Ornithol Sci 15: 1 – 14 (2016)

ORIGINAL ARTICLE Tail movements in —current evidence and new concepts

Christoph RANDLER#

Univ Education Heidelberg, Biology, INF 561-2,D-69120 Heidelberg, Germany, 0049622147734

ORNITHOLOGICAL Abstract Birds of a wide range of species show characteristic movements of their tail, often called tail flicking, tail wagging or tail flashing. Tail flicking refers to verti- SCIENCE cal up-and-down movements of the tail, while tail flashing is defined as a horizontal © The Ornithological Society movement, often including tail spreading. Here, I review proposed functions of such of Japan 2016 behaviour. Most relate to communication with conspecifics, predators or prey. Tail flashing may induce movement of the ’s prey that makes the prey more vulner- able to capture (‘prey-flushing’). Tail movements may signal to a predator that the signaller has detected it (‘perception advertisement’), or that the signaller is particu- larly alert or otherwise difficult to catch (‘quality advertisement’). Further, it may warn conspecifics of predators (‘alarm signal’), or it may advertise quality as a mate, signal social status, or aid in flock cohesion. This behaviour may, possibly, though it seems unlikely, represent a cue rather than a signal in that it benefits the receiver, but not the signaller. For each postulated function, I develop predictions stemming from that function, and interpret the available empirical evidence in the context of these predictions. I finish by synthesising our current state of knowledge and by identify- ing the future empirical studies that would most improve our understanding of this widespread but unjustly neglected avian behaviour.

Key words Alarm signal, Ambushing predator, Flock coherence, Tail flashing, Tail flicking, Tail wagging, Vigilance

Tail movements are present and obvious in many about tail movements in birds and offer new con- bird species, and often mentioned as traits in field cepts. The term “tail movement” will be used to guides, as in the case of the White Wagtail Motacilla describe any of the various behaviours that might be alba. These movements have been described using described as tail flashing, tail wagging, tail pump- different terms, such as tail flick, tail wag, tail flash, ing, tail movement, or wag display, where the tail is tail pump or tail up display. Although this behav- moved independently from the body in a non-flying iour is widespread, it has received little attention in bird. The direction and speed of movement, and the ornithology. Tail movements have been more often difference in the speed between any upward and investigated in mammals, such as the tail flick/flag downward stroke are not addressed here (see details of ungulates (Caro et al. 2004; Caro 2005). In orni- in Andrew 1956). thology, tail movements are often described during courtship display (Fitzpatrick 1998, 1999). However, Classification of tail movements most bird species that show tail movements do so Tail movements are diverse, and it would be help- throughout the year, not just in the breeding season. ful if workers in this field could agree on how to This kind of tail movements is the focus of the pres- describe these movements and how to name them. ent study. I used a systematic search through differ- I suggest defining tail flicking as a movement of the ent databases (for details see Appendix) to identify tail upwards and downwards on a vertical axis (see relevant papers. Table 1 for an overview). Flicking is different from In this paper, I will review proposed hypotheses side-to-side movements and spreading of the tail. The side-to-side-movements as shown in motmots (Received 14 April 2015; Accepted 17 June 2015) (Murphy 2006), could be described as pendulous tail # Corresponding author, E-mail: [email protected] movement, or for convenience, explicitly stated as

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Table 1. Overview over the tail movements and definitions. In bold: term used for the review.

Axis Tail Description Examples Possible function Tail flicking, Vertical unspread Up-and-downward wagtails, , Predator-prey Tail pumping, movement movement of the tail North American phoebes context, social tail wagging function Tail flashing, Horizontal spread horizontal fanning, Hooded Warbler, Prey flushing Tail fanning movement spreading of the Myioborus redstarts, Tail spreading rectrices, display Rhipidura fantails of conspicuous, contrasting plumage patches in the rectrices Pendulous Horizontal unspread Pendulous movement, Motmot Predator-prey movement axis side-to-side wagging communication

“side-to-side wagging”. Third, movements on a hori- functions for tail movements, but also discusses the zontal axis should be described as tail flashing which possibility that tail movements may have non-signal- includes tail fanning and tail spreading. Often these ling functions. movements involve display of conspicuous, contrast- ing plumage patches in the rectrices. They are also Functions of tail movements often associated with the spreading or drooping of Based on the theory of signalling, the the wings. Tail flashing might be further separated hypotheses drawn from the studies listed in the into two categories that include only very short peri- Appendix can be grouped in different ways: ods of flashing of less than 0.1 sec, and in contrast, A. First, in an intraspecific signalling context, tail fanning with longer periods. In this review, I will movements may be directed at potential mates or summarise both these movements under tail flashing. used in a social context (dominance/submission) or Also, tail wagging is defined as an independent in terms of flock-cohesion. movement of the tail, and not a movement of the B. Second, as an interspecific signal (in this case body, as for example in the Actitis sandpipers where directed at a predator) or as foraging enhancement. the birds do not flick or wag but rather move (bob) C. Thirdly, tail movements might be a cue rather the hind part of their body along with the tail. It than a signal. is also different from head bobbing (Fujita 2004) or nodding, which has an optokinetic function or is Group A: Intraspecific context controlled by biomechanical constraints. Research- Hypothesis A1: Tail movement is a sexual signal ers on this topic should describe the tail movements addressed at a potential mate. of their study species in detail, whether they fall in Intuitively, this hypothesis does not seem to apply the categories described here (following Table 1), or to year-round tail movement displays. In addition, if whether they involve combined movements, shown the signal is predominantly used in a sexual context, habitually or only in response to external stimuli, and then: should describe how the tail is moved (spreading, • it should be given during the presence of a sexual turning, twisting etc.). partner There are two hypotheses for the evolutionary ori- • there should be differences between males and gin of tail movements, suggesting evolution from females (given that in most birds the female is either vigorous hopping or leaping (Daanje 1950), the choosy sex), or non-ritualised intention movements indicating the • the rate should differ between reproductive intention to fly (Andrew 1956). Both hypotheses (adult) and pre-reproductive (juvenile) individu- assume evolution to perform a signalling function als (Spitznagel 1996), being higher in adults, with a sender and one or more intended receivers, • and there should be variation throughout the year both con- or heterospecific individuals (Searcy & and a high incidence of movements in the pre- Nowicki 2005). This review focuses on signalling breeding and breeding season or during pair for-

