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Plastering mud around the entrance hole affects the estimation of threat levels from nest predators in Eurasian Nuthatches

Plastering mud around the entrance hole affects the estimation of threat levels from nest... Background: For cavity-nesting birds, the nest entrance plays an important role in preventing predators from accessing nests. Several species of nuthatches use mud to narrow the entrance of cavities. In theory, the smaller the entrance hole size, the more effective it is against predators; however, few studies have tested whether narrowing the entrance hole size can affect the estimation of threat levels from nest predators in cavity-nesting birds. Methods: Using dummy experiments, we tested whether Eurasian Nuthatches (Sitta europaea, narrow the entrance hole of cavities) and Cinereous Tits (Parus cinereus, do not narrow the entrance hole, as a control) perform different nest defence behaviours against Common Chipmunks (Tamias sibiricus, small nest predator) and Red Squirrels (Sciurus vulgaris, larger nest predator). Results: Both nuthatches and tits exhibited stronger response behaviours (high dummy response scores) against chipmunks than against squirrels. Compared with tits, nuthatches exhibited more aggressive behaviours to chip- munks, but their responses to squirrels were similar. Conclusions: Nest defence behaviours of nuthatches to chipmunks differed from tits, and the results suggested that nuthatches might estimate threat levels of nest predators according to their narrowed entrance-hole size. Keywords: Cavity-nesting birds, Entrance-hole size, Eurasian Nuthatches, Nest defence behaviour, Nest predator Background risk levels of predators (Lima et al. 2005; Yorzinski and Nest predation is the most important factor imped- Vehrencamp 2009; Yorzinski and Platt 2012; Mahr et al. ing successful breeding in birds (Ricklefs 1969; Mar- 2015; Suzuki 2015; Maziarz et  al. 2018). Although nest tin 1995; Caro 2005; Lima 2009). Under such selection defence by parents can increase the survival possibil- pressure, birds have evolved complex anti-predation ity of offspring, it also costs defenders in terms of time strategies to protect their nests and perform specific and energy expenditure and injury or death caused by nest defence behaviours when facing different types or predators (Montgomerie and Weatherhead 1988). Both underestimating or overestimating the danger posed by a predator can be detrimental for parents (Caro 2005). Therefore, parent birds should choose the right nest *Correspondence: kqzhang01@hotmail.com; wanght402@nenu.edu.cn Jilin Engineering Laboratory for Avian Ecology and Conservation defence strategy when defending their offspring against Genetics, School of Life Sciences, Northeast Normal University, predators, including making a decision about whether Changchun 130024, China and how intensively to defend their nests (e.g. Caro School of Zoological Science, Jilin Agricultural Science and Technology University, Jilin 132109, China 2005; Mahr et al. 2015). Full list of author information is available at the end of the article © The Author(s) 2021. 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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 in a credit line to the data. Yu et al. Avian Res (2021) 12:58 Page 2 of 6 Distinguishing different predators and their threat box to approximately 2.5  cm by using mud. Common levels is the first step to effectively avoid predators. The Chipmunks (Tamias sibiricus, chipmunk hereafter) and body size of a predator is a reliable indicator of the threat Red Squirrels (Sciurus vulgaris, squirrel hereafter) are level that it poses to birds (Swaisgood et al. 1999), and it nest predators of nesting cavity, as they enter nests to is especially important in some predators that they are destroy the nest cup and eat the eggs and chicks. Chip- quite similar in overall appearance as well as body shape munks can enter most nest boxes easily due to their (Beránková et  al. 2014). It has been shown that vari- small body size (head-and-body length is approximately ous bird species can distinguish between raptors differ - 130  cm), but squirrels (approximately 200  cm, Piao ing in size and then perform appropriate antipredator et  al. 2013) are rarely found in nest boxes with entrance response behaviours (Evans et  al. 1993; Templeton et  al. hole sizes < 4.5  cm. Here, we tested whether Eurasian 2005; Courter and Ritchison 2010). However, many fac- Nuthatches perform different nest defence behaviours tors, such as habitat, nest stage, sex, nest type and preda- against chipmunks and squirrels according to their tor location, may influence and cause changes in nest adjusted entrance hole size. If mud around the entrance defence behaviour of birds (Burger 1992; Ritchison 1993; prevents nest predators from entering, we expected nut- Møller et al. 2016; Crisologo and Bonter 2017). For exam- hatches to exhibit stronger nest defence behaviours in ple, alarm calling rates increased with the