Journal of Ornithology

, Volume 159, Issue 2, pp 555–563 | Cite as

Breath rate patterns in precocial Northern Lapwing (Vanellus vanellus) chicks in the wild

  • Zuzana Karlíková
  • Tereza Kejzlarová
  • Miroslav Šálek
Original Article


Individual-specific reaction to stressful situations may reveal various, individual-specific features, including personality. Breath rate and its change during and after handling [handling stress (HS) test] has been used to test individual response to stress. In previous laboratory research, the HS test has revealed a continuous decrease from peak values immediately after catching, which was consistent in adults of precocial and altricial species. Because of opposite trends in nestlings versus adults in altricial birds, we ask what breath rate pattern appears in precocial chicks in natural conditions? Advanced development during their early ontogeny compared to altricials could lead to breath rates similar to adults, but the effect of age, (in)experience, as well as environmental conditions, such as ambient temperature, may significantly shape breath rate patterns in chicks in different ways than in adults. In this study, we examined patterns in breath rate in response to HS in chicks of different age in a precocial wader, the Northern Lapwing (Vanellus vanellus) in the wild. Factors responsible for variation were simultaneously identified. We show that breath rate significantly dropped after visual isolation in a textile bag, a pattern similar to that in adult birds, and increased with the age of chicks as well as with higher ambient temperature. Breath rate was individually repeatable, but did not reflect individual behaviour observed before capture. Our results suggest that, when controlled for ambient temperature and time before catching, the breath rate pattern has the potential to be used as a useful HS test for neonatal Northern Lapwing chicks in the field.


Handling stress test Breathing Breath frequency Natural conditions Wader Visual isolation 


Muster in der Atemfrequenz freilebender, nestflüchtender Kiebitzküken ( Vanellus vanellus )

Individuell spezifische Reaktionen auf Stresssituationen können unterschiedliche individuell spezifische Merkmale wie Persönlichkeit aufzeigen. Die Atemrate und ihre Veränderung während und nach dem Handling (Handling-Stresstest) wurden in der Vergangenheit dazu verwendet, die individuelle Stressantwort zu testen. In früheren Untersuchungen unter Laborbedingungen hat dieser Handling-Stresstest bei adulten Vögeln von nestflüchtenden und nesthockenden Arten konsistent einen kontinuierlichen Abfall von den Höchstwerten unmittelbar nach dem Fang gezeigt. Weil Nestlinge und Altvögel bei nesthockenden Vögeln entgegengesetzte Trends aufweisen, stellt sich die Frage, welches Muster in der Atemfrequenz in Nestflüchter-Küken unter natürlichen Bedingungen auftreten. Ein Entwicklungsvorsprung gegenüber Nesthockern während der früheren Ontogenese könnte zu ähnlichen Atemfrequenzen wie bei Altvögeln führen, aber der Effekt von Alter, (mangelnder) Erfahrung sowie Umweltbedingungen wie der Umgebungstemperatur könnte die Atemfrequenzmuster der Küken deutlich anders als die der Altvögel beeinflussen. In der vorliegenden Studie untersuchten wir die Atemfrequenz als Antwort auf Handling-Stress bei unterschiedlich alten Kiebitzküken (Vanellus vanellus), einer nestflüchtenden Watvogelart. Gleichzeitig bestimmten wir die Faktoren, die für die Variation verantwortlich waren. Wir zeigen, dass die Atemfrequenz nach visueller Isolation in einem Beutel deutlich abfiel, ein Muster vergleichbar mit dem der Altvögel, wohingegen sie mit dem Alter der Küken und mit erhöhter Umgebungstemperatur zunahm. Die Atemfrequenz war individuell wiederholbar, spiegelte aber nicht das vor dem Fang beobachtete, individuelle Verhalten wieder. Unsere Ergebnisse legen nahe, dass das Atemfrequenzmuster das Potential hat, als ein nützlicher Freilandtest für Handling-Stress bei frisch geschlüpften Kiebitzküken verwendet zu werden, wenn man die Umgebungstemperatur und die Zeit vor dem Fang kontrolliert.


When in danger, animals trigger hormonal, physiological and behavioural (re)actions which help them to cope with the threat (Romero 2004). Integral components of the stress reaction are the hypothalamic–pituitary–adrenal system (responsible for the release of glucocorticoids, a type of steroid hormone) and the sympathetic nervous system (responsible for releasing epinephrine and norepinephrine) (Reeder and Kramer 2005). The direct way of testing a stress reaction in many vertebrates, including birds, is to analyse levels of glucocorticoids in blood plasma (Sapolsky et al. 2000). However, such a procedure requires bleeding, which may increase the stress experienced by the animal. When intense and repeated, sampling may have sub-lethal effects (van Oers and Carere 2007; Fair and Jones 2010), in particular on small and young animals, for which the necessary amount of blood collected for analysis may represent a significant portion of the total volume. In addition, subsequent analyses also require additional time and financial cost. Therefore, especially in the field, non-invasive simple methods utilising directly measurable manifestations of the sympathetic nervous system, such as breath rate, are highly appreciated (Koolhaas et al. 1999; Carere and van Oers 2004; Fucikova et al. 2009; Zhao et al. 2016).