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mation. be reliably tested across conflicting dyads, rather than Evidence in favour of this hypothesis can be found each individual’s average behaviour. in the Common Gallinula chloropus, in Evidence against this hypothesis comes from which species females flicks their tails faster than Alvarez et al. (2006) who found that individual males (females are more actively engaged in mate moorhens with a high flick rate had a higher social acquisition) (Alvarez et al. 2006). In addition, flick- status. Also, Randler (2006, 2007) found no differ- ing was correlated with better body condition, and ence between adults versus juveniles in tail wag- this signal can be interpreted as being directed at ging rates in wagtails or tail flicking rates in -moor potential mates (Alvarez & Sanchez 2003, Alvarez et hens. In addition, rates of tail movements were al. 2006). Motmots Momotus spp. do not wag their higher in single individuals (Randler 2006, 2007) tails much outside the breeding season, also sug- and increased with increasing nearest neighbour dis- gesting a sexual function (Wagner 1950). However, tance (Randler 2007). In Eastern Phoebes, conspe- no differences in tail movements have been found cific playback did not evoke a higher or lower tail between adult and juvenile White Wagtails or Com- movement rate, which renders a social submission mon Moorhens (Randler 2006, 2007), or between hypothesis unlikely; because tail movement should the sexes in the Eastern Phoebe Sayornis phoebe either increase or decrease during encounters with a (Carder & Ritchison 2009), Turquoise-browed conspecific male (Carder & Ritchison 2009). There Motmot Eumomota superciliosa (Murphy 2006) or seems little evidence for tail movement as a submis- White-throated Dipper Cinclus cinclus (Spitznagel sion signal, although it may have this function in 1996). There is some evidence for sexual signalling species living at high densities and in large groups, in the , but not in the other species as in the case of the Dusky Moorhen. studied. If tail movements occur among mated pairs that remain together year-round, then this behaviour Hypothesis A3: Tail movements are used to coordi- may fall under hypothesis A3. In this case, a distinc- nate flock behaviour and movement. tion can be drawn in function between mate choice Tail movements make a bird conspicuous and and pair formation versus pair maintenance (see A3). may serve as a signal to conspecifics (Andrew 1956; Hashmi 1988) to keep flocks together and to coordi- Hypothesis A2: Tail movements are a signal of social nate movements. In mated pairs, it may serve for pair status. maintenance. According to Craig (1982), tail flicking is a signal • As tail movements are interpreted as intention of submission and he argues that a high flick rate movements, they should increase before take-off. signals submission. If tail flicking is a signal of sub- • If they are seen as being involved in some kind mission, then of flock-cohesion, the frequency of tail - move • it should be higher in less dominant or subordi- ments should be high before take-off and after nate individuals, landing and then decrease with time. • it should be shown year-round, • If they are used for flock coherence, they should • it should be shown in a social context and not be more frequent in gregarious species. when individuals are alone, Evidence in support of this hypothesis comes from • and tail flicking should decrease with an increas- the Mallard Anas platyrhynchos, where tail move- ing distance to the nearest neighbour. ments occur both as pre-flight and post-flight move- Evidence in favour of this hypothesis comes from ments (Hailman & Baylis 1991). In White-throated the Dusky Moorhen Gallinula tenebrosa, wherein Dippers, dipping movements are also more frequent social status and fighting ability are positively corre- before and after changing location (Spitznagel 1996). lated with the width and breadth of the frontal shield Evidence unsupportive of hypothesis A3 comes from (Crowley & Magrath 2004). Individuals with an elab- several studies that found that single birds flicked orated frontal shield are dominant, and individuals at a higher rate than individuals in groups, which is with a small frontal shield (commonly juveniles) tail contradictory (e.g. Woodland et al. 1980; Ryan et al. flicked more often than individuals with an elaborate 2006; Randler 2006, 2007; but see hypothesis C). shield (Ryan et al. 1996). However, the interpretation However, single birds may also make tail movements is slightly problematic when individuals are not con- at a higher rate to establish a flock. sistently dominant/subordinate. Therefore, it should

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Hypothesis A4: Tail movements as an alarm signal. deterrent signal, then Tail movements might be an alarm signal addressed • it should increase during an encounter with a to conspecifics. If tail movements are interpreted as predator, an alarm signal, they should occur: • it should influence the predator’s behaviour, e.g. • only during an encounter with a predator (and causing an attack to be abandoned, they should be absent in the absence of preda- • and it should be related to predator distance. tors), and Evidence supportive of this hypothesis comes from • when sexual and/or social mates or kin are pres- observational and experimental studies, showing that ent. tail movement rates increase when a predator is pres- Evidence for this hypothesis is found in a multitude ent or when it was experimentally represented by an of reports showing that tail movement rate increased acoustic or visual stimulus (see Wagner 1950; Andrew when a predator was present, either in observational 1956; Woodland et al. 1980; Alvarez 1993; Griffin or experimental studies (for details see hypothesis et al. 2005; Murphy 2006; Randler 2007; Jones & B1; Wagner 1950; Andrew 1956; Woodland et al. Whittingham 2008; Carder & Ritchison 2009; but 1980; Alvarez 1993; Griffin et al. 2005; Murphy see Griffin et al. 2005 for mixed evidence concerning 2006; Randler 2007; Jones & Whittingham 2008; playback vs. models). Tail movements should also Carder & Ritchison 2009). Evidence unsupportive of be related to predator distance (Fig. 1): they may this hypothesis comes from studies that showed that occur at a low baseline level (even in the absence of single individuals showed a higher rate of tail move- a predator) and should increase at a critical distance ments than individuals in groups (e.g. Woodland et at which the predator is still far enough to base the al. 1980; Murphy 2006; Ryan et al. 2006; Randler decision to attack on the signal. If the predator is too 2006, 2007). Further, alarm signals should be close, then tail movements should decline (or stop) directed to conspecifics only if a predator is present, and the individual should flee. Woodland et al. (1980) but individuals also showed tail movements when provide evidence for a relationship between predator predators were absent. In addition, Woodland et al. distance and tail flicking in Dusky Moorhen. Dusky (1980) and Alvarez (1993) argue that the white tails Moorhen increased flicking with a decreasing preda- of rails is oriented towards predators and not towards tor distance (see Fig. 1). conspecifics during flicking. As attacking predators Evidence unsupportive of this hypothesis comes are absent most of the time, tail movements should from the fact that individuals also flick when preda- not occur at a constant rate. These arguments render tors are apparently absent. However, it is very hard the intraspecifc alarm signal hypothesis unlikely, but to experimentally manipulate the environment so that conspecifics might use a signal addressed at a preda- predators are absent. It would be interesting to make tor (hypotheses B1 and B2) in the form of eavesdrop- comparisons between populations where predators ping. are absent or present.