nesting stage in chipmunks than in squirrels. Southern House Wrens (Troglodytes musculus) (Fasanella and Fernández 2009). Methods Generally, cavity-nesting birds are better protected Study area and subjects against nest predator’s attacks than open-cup nesters Our experiments were carried out in Zuojia Nature (Martin and Li 1992), as nest entrance can play a role in Reserve (44°1′–45°0′ N, 126°0′–126°8′ E) in Jilin, north- preventing predator’s access to nests (Wesołowski 2002). eastern China. The vegetation within the study area was However, nest predation is still the main cause of repro- diverse, with a continental monsoon climate and four dis- ductive failure for cavity-nesting species (Lima 2009). tinct seasons in the temperate zone, although the exist- Some predators can enter the nest cavity if the entrance ing forest was secondary (E et  al. 2019; Liu et  al. 2019). of a hole is sufficiently large, such as chipmunks, snakes We attached nest boxes to trees approximately 3–4  m and small owls (Solheim 1984; Suzuki 2011; Yu et  al. above the ground, and the number of nest boxes dis- 2020). A cavity with a small entrance size can prevent tributed in Zuojia was maintained at approximately 450 more predators from entering and plundering the nest per year (Yu et  al. 2017a). The entrance hole size of an than a cavity with a large entrance size (Wesołowski original artificial nest box in our study area was 4.5  cm. 2002). Therefore, the body size of a nest predator, in the - However, woodpeckers often peck holes in nest boxes, ory, should indicate the level of threat that they pose to which results in expansion of the entrance hole size up cavity-nesting birds. to a maximum of 6.5 cm. If a pecked nest box can still be Secondary cavity-nesting species are unable to excavate used by birds, we will not replace it. Thus, the range of their own nest holes, and they depend on cavities created the entrance hole size of an artificial nest box in our study by primary excavators (e.g., woodpeckers) and natural area was 4.5 to 6.5 cm. decay processes (Newton 1994). Most secondary cavity- During the breeding season, the total number of nests nesting species build their nests, which are placed at the used by birds in the study area was approximately 180 base of the cavity, and do not adjust the entrance of holes, (including 10–20 pecked nest boxes) per year. In addi- such as the Mandarin Duck (Aix galericulata). Several tion to secondary cavity-nesting birds, rodent chipmunks Sitta nuthatches have the ability to narrow the cavity and squirrels are also bred in artificial nest boxes. Based entrance by plastering mud around the openings (Mat- on our observations, the population size of squirrels thysen 1998; Wesołowski and Rowiński 2004; Strubbe was slightly larger than that of chipmunks. The num - and Matthysen 2009). In theory, a smaller entrance hole bers of nest boxes used by chipmunks and squirrels size should give nuthatches an advantage as protection were approximately 10–15 nests and 1–2 nests per year, against larger predators (Wesołowski 2002). However, respectively. The nest boxes were checked at intervals of few studies have tested whether narrowing the entrance 5–7  days from March to July to determine occupancy, hole size can affect the estimation of threat levels from and we classified boxes with at least one egg as occupied nest predators in cavity-nesting birds. (E et al. 2019). Eurasian Nuthatches (Sitta europaea, nuthatches here- Previous studies found that nuthatches exhibit signifi - after) breed in nest boxes (the range of the entrance hole cantly different nest defence behaviours than terrestrial size was 4.5 to 6.5  cm, see details below) in our study and aerial nest predators (Matthysen 1998; Sun et  al. area. They usually  narrow the entrance hole of a nest 2017; Nad’o et  al. 2018). They usually exhibit specific Yu  et al. Avian Res (2021) 12:58 Page 3 of 6 aggressive behaviours in terrestrial vertebrates, such as the model, response scores or attack numbers were the hovering over and spreading out wings and tails (Sun dependent variable, whereas bird species, treatment and et al. 2017). Therefore, we did not pose any other species order of treatment exposure were treated as fixed terms, dummy to nuthatches as a neutral or negative control and individuals distinguishing birds’ nests were random in this study. Instead, we chose another cavity-nesting terms. If there was a significant effect of bird species and bird species, Cinereous Tits (Parus cinereus, tits hereaf- treatment, we further performed post hoc pairwise com- ter), as a positive control. Nuthatches and tits are small parisons between species and treatments. To reduce the cavity-nesting birds with similar body sizes. Tits do not probability of type I errors, Bonferroni correction was adjust the entrance hole, while nuthatches use mud to used to adjust P values (P.adjust function in the R pack- narrow the entrance. Here, we compared the intensity age stats, Rice 1989; Yu et al. 2017b). of defence behaviours of nuthatches