Breath rate, represented by the count of breast movements measured per time unit, is a well-established and positively correlated measure of stress reaction, and is utilised as a measure of the handling stress (HS) test (Fucikova et al. 2009). However, this test has been used with several modifications, and experiments have led to varied findings. In adult Great Tits (Parus major), breath rate generally decreases after capture, with the highest rate immediately after capture (Fucikova et al. 2009). Similar results were also observed in hand-reared juveniles of the same species (Carere and van Oers 2004; van Oers and Carere 2007). In nestlings of Great Tit, however, the results were reversed, i.e. breath rate increased during handling and rose after a few minutes of experimental isolation from siblings (Fucikova et al. 2009). Breath rate has been proved to be heritable (Brommer and Kluen 2012) and thus consistent within individuals (Carere and van Oers 2004; Fucikova et al. 2009; Kluen et al. 2014). It was found to be associated with behavioural traits such as boldness (lower breath rate in bolder individuals) or exploratory behaviour (lower breath rate in slow explorers) which suggests that it may reflect a component of the personality of an individual (Carere and van Oers 2004; van Oers and Carere 2007; Fucikova et al. 2009; Brommer and Kluen 2012; but see David et al. 2011; Kluen et al. 2014; Zhao et al. 2016).

Together with an increasing number of studies utilising the HS test in laboratory conditions, there is also an increasing demand to study its use in wild populations under natural conditions (Kluen et al. 2014; Angelier et al. 2016). However, many factors easily controlled in the laboratory may act upon the behavioural and hormonal response of individuals captured and handled in the wild, making the findings in the field unreliable or difficult to interpret. In particular, the effects of different body mass (David et al. 2011), stage of ontogeny and experience (Groothuis and Carere 2005), ambient temperature (de Bruijn and Romero 2011; Lynn and Kern 2014), and time to catching (Dallman et al. 1992) may be strong and eventually interact, which could unpredictably influence physiological and behavioural measurements. As a result, weakly pronounced traits may be completely masked due to these side effects. Despite these limitations, there is an undeniable value of studies analysing effects of various factors influencing behavioural traits, including breath rate, as field measures of HS, carried out under field conditions. The results obtained in the field may more authentically demonstrate the effects of real processes in nature (Fisher et al. 2015).

To our knowledge, with the exception of modifications when heart rate was measured instead of breath rate (Korte et al. 1998; Cabanac and Aizawa 2000; Cabanac and Guillemette 2001), the HS test has only been used on altricial species such as tits or Zebra Finch (Taeniopygia guttata), and more often in laboratory conditions. When the heart rate instead of breath rate was measured in adults, the results in precocials were same as in altricial species: the rate was highest immediately after Chicken (Gallus domesticus) (Korte et al. 1998; Cabanac and Aizawa 2000) or Common Eider (Somateria mollissima) (Cabanac and Guillemette 2001) were caught or even touched, and then decreased. Opposite trends of breath rate during handling in nestlings versus adults in altricial birds prompt the first question of what breath rate pattern (as a part of the complex stress response) appears in precocial chicks in the wild. On the one hand, because of their higher developmental stage during their early ontogeny (maturation) compared to altricials (Starck and Ricklefs 1998), their behavioural responses could resemble those of adults. On the other hand, reactions to danger in wader chicks change during their ontogeny (Sordahl 1982) and their stress reaction may change as well. Breath rate may then be the measure in which such a change might be reflected.

The aim of this study was to assess breath rates as an indicator of a potentially easily measurable component of stress response in precocial chicks of a common Eurasian wader, the Northern Lapwing (Vanellus vanellus), in field conditions. Lapwing chicks are typical representatives of precocial species—they are mobile and open-eyed on hatching and are dependent on their parents only in terms of brooding and guidance (Cramp and Simmons 1983; Starck and Ricklefs 1998). In the case of danger, parents warn their chicks by alarm calls and, while the adult birds attract the attention of a potential predator by calling and conspicuous behaviour, the chicks crouch on the ground and rely on their inconspicuousness (Walters 1990). We were interested in the role of individual characteristics of Northern Lapwing chicks in breath rates before and after handling, followed by visual isolation in the field, as well as of ambient temperature, which represents a crucial environmental factor. We hypothesised that:

  1. 1.

    In contrast to altricial young, Northern Lapwing chicks respond to the HS test similarly to adult individuals—breath rate is highest immediately after grasping them by hand and it gradually decreases and remains lower after several tens of minutes of restraint (soothing).

  2. 2.

    Especially for thermally non-independent Northern Lapwing chicks with considerable thermoregulatory needs (Visser and Ricklefs 1993), the breath rate should be affected by the ambient temperature (Brent et al. 1983), i.e. breath rate per minute should increase with rising ambient temperature, in order for the bird to cope with overheating (Brent et al. 1984).