Hypotheses B1-B3: Tail movements in a predator- prey context (interspecific context). Pursuit deterrence can be divided into two classes: Predator ‘perception advertisement’ in which the prey individ- distance ual signals to a predator that it has been detected, and ‘quality advertisement’ in which the prey individual signals that it is in good condition and thus difficult to catch (Caro 1986a, 1986b; Caro et al. 1995).

Hypothesis B1: Tail movements as signals to a preda- Tail movement rate tor that it has been detected (‘perception advertise- Fig. 1. Schematic representation of relationship between ment’). predator distance and tail movement rate. An individual may Tail movements may inform a predator that it has move at a given baseline when predators are absent or far been spotted, conveying the message that launching away. Then, movement increases with decreasing predator an attack without the element of surprise will not distance (not necessarily linearly) until prey stops tail move- pay the predator. If tail movement serves as a pursuit ment and flees.

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Hypothesis B2: Tail movements are a signal of alert- ment’). This hypothesis has the attraction that it has ness addressed at a potential ambushing predator the potential to explain intraspecifc variation in tail (‘quality advertisement’). movements among individuals. However, the mecha- Tail movements also occur, often instantaneously, nism that would keep such a signal honest is not even when predators are not obviously visible (or in currently fully resolved. ambush). The signal itself reflects individual differ- ences, for example in alertness or body condition (see Hypothesis B3: Tail movements are used to flush prey Spitznagel 1996; Alvarez & Sanchez 2003; Alvarez (foraging enhancement). et al. 2006; ‘quality advertisement’). If this hypoth- Tail movements are used to flush insect or arthro- esis is true, then tail movements pod prey that are hidden or less active during unfa- • should occur when predators are absent (or in vourable weather conditions; tail movements may ambush), flush insects, making them easier to catch. Tail move- • should be related to body condition, ments may often be combined with wing-flashing • should be related to alertness/vigilance. (e.g., Jablonski 1999; Jablonski et al. 2006). If tail Evidence in support of this hypothesis comes from movements are used to flush insect prey, then these studies reporting that flicking is shown year-round • should be used only during feeding bouts, not (Randler 2006, 2007), and is related to body condi- during perching or preening, tion (Alvarez et al. 2006). Some studies have showed • should be used year-round, a positive relationship between tail flicking and vigi- • should occur independently of the presence/ lance (Ryan et al. 1996; Alvarez et al. 2006; Randler absence of conspecifics or predators, 2006, 2007). Further, individuals nearer to protective • should be absent in perch-pounce species that cover flicked less (Alvarez 1993), perhaps because forage from a perch or in species that forage by protective cover leads to greater safety, which, in aerial sallying, turn, is expressed as a lower flicking rate. • should be dependent on weather conditions and Evidence unsupportive of this hypothesis comes the rate and catch rate should be in some way mainly from theoretical viewpoints: Movements related. should be a costly signal, furthermore they should Evidence for this hypothesis comes from: North- mostly be honest, and predators should respond ern Mockingbird Mimus polyglottus (Hailman accordingly (Hasson 1991; Spitznagel 1996). How- 1960), Painted Redstart Myioborus pictus (Jablonski ever, the cost of tail movements is not obviously high 1999), Slate-throated Redstart (Mumme et al. 2006), and cheating seems possible, but studies by Alvarez American Redstart Setophaga ruticilla (Robinson & et al. (2006) and Randler (2007) suggest that it is Holmes 1982), Hooded Warbler Setophaga citrina an honest indicator/signal of vigilance or alertness. (Mumme 2014), and Willie Wagtail (Rhipidura Also predators should learn rather quickly to ignore leucophrys; Jackson & Elgar 1993). Jackson and the signal if they are cheated. If a predator attacks Elgar (1993) found that Willie Wagtails moved their individuals flicking at different rates, and there is tails only during feeding and rarely during perching; no difference in catching success, then the predator also the rate was higher in the shade than in bright should not rely on the signal (see discussion about sunlight. In addition, there is good experimental evi- deception in Searcy & Nowicki 2005). The ‘quality dence from redstarts (Mumme 2002, 2014; Mumme advertisement’-hypothesis makes sense in birds that et al. 2006), which use their white tail feathers to are victims of surprise hunting predators that may flush insect prey. Experimental birds with darkened launch an attack in ambush because these signals tail feathers were significantly less successful in should be visible over a long distance (Hasson 1991). flush–pursuit foraging. Tail movements developed The predator may base its decision on the movement ontogenetically parallel with foraging efficiency rate if it honestly signals the quality of an individual, (Mumme 2014). either its vigilance or its escape capability. Vega- Evidence unsupportive of this hypothesis comes Redondo and Hasson (1993) suggested that the sig- from White Wagtails that wagged while preening nal does not communicate that the predator has been (Randler 2006), and Carder and Ritchison (2009) spotted (‘perception advertisement’, hypothesis B1), found no evidence to support the foraging enhance- but that the signaller is an individual of high quality ment hypothesis in Eastern Phoebes. There is some that would be difficult to catch (‘quality advertise- convincing evidence (especially from different exper-