and tits to the same nest predators. Results The dummy response scores of nuthatches and tits dif - fered significantly between species (CLMMs, χ = 10.50, Dummy experiments P = 0.001) and treatments (χ = 20.16, P < 0.001), while During the nestling period of Eurasian Nuthatches there were no significant effects of trial order ( χ = 0.02, (n = 17 nests) and Cinereous Tits (n = 20 nests, 6 of the P = 0.88) on dummy response scores. The dummy 20 nesting boxes were pecked by woodpeckers), we pre- response scores of nuthatches (adjusted P < 0.001) and tits sented taxidermic dummies of Common Chipmunks (adjusted P = 0.047) were sufficiently stronger to chip - (small nest predator, 2 models) and Red Squirrels (large munks than to squirrels (Fig. 1). In addition, the dummy nest predator, 2 models) above the nest boxes. The tri - response scores of nuthatches to chipmunks were suffi - als were conducted during sunny days between 8:30 a.m. ciently stronger than those of tits to chipmunks (adjusted and 5:00 p.m., from May 10 to June 1, 2019, and each nest P < 0.001). The dummy response scores of nuthatches and received two dummy presentations in  a random order. tits to squirrels were similar (adjusted P = 1.000). Video recorders were set up to record the experimen- The number of attacks of nuthatches and tits differed tal process. We scored the dummy responses (response significantly between species (GLMMs, χ = 12.96, scores hereafter) of nuthatches and tits on a five-point P < 0.001) and treatments (χ = 63.52, P < 0.001), while scale: (i) entered the nest; (ii) produced alarm calls dur- there were no significant effects of trial order ( χ = 2.52, ing stationary observation; (iii) produced alarm calls with P = 0.11) on attack numbers. Nuthatches attacked agitated skipping and flicking of wings; (iv) approached chipmunks significantly more strongly than squir - the rodent closely and hovered over it, spreading their rels (adjusted P < 0.001, Fig.  2). In contrast, tits rarely wings and tail, or performed attack behaviour with no attacked chipmunks and squirrels (adjusted P = 1.000). physical encounter; and (v) performed attack behaviour with physical impact (Liang and Møller 2015; Yu et  al. 2017a; 2019). As the birds often attacked nest preda- tors, we also quantified aggressive behaviour by count - ing the number of contact attacks of focal parent birds (attack numbers hereafter, we counted the exact number of attacks indoors by playing back the video). This ena - bled us to determine the primary target of attacks of the defending parents. Statistical analysis All data were analysed using R 3.6.1 software (http:// www.r- proje ct. org). For the response scores (ranked response, 5 levels) of nuthatches and tits, cumulative link mixed models (CLMMs, clmm in R package ordi- nal) with logit-link function were used, and we used two-tailed likelihood ratio tests to obtain P values. For attack numbers of nuthatches and tits, generalized lin- ear mixed models (GLMMs, glmer in R package lme4) Fig. 1 Response of Eurasian Nuthatches (Sitta europaea) and Cinereous Tits (Parus cinereus) to Common Chipmunks (Tamias with a Poisson error structure and log-link function were sibiricus, a small nest predator) and Red Squirrels (Sciurus vulgaris, a used, and we calculated P values using Wald Chi-square larger nest predator) tests with the Anova function in the car package. In Yu et al. Avian Res (2021) 12:58 Page 4 of 6 The number of attacks of nuthatches to chipmunks more efficient and result in successfully deterring preda - were greater than those of tits to chipmunks (adjusted tors from the brood. However, anti-predator behaviour P = 0.001). The number of attacks of nuthatches and tits is usually energetically taxing (Krams and Krama 2002), to squirrels were similar (adjusted P = 1.000). and defending parents experience risk of injury or death (Brunton 1986; Montgomerie and Weatherhead 1988; Sordahl 1990). Here, specific attacking behaviours against Discussion the more dangerous chipmunks were most likely an anti- In our study, both nuthatches and tits exhibited stronger predator strategy for nuthatches, which may help them response behaviours (high dummy response scores) to to reduce the energy costs of unnecessary aggressive chipmunks than to squirrels. For parents, nest defence behaviours (Polak 2013; Kryštofková et al. 2011; Yu et al. behaviours (e.g., defensive displays and direct attacks) 2016). Based on our field observations, tits were unlikely may enhance their reproductive success (Montgomerie to succeed in protecting their nest contents from invad- and Weatherhead 1988). However, decision-making in ing nest predators by performing aggressive behaviours. active nest defence is quite a complex process, and threat Then, enacting displays with a moderate or low degree levels of predators to broods should be taken into account of aggression to nest predator chipmunks and squir- (Kleindorfer et  al. 2005). Chipmunks and squirrels pose rels could enable tits to avoid unnecessary investment in the same kind of