  3. 3.

    Breath rate is correlated to chick behaviour during capture; based on studies on altricial birds (e.g. Carere and van Oers 2004), individuals with lower breath rates are expected to be bolder and more active, i.e. they do not hide (in contrast with ‘hiders’) but try to escape (‘movers’).

  4. 4.

    Breath rate is individually consistent and thus repeatable during chick ontogeny to fledging.



Data collection

The research was carried out during April and May 2015 in Southern Bohemia (49°02′N, 14°22′E), Czech Republic, in an area of about 150 km2. The dominant habitat is composed of agricultural land, mainly a mosaic of cultivated fields (winter wheat, ploughed fields, spring cereals, oilseed rape, maize) interspersed with meadows, pastures, linear habitats along ditches and roads, and fishponds. Lapwing breeding sites were visited from the second half of March up to and including the end of May. The nests were located visually using binoculars and spotting scopes and by direct inspection of densely populated fields by skirmish line with typically five to eight (maximum 12) observers (Kubelka et al. 2012). The positions of the nests were stored in a global positioning system tracker and incubation stage was assessed using a floating method (van Paassen et al. 1984).

Although newborn Northern Lapwing chicks are nidifugous, they must be warmed by their parents for several weeks outside the nests, and parents also warn chicks by calls in the case of danger (Cramp and Simmons 1983). The chicks were sought—preferably on the day of hatching—on or near the nest. In total, 99 chicks from 36 families were captured, and 34 of these were newborns caught on the day of their hatching. Fourteen of 99 chicks were then captured repeatedly until fledging [nine chicks were caught twice, three chicks three times, and two chicks four times; intervals between repeated captures of individuals varied between 4 and 19 days, with a median of 7 days and a mean of 7.8 ± (SE) 0.93 days]. In addition to HS test data, the exact time to grasping them (the elapsed time between entering the nest area and picking up the chick that clung to the ground or tried to escape after the parents had voiced a call of alarm) was recorded [range 2−30 min, mean 10.69 ± (SE) 0.63 min] together with the behaviour (69 hiders; 22 movers; for eight, behaviour not available) before grasping. The air temperature was measured during testing of the individual and varied in a range of 8−22 °C, with a mean of 15.75 ± (SE) 0.54 °C. Chicks undergoing the HS test were examined for breath rate and other measurements in a standardised procedure, including weighing (grams), ringing, and measurement of bill, head and tarsus (millimetres). Because bill length reflects chick age (Beintema and Visser 1989), we determined the age of individuals with an unknown hatching date (n = 47) using this measure, verified by data for 18 chicks with exactly known hatching date and caught again later before fledging. However, because the exact age determination with 1-day accuracy based on bill length is highly unreliable due to large overlaps among 1-day categories, the chicks were divided into three broad age categories. The first age category [34 chicks; mean bill length 8.97 ± (SE) 0.474 mm] consisted of newborn chicks on their hatching day. The second age category [55 chicks; bill length 11.53 ± (SE) 1.132 mm] was made up of chicks in the first week of life but not including those in the first age category. The third age category [ten chicks; bill length 15.70 ± (SE) 1.281 mm] included seven chicks in the second week of life and three older unfledged chicks.

HS test

During the HS test, the chick was held firmly in one hand and its head was gently covered by the other hand. In such a position, the chicks were sufficiently still and it was possible to count the breath rate by observing thorax movements. Breath rate was counted for a 1-min period, which was divided into three bouts of 20 s each in order to track the possible patterns on a finer scale. For all individuals, we conducted the first and second measurement periods with three consecutive 20-s bouts each, separated by visual isolation consisting of the chick’s placement alone into a dark textile bag for at least 15 min [mean 24.34 ± (SE) 0.84 min]. Because the birds may perceive danger differently when they are free and when they are held in captivity (Cockrem and Silverin 2002), and inasmuch as we often located more than one chick at a time, just one (randomly selected) chick underwent the HS test while the remaining chicks were left on the ground untouched until the tested chick was placed into the dark textile bag. Thereafter, another randomly selected chick was picked up and tested in the same way. Once a chick had been tested, its weight and morphometric measures were taken. This procedure was performed after the first period, not at the end of the whole experiment, in order to minimize the time spent at the locality and to disturb the chicks for as short a time as possible. Therefore, the measurements were maximally standardised and taken by the same people in the same order for all individuals. When all chicks had undergone the first breath rate measurement and all other measurements, and when at least 15 min had elapsed since the first breath rate measurement had been completed, the second breath rate measurement was taken immediately after chick removal from the bag, again for a 1-min period consisting of three 20-s bouts. When all the chicks had undergone the second breath rate measurement, they were released at the same place where they had been captured. No chick was recaptured at an interval shorter than 4 days [mean 7.81 ± (SE) 0.93 days].