5 C. RANDLER imental studies) that movements are used in prey efits from the response of others, then its behaviour is flushing, but tail movements cannot be explained best seen as a signal; otherwise it is a cue. solely by this hypothesis in most species. Possible non-communication functions of tail Hypothesis C: Tail movements are a cue of an indi- movements vidual’s perceived danger or alertness. That tail movements are not really a signal or even If tail movements are a cue, then they represent an a cue at all seems implausible for the species dis- undirected, uncontrolled nervous behaviour, and this cussed here. However, this possibility should be dis- differs from hypotheses in which tail movements are cussed in the case of investigations into species not considered to be a signal. That is, unlike a signal, previously researched. Such a hypothesis has not yet the communication function of the movement does been tested. For example, species moving on uneven not benefit the bird, but it does benefit those that or slippery surfaces might use tail movements to aid respond to detection of this movement. This hypoth- in balance. This may also explain why species living esis is based on the general assumption that vigilance near running water may flick and others not (Ern (which often involves head-up behaviour in birds) is 1989; Spitznagel 1996). Further, if tail movements a measure of perceived danger/predation. Many stud- are related to maintaining balance, then birds should ies have shown that vigilance correlates with preda- move their tails more frequently during windy con- tion risk (see Elgar 1989, Randler 2005a, 2005b). If ditions or when standing on more flexible perches. this assumption is true, then tail movements However, Carder and Ritchison (2009) found no such • should be correlated with aspects of the ecology relationship between wind speed or perch stability known to influence vigilance rate (e.g. distance and tail movement, but again, studies are scarce. to cover, group size, centre-edge effect), and they should increase with an increasing nearest neigh- DISCUSSION bour distance (in contrast to hypothesis A2). • there should be a measurable stress response cor- One promising hypothesis is that tail movements related with the tail movements. serve as a signal during an encounter with a preda- Evidence for this hypothesis comes from studies tor (‘perception advertisement’ [B1] and/or ‘quality that have shown correlations between many para- advertisement’ [B2]) and are directed to a potential meters that determine vigilance and flicking (e.g. ambushing predator (‘quality advertisement’), but Randler 2007). For example, group size was nega- also towards conspecifics (A4). However, further tively correlated with vigilance and tail movement; studies are needed to disentangle the different predic- individuals at a flock’s edge had higher vigilance tions related to the predator-prey context (see below). and tail movement rates, increasing nearest neigh- The signalling to an ambushing predator and the bour distances were correlated with an increasing flock maintenance hypotheses are refinements of pre- tail movement rate and increasing vigilance. Also, viously less developed concepts. The tail flashing individuals near cover moved their tails less and were movements, as shown by the Willie Wagtail or the less vigilant (Alvarez 1993; Ryan et al. 1996). The Myioborus redstarts may be more related to forag- fact that subdominant birds moved their tails more ing, especially for flushing insects. Thus, one could (Craig 1982, hypothesis A2) may result from the fact hypothesise that flicking (as defined in Table 1) may that dominant birds feed in safer places, for example function primarily in the predator-prey context, while nearer to cover or in the centre of a group, than less flashing seems more related to foraging behaviour. dominant birds (Craig 1982). This idea may also However, there are some exceptions to this rule, e.g., explain why single birds give so many tail move- the Rufous Bush Chat spreads its tail, but more likely ments. Tail movements as a cue of perceived danger in a predator-prey context (Alvarez & Sánchez 2003). may be exploited by conspecifics and/or heterospecif- Concerning predator-prey-relationships, there is ics (e.g., predators). Conspecifics should benefit from only limited experimental evidence and none includ- the action and use the cue for foraging decisions and ing the reaction of a predator. Evidence of response joining a group. Whether tail movements are best by signal receivers is required to prove that tail move- described as a cue or a signal (sensu Maynard Smith ments indeed serve as a signal. To test the predator- & Harper 2003) is difficult to evaluate without- fur related hypotheses, we urgently need to investigate ther experimental work. If the tail moving bird ben- the behaviour of predators and conspecifics. One step

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Table 2. Overview of the hypotheses, their key predictions and support for and against them. For further details, see Appendix.

Intraspecific hypotheses Evidence for Evidence against A1 sexual signal addressed toward a potential mate Prediction: differences between males and females Alvarez et al. (2006) Carder & Ritchison (2009) Murphy (2006) Prediction: high incidence of movements during pair for- Wagner (1950) mation Prediction: movements signal body condition Alvarez & Sanchez (2003) Alvarez et al. (2006) A2 signal of submission Prediction: higher rate in subordinate individuals Craig (1982) Alvarez et al. (2006) Ryan et al. (1996) Randler (2006) Prediction: movements should decrease with increasing Randler (2007) nearest neighbour distance Prediction: shown in a social context Randler (2007) A3 flock maintenance Prediction: movements should increase before take-off and Hailman & Baylis (1991) decrease with time after landing. Prediction: singeltons should show no tail moves Woodland et al. (1980) Ryan et al. (1996) Randler (2006, 2007) A4 alarm signal Prediction: occurs/increases during an encounter with a Wagner (1950) Griffin et al. (2005) predator Andrew (1956) Woodland et al. (1980) Alvarez (1993) Griffin et al. (2005) Murphy (2006) Randler (2007) Jones & Whittingham (2008) Carder & Ritchison (2009) Prediction: when sexual or social mates or kin are present Woodland et al. (1980) Murphy (2006) Ryan et al. (2006) Randler (2006, 2007) Interspecific hypotheses B1 ‘Perception advertisement’ Prediction: it should increase during an encounter with a Wagner (1950) Griffin et al. (2005) predator Andrew (1956) Woodland et al. (1980) Alvarez (1993) Griffin et al. (2005) Murphy (2006) Randler (2007) Jones & Whittingham (2008) Carder & Ritchison (2009) B2 signal of alertness addressed at predator (‘quality adver- tisement’)