nest predation threat to cavity birds, as costly attacks (Polak 2013). they can enter nests to destroy the nest contents. How- In this study, dummy response scores and attack num- ever, chipmunks are major nest predators in our study bers of nuthatches to chipmunks were significantly higher area, and squirrels may occasionally exhibit opportunis- than those of tits to chipmunks, while the response tic omnivory. Even nuthatches used mud to narrow their behaviours of nuthatches and tits to squirrels were simi- entrance hole, which could completely prevent squirrels lar. Parental behaviours are selected to maximize lifetime but not chipmunks from entering because chipmunks reproductive success, and nest defence intensity of parent could remove a part of the mud to gain access to enter birds will also be influenced by the benefit for the current the cavity (Wesołowski 2002). Our study results indi- brood versus future reproduction (Trivers 1972; Smith cated that nuthatches and tits could discriminate rodents 1977). Both Eurasian Nuthatches and Cinereous Tits are differing in size, and the predatory threat of chipmunks short-lived birds and have similar lifespans, but the pos- to their offspring was higher than that of squirrels. sibility of repeating a lost brood during one breeding sea- The number of attacks could reflect the degree of son differs between them. The population of Cinereous aggressiveness of the attacks (Fuchs et  al. 2019). In our Tits in our study area can produce a second brood imme- study, nuthatches attacked chipmunks significantly more diately after the failure of the first brood effort, while Eur - strongly than squirrels (Fig.  2), while tits rarely attacked asian Nuthatches only produce one large brood per year. them. Parents attacking nest predators directly may be u Th s, nuthatches should have a stronger incentive to attempt to drive dangerous nest predators away through active nest defence behaviours (Curio 1978) because sav- ing energy for future broods is a rather unlikely strategy. For tits, the probability of re-nesting may play a major role in their risk taking; therefore, they might be at less risk for their current brood than a bird with a lower re- nesting potential (Curio et al. 1984; Ghalambor and Mar- tin 2000, 2001). Conclusions Nuthatches and tits exhibited different nest defence behav - iours against the same nest predators, and the results showed that those two species implemented different nest defence strategies. If a nest intruder does not repre- sent an immediate threat to the nest, it is more advanta- geous for nest owners to refrain from aggressive behaviour (Kryštofková et  al. 2011). Moreover, the compromise Fig. 2 The number of attacks of Eurasian Nuthatches and Cinereous between current and future reproduction should be taken Tits to Common Chipmunks and Red Squirrels. Error bars represent into account for defence intensity towards a threat posed standard error of the mean to the offspring (Caro 2005). Results of the present study Yu  et al. Avian Res (2021) 12:58 Page 5 of 6 Courter JR, Ritchison G. Alarm calls of tufted titmice convey information about suggested that nuthatches might estimate threat levels of predator size and threat. Behav Ecol. 2010;21:936–42. nest predators according to their narrowed entrance-hole Crisologo TL, Bonter DN. Defending the weak: parental defense peaks when size. Future studies should determine if mud around the chick vulnerability is greatest in the herring gull Larus argentatus. Ethol- ogy. 2017;123:113–22. entrance can play an important role in preventing nest Curio E. The adaptive significance of avian mobbing. I. Teleonomic hypotheses predators with different sizes from entering, which in turn and predictions. Z Tierpsychol. 1978;48:175–83. may help us to understand the functions of plastering mud Curio E, Regelmann K, Zimmermann U. The defence of first and second broods by great tit Parus major parents: a test of predictive sociobiology. Z in nuthatches. Tierpsychol. 1984;66:101–27. Evans C, Macedonia J, Marler P. Eec ff ts of apparent size and speed on the Acknowledgements response of chickens, Gallus gallus, to computer-generated simulations of We are grateful to Dongxu Li and Junlong Yin for assistance with fieldwork. aerial predators. Anim Behav. 1993;46:1–11. We also thank Zuojia Nature Reserve for their support and permit to carry out Fasanella M, Fernández GJ. Alarm calls of the southern house wren Troglodytes this study. musculus: variation with nesting stage and predator model. J Ornithol. 2009;150:853–63. Authors’ contributions Fuchs R, Veselý P, Nácarová J. How to study predator recognition. In: Fuchs R, HW, KZ and J. Yu conceived the idea and formulated questions. JF, GY and Veselý P, Nácarová J, editors. Predator recognition in birds. The use of key CS performed the experiments. JF and LZ analyzed data. J. Yu and LZ wrote features. Switzerland: Springer International Publishing; 2019. the manuscript. J. Yao contributed substantial materials. HW, KZ and J. Yu Ghalambor CK, Martin TE. Parental investment strategies in two species of contributed resources and funding. All authors read and approved the final nuthatch vary with stage-specific predation risk and reproductive effort. manuscript. Anim Behav. 2000;60:263–7. Ghalambor CK, Martin TE. Fecundity-survival trade-offs and parental risk-taking Funding in birds. Science. 2001;292:494–7. This work is supported by the National Natural Science Foundation of China Kleindorfer S, Fessl B, Hoi H. 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Parental investment and sexual selection. In: Campbell B, editor. Sexual selection and the descent of man. Chicago: Aldine Publishing Company; 1972. p. 136–79. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Avian Research Springer Journals

