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Effects of meteorological conditions on brood care in cooperatively breeding carrion crow and consequences on reproductive success


Meteorological stressors (e.g., temperature and rain shortage) constrain brood provisioning in some bird species, but the consequences on reproductive success have been rarely quantified. Here we show, in a cooperatively breeding population of carrion crow Corvus corone in Spain, that individual feeding rates decreased significantly with rising air temperatures both in breeders and helpers, while lack of rain was associated with a significant reduction in the effort of the male helpers as compared to the other social categories. Group coordination, measured as the degree of alternation of nest visits by carers, was also negatively affected by rising temperature. Furthermore, we found that the body condition of the nestlings worsened when temperatures were high during the rearing period. Interestingly, the analysis of a long-term data set on crow reproduction showed that nestling body condition steadily deteriorated over the last 26-years. Although many factors may concur in causing population changes, our data suggest a possible causal link between global warming, brood caring behaviour and the decline of carrion crow population in the Mediterranean climatic region of Spain.


Understanding how organisms respond to climate change [58, 59] is a central topic in animal ecology[15, 66, 95]. Phenological adjustments, like advanced laying dates, are common in birds [40, 65] with effects that ranged between negative [52, 56], when a mismatch arises between the peak of food availability and the energetic requirements of the developing young [93], neutral [41] or even positive [18, 53], because of increased chances to renest [51, 55]. Birds can also modulate their behaviour to cope with high temperatures, by resting in sheltered places [39, 42], or by increasing panting, wing spreading or gular fluttering to regulate the body temperature [86, 88]. Heat avoidance might trade off with other behaviours that are important for survival or reproduction [33], with possible consequences on individual fitness [34, 80, 91]. Understanding the effects of global warming on key-life behaviours, such as young provisioning, is therefore paramount, but information is still limited [69], especially in cooperatively breeding bird species, where subordinated individuals help raising young that are not their own [17, 30, 38]. In these species, reproductive success depend on the collective effort of several individuals that typically pursue different benefits (direct vs indirect, [29, 44, 72]), face different trade-offs between current and future reproduction [28, 46, 47, 87] and therefore vary largely in their investment in brood provisioning [3, 67]. The effect of external stressors, like increasing temperatures and rain shortage, may therefore affect group members in different ways, with complex consequences on the dynamic of cooperation that urgently need to be addressed.

One reason behind our incomplete understanding of brood care in birds is that most research, particularly on cooperative species, has focused so far on quantifying the individual contribution of carers, overlooking other important dimensions of this behaviour [82]. Recent studies have uncovered that reproductive success can depend on the coordination of nest visits among different group members. In long tailed tits Aegithalos caudatus, for example, joint visits at the nest (usually referred to as “synchrony” in the literature, e.g. [61] reduce the risk of brood predation [11], whereas, in carrion crows Corvus corone, alternation of carers in provisioning the brood (also referred to as “turn taking”, e.g. [81] improves the body condition of the young and their post-fledging survival [90]. Therefore, to fully understand how meteorological stressors affect the provisioning behaviour of birds and what are the consequences on reproduction, a comprehensive approach shall be adopted.

Some short-term studies have shown that weather conditions affect nest visitation rate in cooperative bird societies like the long-tailed tit, where all carers provision the brood significantly less in warmer days [63]. Hot temperatures may affect group members in different ways, like in the pied babbler Turdoides bicolor, where dominants but not helpers reduce their provisioning rate in hot days, with negative consequences on nestling growth [94]. Similarly, in chestnut-crowned babblers Pomatostomus ruficeps, the lack of rainfall, high wind speed and high temperature affect breeders and helpers differently and group coordination (measured as proportion of synchronous visits) declines in hot days [69].

However, a key question that remains unanswered is whether these short-term effects of weather conditions on provisioning behaviour translate into measurable consequences over the long term, given the current context of global warming. Here, we address this question in the cooperatively breeding carrion crow, by analysing an extensive data set, which covers the last twenty-six years.

In Spain, carrion crows form complex kin groups where up to seven subordinated individuals can join a dominant breeding couple [8]. Subordinates are non-breeding retained offspring or immigrants, mostly males, that are related to the same-sex breeder and that can sire chick in the brood [6]. Subordinate group members participate in brood care, boosting reproductive success [24], although their contribution can vary largely [22], with some birds refraining from providing care at all [5]. Recently, it has also been found that the degree of alternation of carer in provisioning the brood significantly improves the body condition of the nestlings, enhancing their post-fledging survival [90].

In this study, we first examine the effect of temperature and the number of days since the last rain on the provisioning rate of group members of different sex and social category (breeders/retained offspring/immigrants) and on the degree of alternation of carers in visiting the nest. Subsequently, we analyse how these two meteorological variables affect crow reproductive success, measured as the annual production of offspring and their body condition. We expect that, if high temperatures and lack of rain negatively affect both parental care and breeding success of crows, negative trends will emerge over the long term, due to global warming. To test this prediction, we analysed an extensive data set that encompasses the last 26 years of crow reproduction in a population living in the Northern Mediterranean region of Spain.