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Prediction: rate is related to body condition Alvarez et al. (2006) Prediction: rate related to alertness/vigilance Alvarez (1993) Ryan et al. (1996) Alvarez et al. (2006) Randler (2006, 2007) B3 prey flushing Prediction: movements only during feeding bouts, not dur- Hailman (1960) Randler (2006) ing perching or preening Jablonski (1999) Carder & Ritchison (2009) Mumme et al. (2006) Mumme (2014) Robinson & Holmes (1982) Jackson & Elgar (1993) Prediction: movement rate should correlate with prey cap- Jablonski (1999) Randler (2006) ture rate Mumme et al. (2006) Mumme (2014) Jackson & Elgar (1993) C cue of perceived danger Prediction: movements should correlate with vigilance and Alvarez (1993) other parameters reflecting danger (group size, distance to Ryan et al. (1996) cover) Randler (2007) Non-communicative function Prediction: movements should depend on wind speed and/ Carder & Ritchison (2009) or perch stability forward would be to use video playbacks of individu- lower wag rate. als with different rates of tail movements, or an artifi- Another neglected area is the cost of tail move- cially animated robotic model to test this hypothesis. ments. It seems that this behaviour is not costly in One test could be the model test of Götmark and terms of energy expenditure, but may be costly in Unger (1994) using a model that tail flicks versus a terms of increasing conspicuousness to hidden preda- model that does not tail flick, and in a second test, tors). Therefore, cheating should be easy. However, models that tail flick at different rates. If predators a simple rule would help predators to estimate prof- choose the non-flicking or low-rate flicking model itability. If the signal is not honest, then predators during an attack, then that would provide some evi- should not base their pursuit decision on tail move- dence for the pursuit deterrent and ambushing preda- ments and simply ignore them. It is difficult to mea- tor function. It is also crucial to design studies that sure the costs of tail movements, but if a predator differentiate between the ‘quality-advertisement’ and is more likely to detect a model with a higher tail ‘perception advertisement’ hypotheses, but evidence movement rate, then this could be interpreted as a from birds and other vertebrates is scarce (Caro cost. 1986a, 2005; Ruxton et al. 2004). In general, when Concerning the prey flushing hypothesis, espe- signalling quality, there should be a larger inter- cially related to tail flashing (Table 1), there is evi- individual difference than when signalling percep- dence that the birds reveal their tail markings – which tion. Moreover, signalling perception would be more are usually hidden – by spreading their tails. Here, effective if it was more or less standardized (e.g. a there is some evidence that the tail markings indeed similar wag rate in all individuals would be sufficient flush prey because when dying them or darkening to address the predator). This could be investigated the white parts, foraging efficiency decreases (e.g., by looking at wag rates in different individuals at Mumme 2014). different times (repeatability), or in the same individ- Studies investigating the pair maintenance func- ual during different condition. For example, when a tion (as might occur for example in duetting, Hall previously-healthy individual is impaired experimen- 2004), should compare tail movements during differ- tally, the quality advertisement hypothesis predicts a ent times of the year. For example, tail movements

8 Tail movements in birds should be present before and after incubating, but in structuring the review. individuals of a pair might reduce their rate when the partner is incubating (e.g. in hole nesting birds) REFERENCES when the signal is unnecessary. Also, tail movement rate might increase after moving of an individual to Alvarez F (1993) Alertness signalling in two spe- signal the partner about their new location. cies. Anim Behav 46: 1229–1231. Apart from single-species studies, comparative Alvarez F & Sánchez C (2003) The features of distrac- evidence is scarce (Stang & McRae 2009). In their tion behaviour and their relationship with physical study, the authors found support for two conclusions: condition in Rufous Bush Chats. Ethol Ecol Evol 15: rail species with white undertail coverts were found 355–368. in open habitats and were mostly gregarious. Assum- Alvarez F, Sánchez C & Angulo S (2006) Relationships ing white tails evolved to enhance tail movement between tail-flicking, morphology, and body condi- tion in Moorhens. J Field Ornithol 77: 1–6. signals, they further conclude that the white under- Andrew RJ (1956) Intention movements of flight in cer- tail coverts evolved before gregariousness, suggest- tain passerines, and their use in systematics. Behav ing that the signal was first addressed at a predator, 10: 178–204. and then the species became social. Furthermore, Byrkjedal, I (1987) Antipredator behavior and breeding it would be interesting to compare species forag- success in greater golden plover and eurasian dot- ing by perch-pounce or aerial sallying techniques terel. Condor 89: 40–47. with ground hunting species and herbivorous spe- Carder ML & Ritchison G (2009) Tail pumping by East- cies. Insect feeders foraging on the ground or in foli- ern Phoebes: an honest, persistent predator-deterrent age might use tail movements to flush prey, perch- signal? J Field Ornithol 80: 163–170. pounce species feeding at long-distances should not Caro T (2005) Anti-predator defence in mammals and show tail movements, and these should be absent in birds. Chicago University Press, Chicago. seed eaters. Assessing the pair maintenance function Caro TM (1986a) The functions of stotting: a review of could be done by comparing species where pairs stay the hypotheses. Anim Behav 34: 649–662. together year-round versus species with seasonally Caro TM (1986b) The functions of stotting in Thom- pairs. Finally, one could explain whether the tail is son’s gazelles: some tests of the predictions. Anim elaborated, either in length, feather structure, or con- Behav 34: 663–684. trasting colour pattern and relate this to tail move- Caro TM, Graham CM, Stoner CJ & Vargas JK (2004) ments (Fitzpatrick 1998). These suggestions indicate Adaptive significance of antipredator behaviour in several open questions that might open new avenues artiodactyls. Anim Behav 67: 205–228. of research for both comparative and single-species Caro TM, Lombardo L, Goldizen AW & Kelly M analyses. (1995) Tail-flagging and other antipredator signals in white-tailed deer: new data and synthesis. Behav Ecol 6: 442–450. CONCLUSION Craig JL (1982) On the evidence for a “pursuit deter- rent” function of alarm signals of swamphen. Am Nat The review shows that tail movements may serve 119: 753–755. different functions in different taxa. Furthermore, Crowley CE & Magrath RD (2004) Shields of offence: the overview clearly indicates that future studies are signalling competitive ability in the dusky moorhen, rewarding, because tail movements may be depen- Gallinula tenebrosa. Aust J Zool 52: 463–474. dent on the behaviour, feeding place, foraging tac- Daanje A (1950) On locomotory movements in birds tics, and social nature, such as gregariousness, of the and the intention movements derived from them. different species. The several hypotheses mentioned Behav 3: 48–98. in this paper are not mutually exclusive, and there- Elgar MA (1989) Predator vigilance and group size in fore, there is a possibility of multiple functions of tail mammals and birds: a critical review of the empirical movement even in one species. evidence. Biol Rev 64: 13–33. Ern H (1989) Convergent patterns in the behaviour of ACKNOWLEDGMENTS birds inhabiting fast running water. Ecol Birds 11: 201–207. I am grateful to Graeme Ruxton and the reviewers who Fitzpatrick S (1998) Birds’ tails as signalling devices: provided very helpful comments on the manuscript and helped markings, shape, length, and feather quality. Am Nat