Plastering mud around the entrance hole affects the estimation of threat levels from nest predators in Eurasian Nuthatches

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Springer Journals
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Copyright © The Author(s) 2021
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2053-7166
DOI
10.1186/s40657-021-00294-1
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Abstract

Background: For cavity-nesting birds, the nest entrance plays an important role in preventing predators from accessing nests. Several species of nuthatches use mud to narrow the entrance of cavities. In theory, the smaller the entrance hole size, the more effective it is against predators; however, few studies have tested whether narrowing the entrance hole size can affect the estimation of threat levels from nest predators in cavity-nesting birds. Methods: Using dummy experiments, we tested whether Eurasian Nuthatches (Sitta europaea, narrow the entrance hole of cavities) and Cinereous Tits (Parus cinereus, do not narrow the entrance hole, as a control) perform different nest defence behaviours against Common Chipmunks (Tamias sibiricus, small nest predator) and Red Squirrels (Sciurus vulgaris, larger nest predator). Results: Both nuthatches and tits exhibited stronger response behaviours (high dummy response scores) against chipmunks than against squirrels. Compared with tits, nuthatches exhibited more aggressive behaviours to chip- munks, but their responses to squirrels were similar. Conclusions: Nest defence behaviours of nuthatches to chipmunks differed from tits, and the results suggested that nuthatches might estimate threat levels of nest predators according to their narrowed entrance-hole size. Keywords: Cavity-nesting birds, Entrance-hole size, Eurasian Nuthatches, Nest defence behaviour, Nest predator Background risk levels of predators (Lima et al. 2005; Yorzinski and Nest predation is the most important factor imped- Vehrencamp 2009; Yorzinski and Platt 2012; Mahr et al. ing successful breeding in birds (Ricklefs 1969; Mar- 2015; Suzuki 2015; Maziarz et  al. 2018). Although nest tin 1995; Caro 2005; Lima 2009). Under such selection defence by parents can increase the survival possibil- pressure, birds have evolved complex anti-predation ity of offspring, it also costs defenders in terms of time strategies to protect their nests and perform specific and energy expenditure and injury or death caused by nest defence behaviours when facing different types or predators (Montgomerie and Weatherhead 1988). Both underestimating or overestimating the danger posed by a predator can be detrimental for parents (Caro 2005). Therefore, parent birds should choose the right nest *Correspondence: kqzhang01@hotmail.com; wanght402@nenu.edu.cn Jilin Engineering Laboratory for Avian Ecology and Conservation defence strategy when defending their offspring against Genetics, School of Life Sciences, Northeast Normal University, predators, including making a decision about whether Changchun 130024, China and how intensively to defend their nests (e.g. Caro School of Zoological Science, Jilin Agricultural Science and Technology University, Jilin 132109, China 2005; Mahr et al. 2015). Full list of author information is available at the end of the article © The Author(s) 2021. 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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 in a credit line to the data. Yu et al. Avian Res (2021) 12:58 Page 2 of 6 Distinguishing different predators and their threat box to approximately 2.5  cm by using mud. Common levels is the first step to effectively avoid predators. The Chipmunks (Tamias sibiricus, chipmunk hereafter) and body size of a predator is a reliable indicator of the threat Red Squirrels (Sciurus vulgaris, squirrel hereafter) are level that it poses to birds (Swaisgood et al. 1999), and it nest predators of nesting cavity, as they enter nests to is especially important in some predators that they are destroy the nest cup and eat the eggs and chicks. Chip- quite similar in overall appearance as well as body shape munks can enter most nest boxes easily due to their (Beránková et  al. 2014). It has been shown that vari- small body size (head-and-body length is approximately ous bird species