To analyse the factors responsible for variation in breath rates, we fitted a mixed-effect model using the R package lme4 (R Core Team 2014) with a likelihood ratio testing procedure (Bates et al. 2015). We modelled the effects of period, bouts nested within period (fixed effect), ambient temperature, time to grasping of a chick, its age, initial behaviour (hider vs. mover), weight and body constitution (through tarsus length). As weight and tarsus length were strongly intercorrelated (Pearson correlation coefficient, r = 0.85, p < 0.001), we only included weight in the model. In order to avoid over-parameterization of the model, we only included two reasonable interaction periods × time to grasping and period × visual isolation. First, time to grasping should have a stronger effect on breath rate in the first period before visual isolation than on the second period after visual isolation. Second, the length of visual isolation cannot influence the preceding measurement of the first breath rate and we thus expected no effect in the first period. Chick identity was a random factor. Only one (the first) record for each chick was included in this model. We verified that the significant factors also remained significant in the reduced model, so that their significance in the full model was not the result of over-parameterization (Crawley 2013). Consistency (repeatability) of breath rates within individuals was calculated using R package rptR and a mixed-effect modelling approach (Nakagawa and Schielzeth 2010; Dingemanse and Dochtermann 2013) with individual as a random effect. Where appropriate, we used the permutation test to assess the significance of repeatability (n  =  1000). All intervals are expressed as means ± SE. Normality of model residuals was tested using the Shapiro–Wilk test, and log transformation was used where this was helpful in normalizing the data. The level of significance was set at p = 0.05.


Breath rate patterns

Immediately after the first grasping of a chick from the field, its breath rate was the highest from all measured times (Fig. 1) and it decreased from this first 20-s bout (38.6 ± 1.52) through the second (38.0 ± 1.35) till the third bout (36.4 ± 1.31). After visual isolation (lasting 24 ± 0.8 min; Table 1), breath rate again decreased from the first (25.9 ± 0.69) through the second (25.7 ± 0.71) till the third 20-s bout (25.2 ± 0.71). As shown, the breath rate significantly dropped both within as well as between the first and second periods (Table 2) but with a steeper slope in the first period. Breath rates were individually highly repeatable within the three consecutive 20-s bouts before visual isolation [R ± SE (95% confidence interval; CI) = 0.91 ± 0.016 (0.87, 0.93)] as well as after it [R ± SE (95% CI) = 0.91 ± 0.014 (0.88, 0.94)]. Therefore, we summed the three consecutive 20-s counts of breath rates before as well as after the visual isolation of each individual, resulting in 1-min breath rates for the first and second periods (BR1 and BR2, respectively). Thus, individual 1-min breath rates dropped strongly from BR1 (113.1 ± 3.85) to BR2 (76.7 ± 2.05). Repeatability in individuals was lower between the BR1 and BR2 than within the periods [R ± SE (95% CI) = 0.13 ± 0.097 (0, 0.34), p = 0.01] suggesting that, beyond individual repeatability, other factors also influenced the relationship between BR1 and BR2.
Fig. 1

Breath rate (mean ± SE) of Northern Lapwing chicks during the first (20-s bouts ac) and second 1-min period (20-s bouts df) of 1-min periods separated by visual isolation lasting 24 ± (SD) 0.8 min. Regression slope was higher for the first period (β = − 1.2, p < 0.001) than the second period (β = − 0.425, p = 0.011)

Table 1

Range and variation of numerical predictors included in the model





Mean ± SE

Time to grasping (min)




10.7 ± 0.63

Length of visual isolation (min)




24.3 ± 0.84

Ambient temperature (°C)




15.3 ± 0.39

Age category




1.8 ± 0.06

Tarsus length (mm)




30.5 ± 0.21

Weight (g)




20.3 ± 0.85

Table 2

Results of the mixed-effect model evaluating effects of breath rate predictors in Northern Lapwing chicks


Estimate ± SE


χ 2



− 0.459 ± 0.0678



< 0.001

Period × bouts

− 0.015 ± 0.0058




Age category

0.121 ± 0.0506




Ambient temperature

0.036 ± 0.0076



< 0.001


0.001 ± 0.0032




Visual isolation

− 0.001 ± 0.0685





0.003 ± 0.0035




Behaviour (hiding/moving)

− 0.042 ± 0.0582




Time to grasping

− 0.031 ± 0.0054



< 0.001

Period × time to grasping

0.015 ± 0.0023



< 0.001

Period × visual isolation

− 0.002 ± 0.0029




Each of the two 1-min periods interrupted by time of visual isolation included three 20-s bouts. Family identifier was a random factor. Intercept value is 3.465 ± 0.4211

Factors influencing breath rates

We found that breath rate was significantly influenced by chick age and ambient temperature (Table 2). Breath rates increased with both increasing age of chicks (Fig. 2) as well as ambient temperature (Fig. 3). On the other hand, we did not find significant effects of catching date, length of visual isolation, chick’s weight and behaviour before grasping. However, time to grasping influenced breath rates with a significant interaction with period. Detailed inspection revealed that the breath rates were highest in chicks caught soon after entering the site and measured in the first period, which then dropped, resulting in a much steeper slope compared with measurement in the second period lacking this declining pattern (Fig. 4).
Fig. 2

