias mainly dismantled only the upper attack and chase away any intruders near their nests, such as half of the nests. The bottom half of the nests (cup portion cuckoos Cuculus saturatus, white-bellied thrush Turdus of the nests) was used for laying eggs, hatching, and housing pallidus, rufous-backed shrike Lanius schach,jayGarrulus nestlings and can retain parasites and dirt. Therefore, reusing glandarius, and hill turtledove Streptopelia orientalis (Yang the nesting material from the bottom part is not beneficial to et al. 2014). Intruders include predatory birds, parasitic birds, the health of young chicks (Mazgajski 2007). Only a few nests and individuals from mixed-species bird flocks (Goodale et al. (9.9%) were completely dismantled and the material used for 2015). Attacks on parasitic cuckoos are particularly aggres- building new nests. sive. The 25 pairs of breeding individuals in the Taiwan pop- Yellow-bellied prinias on the island had a higher predation ulation dismantled and rebuilt nests frequently. Although we and breeding failure rate than those of the mainland popula- did not mark the birds with bands, we speculated that birds tion (87 vs. 46%). Under the pressure of high-intensity preda- using old nest material to build a new nest were likely the tion, yellow-bellied prinia rapidly built nests to minimize the same pair that had dismantled an old nest. energetic costs of nesting, and once breeding failed, they Optimal foraging theory states that, under certain condi- quickly started again. This also indirectly explained why tions, natural selection will optimize the behavior of an organ- nest-dismantling frequency was higher during the peak breed- ism to maximize its fitness (Emlen 1966; MacArthur and ing season. Therefore, we suggested that predation pressure Pianka 1966; Schoener 1971). Birds usually use highly ste- should be one of the main reasons for nest-dismantling behav- reotypical movements to search for suitable nesting materials ior in the island population. acta ethol

Birds usually remain at successful breeding nest sites to from the University of California, Berkeley, USA, and Aiwu Jiang, Qiuli build new nests or avoid nest sites where reproduction failed Huang, Demeng Jiang, and Yungao Hu for their assistance with fieldwork in Guangxi. (Gavin and Bollinger 1988). Animals on islands usually have a higher breeding population density and stronger intraspecif- Funding information This work was supported by the National ic competition (MacArthur and Wilson 1967; Grant 1998; Natural Science Foundation of China (nos. 31660617 to LW, 31472013 Losos and Ricklefs 2009). Breeding areas were relatively and 31772453 to WL) and the Initial Fund Key Laboratories of Guizhou Province (grant no. 2011-4005) to LW. small for yellow-bellied prinia on the island—about 10 m2 per breeding pair (Lin 1985). Following a failed breeding, Compliance with ethical standards many pairs did not move out of their territory, but rebuilt nests nearby, demonstrating a high degree of fidelity to their terri- Ethical standards The studies reported in this paper conform to the tory. The relatively short distance between the old and new laws in the countries in which they were performed. Experimental proce- dures were in agreement with the Animal Research Ethics Committee of nests (ca. 4 m) may have facilitated the transfer of nesting Hainan Provincial Education Centre for Ecology and Environment, materials and might also explain the reuse of nesting mate- Hainan Normal University (permit no. HNECEE-2011-005). rials. When searching for nests in the field, we used the site of a dismantled nest to search for a new nest within a 5-m radius. Conflict of interest The authors declare that they have no conflicts of There are only a few examples of birds, such as the great reed interest. warbler Acrocephalus arundinaceus and brambling Fringilla montifringilla that lay and hatch eggs in the same nest after a failed breeding (Hafstad et al. 2005). More commonly, old References nests are rarely reused due to damage, infestation by parasites and bacteria, or increased predation risk (Mazgajski 2007). Adler GH, Levins R (1994) The island syndrome in rodent populations. Q Rev Biol 69(4):473–490. https://doi.org/10.1086/418744 This may explain why we did not find any yellow-bellied Andersson M (1982) Female choice selects for extreme tail length in a prinia reusing their old nests in our study areas. Unlike the widowbird. 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