can distinguish between raptors differ - 130  cm), but squirrels (approximately 200  cm, Piao ing in size and then perform appropriate antipredator et  al. 2013) are rarely found in nest boxes with entrance response behaviours (Evans et  al. 1993; Templeton et  al. hole sizes < 4.5  cm. Here, we tested whether Eurasian 2005; Courter and Ritchison 2010). However, many fac- Nuthatches perform different nest defence behaviours tors, such as habitat, nest stage, sex, nest type and preda- against chipmunks and squirrels according to their tor location, may influence and cause changes in nest adjusted entrance hole size. If mud around the entrance defence behaviour of birds (Burger 1992; Ritchison 1993; prevents nest predators from entering, we expected nut- Møller et al. 2016; Crisologo and Bonter 2017). For exam- hatches to exhibit stronger nest defence behaviours in ple, alarm calling rates increased with the nesting stage in chipmunks than in squirrels. Southern House Wrens (Troglodytes musculus) (Fasanella and Fernández 2009). Methods Generally, cavity-nesting birds are better protected Study area and subjects against nest predator’s attacks than open-cup nesters Our experiments were carried out in Zuojia Nature (Martin and Li 1992), as nest entrance can play a role in Reserve (44°1′–45°0′ N, 126°0′–126°8′ E) in Jilin, north- preventing predator’s access to nests (Wesołowski 2002). eastern China. The vegetation within the study area was However, nest predation is still the main cause of repro- diverse, with a continental monsoon climate and four dis- ductive failure for cavity-nesting species (Lima 2009). tinct seasons in the temperate zone, although the exist- Some predators can enter the nest cavity if the entrance ing forest was secondary (E et  al. 2019; Liu et  al. 2019). of a hole is sufficiently large, such as chipmunks, snakes We attached nest boxes to trees approximately 3–4  m and small owls (Solheim 1984; Suzuki 2011; Yu et  al. above the ground, and the number of nest boxes dis- 2020). A cavity with a small entrance size can prevent tributed in Zuojia was maintained at approximately 450 more predators from entering and plundering the nest per year (Yu et  al. 2017a). The entrance hole size of an than a cavity with a large entrance size (Wesołowski original artificial nest box in our study area was 4.5  cm. 2002). Therefore, the body size of a nest predator, in the - However, woodpeckers often peck holes in nest boxes, ory, should indicate the level of threat that they pose to which results in expansion of the entrance hole size up cavity-nesting birds. to a maximum of 6.5 cm. If a pecked nest box can still be Secondary cavity-nesting species are unable to excavate used by birds, we will not replace it. Thus, the range of their own nest holes, and they depend on cavities created the entrance hole size of an artificial nest box in our study by primary excavators (e.g., woodpeckers) and natural area was 4.5 to 6.5 cm. decay processes (Newton 1994). Most secondary cavity- During the breeding season, the total number of nests nesting species build their nests, which are placed at the used by birds in the study area was approximately 180 base of the cavity, and do not adjust the entrance of holes, (including 10–20 pecked nest boxes) per year. In addi- such as the Mandarin Duck (Aix galericulata). Several tion to secondary cavity-nesting birds, rodent chipmunks Sitta nuthatches have the ability to narrow the cavity and squirrels are also bred in artificial nest boxes. Based entrance by plastering mud around the openings (Mat- on our observations, the population size of squirrels thysen 1998; Wesołowski and Rowiński 2004; Strubbe was slightly larger than that of chipmunks. The num - and Matthysen 2009). In theory, a smaller entrance hole bers of nest boxes used by chipmunks and squirrels size should give nuthatches an advantage as protection were approximately 10–15 nests and 1–2 nests per year, against larger predators (Wesołowski 2002). However, respectively. The nest boxes were checked at intervals of few studies have tested whether narrowing the entrance 5–7  days from March to July to determine occupancy, hole size can affect the estimation of threat levels from and we classified boxes with at least one egg as occupied nest predators in cavity-nesting birds. (E et al. 2019). Eurasian Nuthatches (Sitta europaea, nuthatches here- Previous studies found that nuthatches exhibit signifi - after) breed in nest boxes (the range of the entrance hole cantly different nest defence behaviours than terrestrial size was 4.5 to 6.5  cm, see details below) in our study and aerial nest predators (Matthysen 1998; Sun et  al. area. They usually  narrow the entrance hole of a nest 2017; Nad’o et  al. 2018). They usually exhibit specific Yu  et al. Avian Res (2021) 12:58 Page 3 of 6 aggressive behaviours in terrestrial vertebrates, such as the model, response scores or attack numbers were the hovering over and spreading out wings and tails (Sun dependent variable, whereas bird species, treatment and et