Breath rates (mean ± SE) of Northern Lapwing chicks in three age categories before (white dots) and after (black dots) visual isolation. Sample size includes 34 hatched (newborn) chicks, 55 chicks 2–7 days old and ten chicks > 7 days old

Fig. 3

Relationship between ambient temperature and 1-min breath rate (mean ± SE) in Northern Lapwing chicks before (left) and after (right) visual isolation. Dashed lines define the 95% confidence intervals

Fig. 4

Relationship between time to grasping and 1-min breath rate (mean ± SE) before visual isolation (white dots; linear relationship dotted line) and after visual isolation (black dots; linear relationship dashed line). Regression slope was higher for the first (β = − 1.5, p = 0.038) than the second period (β = − 0.1, p = 0.381)

Individual consistency during development

We tested the consistency of breath rate within individuals (n = 14) caught repeatedly until fledging. We found significant repeatability for BF1 [R ± SE (95% CI) = 0.46 ± 0.187 (0, 0.74), p = 0.001] as well as for BF2 [R ± SE (95% CI) = 0.37 ± 0.186 (0, 0.69), p = 0.004]. Because most chicks were caught just twice (n = 9), we also tested the breathing consistency for this reduced set of chicks. We also found similar and significant repeatabilities [R ± SE (95% CI) = 0.40 ± 0.248 (0, 0.81), p = 0.003 and R ± SE (95% CI) = 0.39 ± 0.249 (0, 0.81), p = 0.005] for BF1 and BF2.


Breath rate expressed as the number of breast movements per time unit, which has been well established as an easily obtained measurement of stress reaction in altricial birds (Carere and van Oers 2004; Fucikova et al. 2009), was measured for the first time in chicks of a precocial shorebird. The highly repeatable frequency of breaths during the three 20-sec handling bouts within 1-min individual trials indicate high short-term consistency of this measure. Three consecutive measurements merged into a 1-min summary value could be, therefore, used as an indicator of breath frequency rate for subsequent analysis.

In our study, breath rate was highest immediately after grasping of chicks, while it dropped in each subsequent bout and, particularly, after visual isolation. The latter drop in breath rate may mirror release from stress as a result of further action accompanied by a painless procedure, which is unprecedented in real situations. A similar pattern of heart rate decrease was recorded in adult precocial domestic Chicken. After Chickens were handled or simply touched, their heart rate rose immediately but then dropped again (Korte et al. 1998; Cabanac and Aizawa 2000; Cabanac and Guillemette 2001). In adult Herring Gull (Larus argentatus), tachycardia (i.e., an abnormally rapid heart rate) occurred when a human merely approached a bird, and was double the rate before the experiment (Ball and Amlaner 1980). The same tests produced similar results when conducted by Carere and van Oers (2004) on adult hand-reared Great Tits. All these studies show findings consistent with ours, suggesting that the pattern of rapid decrease of breath rate after the first impression of stress in Northern Lapwing chicks is similar to that in adults of both precocial and altricial birds.

In young, however, the suggested trend is much less clear, as documented by Fucikova et al. (2009) who studied the change in breath rate of Great Tit offspring born in the wild. In 14-day-old young, the authors found increasing breath rates after a few minutes of social isolation of individually treated young in opaque bags, i.e. the opposite trend of that recorded in our study on Northern Lapwing chicks. What is more interesting, when Fucikova et al. (2009) tested the same individual Great Tits at 6 months of age, the trend was reversed, and likewise in adults, i.e. there was a decreasing breath rate in birds which had previously experienced social isolation. Such a change in breath frequency reflecting the response to stress in individuals of different ages may be explained by a different perception of danger (Fucikova et al. 2009) due to previous experience or/and age (Impekoven 1976; Rydéan 1982; Love et al. 2003; Korneeva et al. 2006; Dingemanse and Wolf 2013). Fucikova et al. (2009) suggest that social isolation was the main stressor for Great Tit young in their treatments. For a songbird brood remaining in the nest and tightly associated with siblings for approximately 2 weeks, social isolation may represent a crucial stressor. In lapwing chicks, however, grasping by hand associated with the parents warning call might be perceived as a direct threat causing the highest stress response. On the other hand, subsequent visual isolation did not constitute a stress situation for chicks which are used to operating independently in the field. Similarly, later ongoing manipulation is unprecedented in any real situation. Therefore, the pattern of breath rate before and after the period of isolation (a dark space in a bag) was in agreement with patterns in adults, but opposite to the response of early altricial young.