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151: 157–173. Hooded Warbler. Auk 131: 141–149. Fitzpatrick S (1999) Tail length in birds in relation to Mumme RL, Galatowitsch ML, Jabłoński PG, Sta- tail shape, general flight ecology and sexual selection. warczyk TM & Cygan JP (2006) Evolutionary sig- J Evol Biol 12: 49–60. nificance of geographic variation in a plumage-based Fujita M (2004) Kinematic parameters of the walking foraging adaptation: An experimental test in the slate- of herons, ground-feeders, and waterfowl. Comp Bio- throated redstart (Myioborus miniatus). Evolution 60: chem Physiol Part A 139: 117– 124. 1086–1097. Götmark F & Unger U (1994) Are conspicuous birds Murphy TG (2006) Predator-elicited visual signal: why unprofitable prey? Field experiments with hawks and the turquoise-browed motmot wag-displays its rack- stuffed prey species. Auk 111: 251–262. eted tail. Behav Ecol 17: 547–553. Griffin AS, Savani RS, Hausmanis K & Lefebvre L Murphy TG (2007) Dishonest ‘preemptive’ pursuit- (2005) Mixed-species aggregations: zenaida doves, deterrent signal or misfired signal? Why the- tur Zenaida aurita, respond to the alarm calls of carib quoise-browed motmot wag-displays its tail before grackles, Quiscalus lugubris. Anim Behav 70: 507– feeding nestlings. Anim Behav 73: 965–970. 515. Randler C (2005a) Vigilance during preening in Coots Hailman JP (1960) A field study of the mockingbird’s Fulica atra. Ethology 111: 169–178. wingflashing behavior and its association with forag- Randler C (2005b) Coots Fulica atra reduce their vigi- ing. Wilson Bull 72: 346–357. lance under increased competition. Behav Proc 68: Hailman JP & Baylis JR (1991) Post-flight tail-wagging 173–178. in the mallard. J Field Ornithol 62: 226–229. Randler C (2006) Is tail wagging in white wagtails, Hall ML (2004) A review of hypotheses for the function Motacilla alba, an honest signal of vigilance? Anim of avian duetting. Behav Ecol Sociobiol 55: 415–430. Behav 71: 1089–1093. Hashmi D (1988) Zur möglichen Konvergenz wip- Randler C (2007) Observational and experimental evi- pender Körperbewegungen bei Vögeln. J Ornithol dence for the function of tail flicking in Eurasian 129: 463–466. moorhen Gallinula chloropus. Ethology 113: 629– Hasson O (1991) Pursuit-deterrent signals: communica- 639. tion between prey and predator. TREE 10: 325–329. Robinson SK & Holmes RT (1982) Foraging behavior Jablonski PG (1999) A rare predator exploits prey escape of forest birds: the relationship among search tactics, behavior: the role of tail-fanning and plumage con- diet, and habitat structure. Ecology 63: 1918–1931. trast in foraging of the painted redstart (Myioborus Ruxton GD, Sherrat TN & Speed MP (2004) Avoiding pictus). Behav Ecol 10: 7–14. attack. Oxford University Press, Oxford. Jabłoński PG, Lasater K, Mumme RL, Borowiec M, Ryan DA, Bawden KM, Bermingham KT & Elgar MA Cygan JP, Pereira J & Sergiej EWA (2006) Habitat- (1996) Scanning and tail flicking in the Australian specific sensory-exploitative signals in birds: Propen- Dusky Moorhen (Gallinula tenebrosa). Auk 113: sity of dipteran prey to cause evolution of plumage 499–501. variation in flush-pursuit insectivores. Evolution 60: Searcy WA, Nowicki S (2005) The evolution of 2633–2642. Animal Communication. Princeton University Press, Jackson J & Elgar MA (1993) The foraging behaviour Princeton. of the willie wagtail Rhipidura leucophrys. Emu 93: Spitznagel A (1996) Why dippers dip – on the adaptive 284–286. significance of fitness-signalling and predator-pursuit Jones KA & Whittingham MJ (2008) Anti-predator sig- deterring movements in birds. Zool Anz 235: 89–99. nals in the chaffinch Fringilla coelebs in response to Stang AT & McRae SB (2009) Why some rails have habitat structure and different predator types. Ethol- white tails: the evolution of white undertail plumage ogy 114: 1033–1043 and antipredator signaling. Evol Ecol 23: 943-961. Maynard Smith J & Harper D (2003) Animal Signals. Vega-Redondo F & Hasson O (1993) A game-theoretic Oxford University Press, Oxford. model of predator-prey signalling. J Theoret Biol Mumme RL (2002) Scarce tactics in a neotropical war- 162: 309–319. bler: white tail feathers enhance flush-pursuit foraging Wagner HO (1950) Observations on the racquet-tips of performance in the slate-throated redstart (Myioborus the motmot’s Tail. Auk 67: 387–389. miniatus). Auk 119: 1024–1035. Woodland DJ, Jaafar Z &Knight ML (1980) The “pur- Mumme RL (2014) White tail spots and tail-flick- suit deterrent” function of alarm signals. Am. Nat. ing behavior enhance foraging performance in the 115: 748–753.