al. 2017). Therefore, we did not pose any other species order of treatment exposure were treated as fixed terms, dummy to nuthatches as a neutral or negative control and individuals distinguishing birds’ nests were random in this study. Instead, we chose another cavity-nesting terms. If there was a significant effect of bird species and bird species, Cinereous Tits (Parus cinereus, tits hereaf- treatment, we further performed post hoc pairwise com- ter), as a positive control. Nuthatches and tits are small parisons between species and treatments. To reduce the cavity-nesting birds with similar body sizes. Tits do not probability of type I errors, Bonferroni correction was adjust the entrance hole, while nuthatches use mud to used to adjust P values (P.adjust function in the R pack- narrow the entrance. Here, we compared the intensity age stats, Rice 1989; Yu et al. 2017b). of defence behaviours of nuthatches and tits to the same nest predators. Results The dummy response scores of nuthatches and tits dif - fered significantly between species (CLMMs, χ = 10.50, Dummy experiments P = 0.001) and treatments (χ = 20.16, P < 0.001), while During the nestling period of Eurasian Nuthatches there were no significant effects of trial order ( χ = 0.02, (n = 17 nests) and Cinereous Tits (n = 20 nests, 6 of the P = 0.88) on dummy response scores. The dummy 20 nesting boxes were pecked by woodpeckers), we pre- response scores of nuthatches (adjusted P < 0.001) and tits sented taxidermic dummies of Common Chipmunks (adjusted P = 0.047) were sufficiently stronger to chip - (small nest predator, 2 models) and Red Squirrels (large munks than to squirrels (Fig. 1). In addition, the dummy nest predator, 2 models) above the nest boxes. The tri - response scores of nuthatches to chipmunks were suffi - als were conducted during sunny days between 8:30 a.m. ciently stronger than those of tits to chipmunks (adjusted and 5:00 p.m., from May 10 to June 1, 2019, and each nest P < 0.001). The dummy response scores of nuthatches and received two dummy presentations in  a random order. tits to squirrels were similar (adjusted P = 1.000). Video recorders were set up to record the experimen- The number of attacks of nuthatches and tits differed tal process. We scored the dummy responses (response significantly between species (GLMMs, χ = 12.96, scores hereafter) of nuthatches and tits on a five-point P < 0.001) and treatments (χ = 63.52, P < 0.001), while scale: (i) entered the nest; (ii) produced alarm calls dur- there were no significant effects of trial order ( χ = 2.52, ing stationary observation; (iii) produced alarm calls with P = 0.11) on attack numbers. Nuthatches attacked agitated skipping and flicking of wings; (iv) approached chipmunks significantly more strongly than squir - the rodent closely and hovered over it, spreading their rels (adjusted P < 0.001, Fig.  2). In contrast, tits rarely wings and tail, or performed attack behaviour with no attacked chipmunks and squirrels (adjusted P = 1.000). physical encounter; and (v) performed attack behaviour with physical impact (Liang and Møller 2015; Yu et  al. 2017a; 2019). As the birds often attacked nest preda- tors, we also quantified aggressive behaviour by count - ing the number of contact attacks of focal parent birds (attack numbers hereafter, we counted the exact number of attacks indoors by playing back the video). This ena - bled us to determine the primary target of attacks of the defending parents. Statistical analysis All data were analysed using R 3.6.1 software (http:// www.r- proje ct. org). For the response scores (ranked response, 5 levels) of nuthatches and tits, cumulative link mixed models (CLMMs, clmm in R package ordi- nal) with logit-link function were used, and we used two-tailed likelihood ratio tests to obtain P values. For attack numbers of nuthatches and tits, generalized lin- ear mixed models (GLMMs, glmer in R package lme4) Fig. 1 Response of Eurasian Nuthatches (Sitta europaea) and Cinereous Tits (Parus cinereus) to Common Chipmunks (Tamias with a Poisson error structure and log-link function were sibiricus, a small nest predator) and Red Squirrels (Sciurus vulgaris, a used, and we calculated P values using Wald Chi-square larger nest predator) tests with the Anova function in the car package. In Yu et al. Avian Res (2021) 12:58 Page 4 of 6 The number of attacks of nuthatches to chipmunks more efficient and result in successfully deterring preda - were greater than those of tits to chipmunks (adjusted tors from the brood. However, anti-predator behaviour P = 0.001). The number of attacks of nuthatches and tits is usually energetically taxing (Krams and Krama 2002), to squirrels were similar (adjusted P = 1.000). and defending parents experience risk of injury or death (Brunton 1986; Montgomerie and Weatherhead 1988; Sordahl 1990). Here, specific attacking behaviours against Discussion the more dangerous chipmunks were most likely an anti- In our study, both nuthatches and tits exhibited stronger predator strategy for nuthatches, which may