A strong correlation between individual breath rate before and after visual isolation was observed. However, it is important to emphasize that other factors also modulate breath rates. We tested potential effects of time to chick grasping, length of visual isolation, ambient temperature, age category, behaviour, weight and body size (tarsus length) on breath rate before and after visual isolation. In spite of a wide variation in all variables, except the experimentally manipulated length of visual isolation, only age category and ambient temperature were significant predictors affecting breath rate before, as well as after, visual isolation. Time to grasping was an important predictor of breath rate before visual isolation, i.e. the earlier the chick was grasped after entering the site, the higher the initial breath rate detected. Therefore, especially in field studies where it is quite hard to follow standardised sampling, the differences in minutes between location and grasping of hidden individuals may affect breath rate significantly, which emphasizes the need to always consider these temporal events in analyses. On the other hand, length of visual isolation in a bag had no further determining effect on breath rate. Different length of visual isolation also had no effect on breath rate in Great Tit nestlings (Fucikova et al. 2009).

Breath rate before and after visual isolation increased with Lapwing chick age, which ranged from the newborns (first hours after hatching) to chicks in their fourth week of life. This pattern is similar to that found during early ontogeny in resting Rosy-faced Lovebird (Agapornis reseicollis) (Bucher and Bartholomew 1986) and also in the context of HS in Great Tits (Fucikova et al. 2009). Great Tit young evaluated at 6 months of age had a higher initial breath rate than the same individuals when they were 14 days old (Fucikova et al.2009). Contradictory results were found by Pearson et al. (1998) in King Quail (Coturnix chinensis). They showed heart rate decreasing with age, when after the first week, post-hatching King Quails were maintained at the highest levels of heart rate (550–650 beats min−1). Afterwards, heart rate started to decrease with increasing age and body mass. The maximal heart rate of quail chicks represents a greater post-hatching increase in heart rate than is found in larger precocial chicks; this difference is probably attributable to the higher demands of thermoregulation due to the small body mass of the quail. Therefore, further studies shedding light on the trend of breath frequency from newborns up to adult individuals in various taxa, ideally in the wild, are welcome. Taking into consideration the nature of newborns, one would expect the development of breath rate to be more complex in young altricials compared with precocials, and that the difference between breath rates of chicks and adults more pronounced in altricial species. In conclusion, the results so far indicate that a change in breath rate is age dependent and might also be species specific, which must be taken into account when interpreting the results.

Increasing ambient temperature resulted in a significant increase in breath rate in lapwing chicks. Temperature thus has an important effect on breath rate, especially in nestlings with imperfect thermoregulation (Starck and Ricklefs 1998). In such cases, even a small increase in temperature may cause a significant rise in breath rate, in particular when a chick may overheat in a closed cloth bag. Higher explanatory power of the temperature variable after visual isolation than before it might support this suggestion. On the other hand, lowered temperature has also been confirmed in prior studies to act like a stressor (leading to increased heart rate and corticosterone levels) in birds (de Bruijn and Romero 2011, Lynn and Kern 2014). The effect of low temperature may manifest in combination with the stressful situation—the handling after visual isolation—so that the effects of poor weather and handling can cumulate. Such a scenario was not observed in the study of Angelier et al. (2016), however, inasmuch as they found no change between stress reaction to handling among Feral Pigeons (Columba livia f. domestica), either in control or experimentally lowered temperatures. In that laboratory study, levels of all three studied stress hormones—corticosterone, prolactin, and thyroxine—changed regardless of temperature (Angelier et al. 2016). In our study, the ambient temperature (commonly varying by tens of degrees Celsius) probably played a much more important role. The biggest difference compared to our study—and one which could have affected the influence of temperature—was the unpredictability and rather varying temperature at the time and/or season of our study. A bird’s metabolism may react quickly to the current temperature. Additional important questions are whether there is also a significant pattern in adult birds with fully developed thermoregulation, and at what age does this eventually stabilize in chicks. A study addressing these issues would help us to comprehensively understand the importance of ambient temperature and its influence on breath rate among birds. Therefore, the actual temperature must also be taken into account when interpreting the results obtained at different temperatures, e.g. in the field.

Individual breath rate was found to be consistent in lapwing chicks and thus, although we cannot link it to personality in this study because of the lack of measured variables, a possible connection may exist. Such information from precocial bird species could contribute to untangling an uncertain link between breath rate and personality or behavioural traits, which is still not clear. On the one hand, boldness or exploring behaviour were found in Great Tits and Blue Tits (Cyanistes caeruleus) to be correlated with breath rate (Carere and van Oers 2004; van Oers and Carere 2007; Fucikova et al. 2009; Brommer and Kluen 2012), but on the other hand, breath rate does not correlate with activity in Chestnut Thrush (Turdus rubrocanus) (Zhao et al. 2016). Also, in the study of David et al. (2011) on Zebra Finches, breath rate did not correlate with activity, reaction to startling, exploration or neophobia. However, in the work of Carere and van Oers (2004), the breath rate was clearly correlated with personality, with shy Great Tits having higher breath rate scores than bold ones. These results show that, in selected species, breath rate could be used as a non-invasive tool for measuring personality in wild birds in the field, but simultaneously, breath rate should be assessed with caution and with respect to particular species and method.