10 Tail movements in birds D D D C D C C C C D D D C C D D D No relation between wind speed and tail pumping wind speed and tail between No relation No relation between perch stability and pumping No difference in tail flicking after conspecific playbacks Tail Tail pumping similar in perch times ≤ 30 and > 30 s No difference in foray distances between perch times of ≤15 s, 16-30 s, ≥ 30 s Tail Tail flick increased after presentation of a live owl No difference between males and females No difference Tail Tail flicking rate higher towards cat than to hawk model Tail Tail flick more in open habitats – [acts as a visual signal] More wags on ground (foraging) compared to perches. More wags in the shade than in bright sunshine No differences between feeding and preening between feeding No differences and Wagging pecking negatively correlated Single birds wag more Wagging and scanning are correlated Wagging Flicking is correlated with other measures group of size, nearest neighbour danger distance, centre-edge effect...) (e.g. Flicking increased with increasing neighbour distance Hypothesis Balance hypothesis Signal of submission/ signal of aggression Prey flushing Predator Sexual signalling Predator Predator Prey flushing Prey flushing Signal of submissionadults and juveniles between No difference Predator Predator Signal of submission Signal of submissiondid not differ Adult and juveniles Smith 1969, Carder & Ritchison 2009 Carder & Ritchison 2009 Carder & Ritchison 2009 Carder & Ritchison 2009 Carder & Ritchison 2009 Jones & Whittingham 2008 Jones & Whittingham 2008 Jackson & (1993) Elgar Jackson & (1993) Elgar Randler (2006) Randler (2006) Prey flushing Randler (2006) Conspecific alarm signal Randler (2006) Randler (2007) Randler (2007) Conspecific alarm signal Single birds show high flick rate Randler (2007) Randler (2007) Aspect Source O E playback O E O E E O O O O O O O O O O Type Flick Flick Flick Flick Flick Flick Flick Flash Flash Flick Flick Flick Flick Flick Flick Flick Flick Overview of tail movement studies. Type of movement: Flick = Flicking, Flash = Flashing, Pendulous = Pendulous movements, see Table 1 for detailed Species Eastern Phoebe Sayornis phoebe Eastern Phoebe Sayornis phoebe Eastern Phoebe Sayornis phoebe Eastern Phoebe Sayornis phoebe Eastern Phoebe Sayornis phoebe Chaffinch Fringilla coelebs Chaffinch Fringilla coelebs Willie Wagtail Willie Rhipidura leucophrys Willie Wagtail Willie Rhipidura leucophrys White Wagtail Motacilla alba White Wagtail Motacilla alba White Wagtail Motacilla alba White Wagtail Motacilla alba Moorhen Gallinula chloropus Moorhen Gallinula chloropus Moorhen Gallinula chloropus Moorhen Gallinula chloropus Appendix S1. explanations. Aspect: O = Observational study, E = Experimental T study, = Theoretical discussion. Last column: D = hypothesis declined, C = hypothesis confirmed.

11 C. RANDLER C C C C C C C D D C D D C D D D D D - - - - Dishonest signal to a predator – wags before enters the nest Tarsus asymmetry and blood parameters correlated with flick Relation between scanning and flicking (groups of four or more). At edge of group, flicking was (insignificantly) higher Singletons flicked at higher rate ing Females flick faster (females more engaged in mate acquiring) Birds without developed frontal shield flicked at higher rates Wagging increases Wagging after playback of predator calls Tail Tail flicking correlates with vigilance yet they also flicked Wagging decreases Wagging after playback of conspecific calls Tarsus Tarsus asymmetry and blood parameters correlated with flick ing Wagging higher in singletons Wagging Wagging did Wagging not change after heterospecific playbacks When no predator nearby, wagging is seldom shown display Wag when predator occurs birds Motmots did not move closer or closer started to predator) mobbing (moved Wag Wag display occurs during feeding the nestlings, wag is per formed at place where nestlings could not detect it where nestlings could not detect formed at place No sexual differences; presence/absence of mate had no influ ence on wag display, no difference between size of food item and wag display - - - - Pursuit deterrent (ambush) deterrent Pursuit Signal Sexual signalling: ling status (body condition) to a conspecific mate? Sexual signalling Predator or flock-coher ence Signal of submission Predator Predator Signal of submission ity) Signal of submission Signal of submission (interspecific) Predator Self-preservation (such as eliciting mobbing) Sexual signallingand females males between did not differ Wagging Directed towards nest lings tise quality to current or potential mate) Alvarez et al. (2006) Ryan et al. 1996 Ryan et al. 1996 Randler (2007) Alvarez et al. (2006) Ryan et al. 1996 Conspecific alarm signal Tail flicking and scanning were not correlated in single birds Randler (2007) Alvarez et al. (2006) Predator (signalling qual - Randler (2007) Conspecific alarm signal Alvarez et al. (2006) Randler (2007) Murphy (2006) Murphy (2006) Conspecific alarm signal Motmots wag when conspecifics are absent and in unpaired Murphy (2006) Murphy (2006) Murphy (2007) Murphy (2007) Sexual signalling (adver Murphy (2007) O O O E O O E O E O E Flick Flick Flick Flick Flick Flick Flick Flick Flick Flick Flick Pend E Pend E Pend E Pend E Pend O Pend O Pend O Moorhen Gallinula chloropus Dusky Moorhen Gallinula tenebrosa Dusky Moorhen Gallinula tenebrosa Moorhen Gallinula chloropus Moorhen Gallinula chloropus Dusky Moorhen Gallinula tenebrosa Moorhen Gallinula chloropus Moorhen Gallinula chloropus Moorhen Gallinula chloropus Moorhen Gallinula chloropus Moorhen Gallinula chloropus turquoise-browed motmot Eumomota superciliosa turquoise-browed motmot ( Eumomota ) superciliosa turquoise-browed motmot ( Eumomota ) superciliosa turquoise-browed motmot ( Eumomota ) superciliosa Turquoise-browed Turquoise-browed motmot ( Eumomota ) superciliosa Turquoise-browed Turquoise-browed motmot ( Eumomota ) superciliosa Turquoise-browed Turquoise-browed motmot ( Eumomota ) superciliosa