help them response behaviours (high dummy response scores) to to reduce the energy costs of unnecessary aggressive chipmunks than to squirrels. For parents, nest defence behaviours (Polak 2013; Kryštofková et al. 2011; Yu et al. behaviours (e.g., defensive displays and direct attacks) 2016). Based on our field observations, tits were unlikely may enhance their reproductive success (Montgomerie to succeed in protecting their nest contents from invad- and Weatherhead 1988). However, decision-making in ing nest predators by performing aggressive behaviours. active nest defence is quite a complex process, and threat Then, enacting displays with a moderate or low degree levels of predators to broods should be taken into account of aggression to nest predator chipmunks and squir- (Kleindorfer et  al. 2005). Chipmunks and squirrels pose rels could enable tits to avoid unnecessary investment in the same kind of nest predation threat to cavity birds, as costly attacks (Polak 2013). they can enter nests to destroy the nest contents. How- In this study, dummy response scores and attack num- ever, chipmunks are major nest predators in our study bers of nuthatches to chipmunks were significantly higher area, and squirrels may occasionally exhibit opportunis- than those of tits to chipmunks, while the response tic omnivory. Even nuthatches used mud to narrow their behaviours of nuthatches and tits to squirrels were simi- entrance hole, which could completely prevent squirrels lar. Parental behaviours are selected to maximize lifetime but not chipmunks from entering because chipmunks reproductive success, and nest defence intensity of parent could remove a part of the mud to gain access to enter birds will also be influenced by the benefit for the current the cavity (Wesołowski 2002). Our study results indi- brood versus future reproduction (Trivers 1972; Smith cated that nuthatches and tits could discriminate rodents 1977). Both Eurasian Nuthatches and Cinereous Tits are differing in size, and the predatory threat of chipmunks short-lived birds and have similar lifespans, but the pos- to their offspring was higher than that of squirrels. sibility of repeating a lost brood during one breeding sea- The number of attacks could reflect the degree of son differs between them. The population of Cinereous aggressiveness of the attacks (Fuchs et  al. 2019). In our Tits in our study area can produce a second brood imme- study, nuthatches attacked chipmunks significantly more diately after the failure of the first brood effort, while Eur - strongly than squirrels (Fig.  2), while tits rarely attacked asian Nuthatches only produce one large brood per year. them. Parents attacking nest predators directly may be u Th s, nuthatches should have a stronger incentive to attempt to drive dangerous nest predators away through active nest defence behaviours (Curio 1978) because sav- ing energy for future broods is a rather unlikely strategy. For tits, the probability of re-nesting may play a major role in their risk taking; therefore, they might be at less risk for their current brood than a bird with a lower re- nesting potential (Curio et al. 1984; Ghalambor and Mar- tin 2000, 2001). Conclusions Nuthatches and tits exhibited different nest defence behav - iours against the same nest predators, and the results showed that those two species implemented different nest defence strategies. If a nest intruder does not repre- sent an immediate threat to the nest, it is more advanta- geous for nest owners to refrain from aggressive behaviour (Kryštofková et  al. 2011). Moreover, the compromise Fig. 2 The number of attacks of Eurasian Nuthatches and Cinereous between current and future reproduction should be taken Tits to Common Chipmunks and Red Squirrels. Error bars represent into account for defence intensity towards a threat posed standard error of the mean to the offspring (Caro 2005). Results of the present study Yu  et al. Avian Res (2021) 12:58 Page 5 of 6 Courter JR, Ritchison G. Alarm calls of tufted titmice convey information about suggested that nuthatches might estimate threat levels of predator size and threat. Behav Ecol. 2010;21:936–42. nest predators according to their narrowed entrance-hole Crisologo TL, Bonter DN. Defending the weak: parental defense peaks when size. Future studies should determine if mud around the chick vulnerability is greatest in the herring gull Larus argentatus. Ethol- ogy. 2017;123:113–22. entrance can play an important role in preventing nest Curio E. The adaptive significance of avian mobbing. I. 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Parental investment and sexual selection. In: Campbell B, editor. Sexual selection and the descent of man. Chicago: Aldine Publishing Company; 1972. p. 136–79. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions

Journal

Avian ResearchSpringer Journals

Published: Nov 2, 2021

Keywords: Cavity-nesting birds; Entrance-hole size; Eurasian Nuthatches; Nest defence behaviour; Nest predator

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