Breath rates were found to be consistent within repeatedly captured chicks at intervals of 4–19 days (median 7 days) regardless of ambient temperature, time to catching, length of social isolation, age, and interval from last capture. The consistency of breath rate in wild Northern Lapwing chicks thus makes individual breath rate measured during the HS test a useful measure, which may be studied in the context of individual fitness and, perhaps, personality, although direct measurements still need to be performed.

In conclusion, by measuring the breath rates of captured wild Northern Lapwing chicks during the HS test, we showed that breath rate: (1) resembles that of adult birds more than that of altricial young, as it is highest immediately after capture and then decreases; (2) is positively affected by ambient temperature and by the age of the chick; (3) is individually repeatable; and (4) is not correlated with behaviour before grasping. For a better understanding of the patterns of breath rate in precocial chicks, changes in the level of stress hormones, as well as links to the characteristics affecting individual fitness, should be studied.



Permission to capture, handle, and ring wild Northern Lapwing chicks was granted by the Bird Ringing Centre under National Museum, Prague (Krouzkovaci Stanice Narodniho Muzea, Praha), licence number 1165. This study was funded by the Internal Grant Agency of the Faculty of Environmental Sciences of the Czech University of Life Sciences (project no. 20154238). The authors thank Mark Sixsmith for his linguistic advice.