12 Tail movements in birds C C C D C C D - - C D C - - C/D - - Move tail when observer is spotted but not when observer hidden is Tail Tail flicking increased after predator approached flicking awayTail from group was faster than towards the group Vigilance and tail flick correlated Group size negatively correlated with vigilance Moorhens near cover flicked at lower rate compared to distant from cover They flicked away more often, than conspecifics when orientedtowards Tail Tail flicking increased after a predator approached. In singletons tail flick was faster away from cover (in direction of potential predator) Vigilance and tail flick correlated Flicking increases when predator (human) approaches towards intruder Rump patch oriented Birds (in groups) near intruder flicked more than when distant from intruder. Tail Tail flick increases near dominant birds, signal to seems submission balance out the frontal shield. Less dominant birds feed away from cover at the edge, there fore higher flicking rate Orienting towards the predator is simply because of good posi tion for running away. The closer approached towards the dominant birds resulted in higher flicking (byproduct) Tail Tail flick increases after playback of heterospecific alarm call Tail flick did not increase when presentedmodel predator with a Fitness-signalling/alertness and pursuit deterrent Neither age nor sex dependent, signal occurs also often when alone Shown in relation with locomotion (before/after). as Wagging visual signal in noisy habitats the location Signal before and after changing - Flock coherence Pre- and post flight – not associated with tail movement Predator Predator Predator Predator Signal of submission Predator Predator Predator Locomotory function Flock coherence Flock coherence/locomo tory function Hailman & Baylis 1991 Wagner 1950 Wagner Alvarez 1993 Alvarez 1993 Conspecific alarm signal Alvarez 1993 Woodland et al. (1980) al. et Woodland Woodland et al. (1980)al. et Woodland Conspecific alarm signal Solitary birds responded similar to birds in groups Griffin et al. 2005 Spitznagel (1996) Spitznagel (1996) Flock coherence Spitznagel (1996) Hashmi 1988 Hashmi 1988

O O O E E E predator model playback T T Pend O Flick Flick Flick Flick Flick T Craig 1982 Flick T Craig 1982 Flick -O Dip O Pend O Dip O Anas platyrhynchos Motmot Moorhen Purple Gallinule Eastern Swamphen Porphyrio porphyrio Eastern Swamphen Porphyrio porphyrio Eastern Swamphen Porphyrio porphyrio Eastern Swamphen Porphyrio porphyrio Zenaida dove Zenaida aurita Dipper Cinclus cinclus Dipper Cinclus cinclus Dipper Cinclus cinclus Mallard

13 C. RANDLER C C C C C C C ” OR “tail movement” OR “wag display” * ” OR “tail pump * Infrequent and absent out of the breeding season Tail Tail flicking increased when a predator was present Flicking was faster when a predator was at the nest: correlated with flicking body condition C: Tail C: Tail fanning flushes prey When predators approach nest (parental defense, distraction display?) Tail-flicking behavior codevelops with independent foraging in juveniles and is a significant positive predictor of juvenile foraging performance. Predator deterrence, distraction display ” OR “tail flick * Sexual signalling Predator Predator Tail Tail display: flicks tail upwards, then spreads: “raise tail and fan” (orig - inal in Hailman 1960) Tail Tail flagging (showing white undertail coverts)– when predator approaches Wagner 1950 Wagner Andrew (1960) Andrew (1960) Locomotory function Higher when on tree than when on ground Andrew (1960) Flock coherence Tail flick represents flight intention (flock-coherence) Alvarez & Sanchez (2003) Hailman (1960) Byrkjedal (1987) E E E E O O Pend O Flick Flick Flick Flash Flash O/E Jablonski (1999) Prey flushing Flash O/E Mumme (2014) Prey flushing because these databases are specifically ornithological. retrieved SORA 11 citations and OWL 2 records (search: 3.2.2009). The search was update * ) in Scopus (Elsevier) on 3.2.2009. This yielded 19 titles, and basically 9 documents were of relevance. From these documents, in a second round, * OR avian OR bird * * Motmot Buntings Buntings and many other passerines Buntings Buntings and many other passerines Buntings Buntings and many other passerines Cercotrichias Cercotrichias galactotes Hooded warbler Setophaga citrina Mockingbird Mimus polyglottus Dotterel Charadrius morinellus Paineted Redstart Myioborus pictus AND (avian all references have been scrutinised (the abstracts) to yield further studies, and in a third round the In references addition, of all the papers second that round cited have the been 9 titles scrutinised of (snowball the system). first round have been examined. Inthe term bird addition, SORA and OWL have been checked using similar search terms, but without on 27.5.2015 and one additional reference was retrieved and incorporated. The following search terms have been used in a search of title-abstract-keywords: (“tail wag

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