  1. Angelier F, Parenteau C, Ruault S, Angelier N (2016) Endocrine consequences of an acute stress under different thermal conditions: a study of corticosterone, prolactin, and thyroid hormones in the pigeon (Columba livia). Comp Biochem Phys A 196:38–45CrossRefGoogle Scholar
  2. Ball NJ, Amlaner CJ (1980) Changing heart rates of Herring Gulls when approached by humans. In: Amlaner CJ, MacDonald DW (eds) A handbook on biotelemetry and radio tracking. Pergamon, OxfordGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. CrossRefGoogle Scholar
  4. Beintema AJ, Visser GH (1989) Growth parameters in chicks of charadriiform birds. Ardea 77:169–180Google Scholar
  5. Brent R, Rasmussen JG, Bech C, Martini S (1983) Temperature dependence of ventilation and O2-extraction in the Kittiwake, Rissa tridactyla. Experientia 39(10):1092–1093CrossRefGoogle Scholar
  6. Brent R, Pedersen PF, Bech C, Johansen K (1984) Lung ventilation and temperature regulation in the European Coot Fulica atra. Physiol Zool 57(1):19–25CrossRefGoogle Scholar
  7. Brommer JE, Kluen E (2012) Exploring the genetics of nestling personality traits in a wild passerine bird: testing the phenotypic gambit. Ecol Evol 2(12):3032–3044CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bucher TL, Bartholomew GA (1986) The early ontogeny of ventilation and hemeothermy in an altricial bird, Agapornis reseicollis (Psittaciformes). Resp Physiol 65(2):197–212CrossRefGoogle Scholar
  9. Cabanac M, Aizawa S (2000) Fever and tachycardia in a bird (Gallus domesticus) after simple handling. Physiol Behav 69(4):541–545CrossRefPubMedGoogle Scholar
  10. Cabanac AJ, Guillemette M (2001) Temperature and heart rate as stress indicators of handled Common Eider. Physiol Behav 74(4):475–479CrossRefPubMedGoogle Scholar
  11. Carere C, van Oers K (2004) Shy and bold Great Tits (Parus major): body temperature and breath rate in response to handling stress. Physiol Behav 82(5):905–912CrossRefPubMedGoogle Scholar
  12. Cockrem JF, Silverin B (2002) Sight of a predator can stimulate a corticosterone response in the Great Tit (Parus major). Gen Comp Endocr 125:248–255CrossRefPubMedGoogle Scholar
  13. Cramp S, Simmons KEL (1983) Handbook of the birds of Europe, the Middle East, and North Africa: the birds of the Western Palearctic, vol III: waders to gulls. Oxford University Press, OxfordGoogle Scholar
  14. Crawley MJ (2013) The R book, 2nd edn. Wiley, ChichesterGoogle Scholar
  15. Dallman MF, Akana SF, Scribner KA, Bradbury MJ, Walker CD, Strack AM, Cascio CS (1992) Stress, feedback and facilitation in the hypothalamo-pituitary-adrenal axis. J Neuroendocrinol 4:517–526CrossRefPubMedGoogle Scholar
  16. David M, Auclair Y, Dechaume-Moncharmont FX, Cézilly F (2011) Handling stress does not reflect personality in female Zebra Finches (Taeniopygia guttata). J Comp Psychol 126:10–14CrossRefPubMedGoogle Scholar
  17. de Bruijn R, Romero LM (2011) Behavioral and physiological responses of wild-caught European Starlings (Sturnus vulgaris) to a minor, rapid change in ambient temperature. Comp Biochem Phys A 160:260–266CrossRefGoogle Scholar
  18. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82(1):39–54CrossRefPubMedGoogle Scholar
  19. Dingemanse NJ, Wolf M (2013) Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim Behav 85:1031–1039CrossRefGoogle Scholar
  20. Fair JM, Jones J (eds) (2010) Guidelines to the use of wild birds in research. Ornithological Council, Washington, DCGoogle Scholar
  21. Fisher DN, James A, Rodriguez-Munoz R, Tregenza T (2015) Behaviour in captivity predicts some aspects of natural behaviour, but not others, in a wild cricket population. Proc R Soc B. PubMedPubMedCentralGoogle Scholar
  22. Fucikova E, Drent PJ, Smits N, van Oers K (2009) Handling stress as a measurement of personality in Great Tit nestlings (Parus major). Ethology 115:366–374CrossRefGoogle Scholar
  23. Groothuis TGG, Carere C (2005) Avian personalities: characterization and epigenesis. Neurosci Biobehav R 29:137–150CrossRefGoogle Scholar
  24. Impekoven M (1976) Prenatal parent-young interactions in birds and their long-term effects. Adv Stud Behav 7:201–253CrossRefGoogle Scholar
  25. Kluen E, Siitari H, Brommer JE (2014) Testing for between individual correlations of personality and physiological traits in a wild bird. Behav Ecol Sociobiol 68:205–213CrossRefGoogle Scholar
  26. Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MA, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav R 23(7):925–935CrossRefGoogle Scholar
  27. Korneeva EV, Aleksandrov LI, Golubeva TB, Raevskii VV (2006) Development of the auditory sensitivity and formation of the acoustically guided defensive behavior in nestlings of the Pied Flycatcher Ficedula hypoleuca. J Evol Biochem Phys 42:691–698CrossRefGoogle Scholar
  28. Korte SM, Ruesink W, Blokhuis HJ (1998) Heart rate variability during manual restraint in chicks from high- and low-feather pecking lines of laying hens. Physiol Behav 65(4):649–652CrossRefGoogle Scholar
  29. Kubelka V, Zámečník V, Šálek M (2012) Přímá ochrana hnízd čejky chocholaté (Vanellus vanellus)—metodika pro rok 2012. Vanellus—Zpravodaj Skupiny Pro Výzkum Ochranu Bahňáků ČR 7:66–75Google Scholar
  30. Love OP, Bird DM, Shutt LJ (2003) Corticosterone levels during post-natal development in captive American Kestrels (Falco sparverius). Gen Comp Endocrinol 130:135–141CrossRefPubMedGoogle Scholar
  31. Lynn SE, Kern MD (2014) Environmentally relevant bouts of cooling stimulate corticosterone secretion in free-living Eastern Bluebird (Sialia sialis) nestlings: potential links between maternal behavior and corticosterone exposure in offspring. Gen Comp Endoc 196:1–7CrossRefGoogle Scholar
  32. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  33. Pearson JT, Tsudzuki M, Nakane YO, Akiyama RY, Tazawa HI (1998) Development of heart rate in the precocial King Quail Coturnix chinensis. J Exp Biol 201(7):931–941PubMedGoogle Scholar
  34. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  35. Reeder DM, Kramer KM (2005) Stress in free-ranging mammals: integrating physiology, ecology, and natural history. J Mammal 86(2):225–235CrossRefGoogle Scholar
  36. Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19(5):249–255CrossRefPubMedGoogle Scholar
  37. Rydéan OO (1982) Selective resistance to approach: a precursor to fear responses to an alarm call in Great Tit nestlings Parus major. Dev Psychobiol 15:113–120CrossRefGoogle Scholar
  38. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, supppressive, stimulatory, and preparative actions. 1. Endocrine Rev 21:55–89Google Scholar
  39. Sordahl TA (1982) Antipredator behavior of American Avocet and Black-necked Stilt chicks. J Field Ornithol 53(4):315–325Google Scholar
  40. Starck JM, Ricklefs RE (1998) Patterns of development: the altricial-precocial spectrum. In: Starck JM, Ricklefs RE (eds) Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, OxfordGoogle Scholar
  41. van Oers K, Carere C (2007) Long-term effects of repeated handling and bleeding in wild caught Great Tits Parus major. J Ornithol 148:185–190CrossRefGoogle Scholar
  42. van Paassen AG, Veldman DH, Beintema AJ (1984) A simple device for determination of incubation stages in eggs. Wildfowl 35:173–178Google Scholar
  43. Visser GH, Ricklefs RE (1993) Development of temperature regulation in shorebirds. Physiol Zool 66(5):771–792CrossRefGoogle Scholar
  44. Walters JR (1990) Anti-predatory behavior of lapwings: field evidence of discriminative abilities. Wilson Bull 102:49–70Google Scholar
  45. Zhao QS, Hu YB, Liu PF, Chen LJ, Sun YH (2016) Nest site choice: a potential pathway linking personality and reproductive success. Anim Behav 118:97–103CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2017

Authors and Affiliations

  1. 1.Faculty of Environmental SciencesCzech University of Life Sciences PraguePrague 6-SuchdolCzech Republic

Personalised recommendations