Study area and population

We studied a cooperatively breeding population of carrion crows in a 45Km2 area at La Sobarriba, Castilla y León, Northern Spain (42°37’, 5°26’W), characterized by a mosaic of crops, scrubs, oak forest patches, meadows, poplar and pine plantations and uncultivated land [7, 77]. Castilla y León region has a Mediterranean climate with long cold winters and short hot summers, being January the coldest month and July the warmest [4, 78]. In the last decades, monthly, seasonal and annual temperatures have increased in Spain [43, 75], especially during spring and summer [75], and rainfalls have decreased [76, 92]. Castilla y León, in particular, has changed toward a warmer and drier climate, notably in winter, spring and summer [36, 37].

In our study population, carrion crows form cohesive kin groups of up to nine individuals (average size ± SE = 3.2 ± 0.08; [5] that comprise a dominant breeding pair, its non-dispersing offspring, which can remain at natal territory for up to 4 years, and/or individuals, called “immigrants”, that fledged in other territories and settled in already established groups, where they are related to the resident breeder of the same sex [6]. Therefore, groups are extended families where subordinates can contribute to nestling care (nest building, feeding the incubating female and the chicks, and nest sanitation). Provisioning the brood is costly for crows, which lose mass in proportion to their effort [21, 23] and hence finely tune their contribution depending on extrinsic (food availability) and intrinsic (own condition) factors [5, 27]. Typically, breeders show the highest brood feeding rates, followed by male helpers and, lastly, the female helpers [22]. Helpers rise the total provisioning rate of the group, increasing nestling survival, and augment the probability of re-nesting after early nest failure [24]. A recent study also revealed that crow group members take turns in visiting the nest and that such coordination significantly increases the body condition of nestlings, boosting post-fledging survival rates [90].

Data collection

Since 1995 we have monitored crow reproduction in the study area, by surveying all nests throughout the breeding season (March-July). Upon early nest failure, crows may renest up to three times in a season, but they never raise multiple successful broods [24]. Every year, nestlings were banded with colour rings and wind tags just before they left the nest (28–30 days old). Adult crows were captured with two-compartments walk-in traps and “snap traps” specifically developed for this species (for details on catching methods, see [8]. A sample of blood (200 µl) was taken from all the banded individuals for genetic analyses. The sex of each individual was determined by P2/P8 molecular method [49], while parentage analyses based on DNA microsatellites provided the breeding status of group members [9, 26].

We collected data on provisioning rate and timing of nest visits by placing camouflaged micro video cameras from a distance of ca. 1,5 – 2 m from nests with chicks older than 10 days [22] during the breeding seasons 1999, 2000, 2003–2007, 2015, 2018, 2019 and 2021. Daily recording bouts (lasting between 4 and 15 h) were distributed between 05:00 am and 08:00 p.m. (UTC time). Video recordings were analysed in the laboratory with VLC media player using slow motion when necessary, extracting the following data for each nest visit: the identity of the carer, the entrance and departure time from the nest (according to the UTC time displayed on all recordings) and the number of feeds delivered to chicks (i.e., the number of times the carer put its beak in a nestling’s open gape to regurgitate food [22]. We analysed a total of 2520 hours of video recordings that comprised 12,467 nest visits. We sampled 76 nests (average ± SE recording time per nest = 32 hours ± 3.56) in 50 different territories collecting data on 221 caregivers (68 breeding males, 69 breeding females, 45 helping male offspring, 11 helping male immigrants and 28 helping female offspring).

To analyse carers’ turn-taking, measured as the proportion of nest visits where a carer is followed by any other carer of the group) we restricted the data set to groups where all individuals were recognisable. The sample eventually comprised 58 nests from 40 different territories and 196 caregivers (64 breeding males, 63 breeding females, 31 helping male offspring, 11 helping male immigrants, 23 helping female offspring and 4 individuals of unknown sex and social category) for a total of 2157 hours of video recording (34.24 hours ± 4.29 per nest) and 11,309 nest visits.

Both in the analysis of feeding rate and carers’ alternation, six breeding males, six breeding females and two helping male offspring were sampled twice in different years, and one breeding male, two breeding females, one helping male immigrant, one helping male offspring and one helping female offspring three times. We retained them in the sample because, in all cases, they were observed in groups of different composition. In any case, their exclusion did not qualitatively change the results presented.

Reproductive success was measured as the number of chicks that survived until fledging. We collected data of 989 reproductive attempts in 125 territories during 1995–2021. Nestlings were measured when the eldest of the brood (hatching is asynchronous in crows, causing differences between 1 and 4 days among siblings; [24] was about to leave the nest, at the age of 28 – 30 days. Nestling body condition was quantified by dividing body mass by tarsus length, which is suitable lineal measure of structural size [60]. This index correlates with post-fledging survival in crows [90] and allows simplifying the statistical models, because it accounts for differences in body size due to sex and age. The sample comprised 901 chicks in 375 broods during the breeding seasons 1995–2021.

The Spanish National Agency of Meteorology (AEMET) provided data on hourly temperatures (in Celsius degrees) and daily rainfalls (mm) for the whole sampled period, collected at the weather station “Virgen del Camino”, located 11 km away from our study area.

Statistical analyses

All data were analysed with Mixed Models with R 4.1.1. [73] with lme4 package [10]. Normality of DARMHa scaled residuals, heteroscedasticity and outliers were checked with the package DARMHa [54], while multicollinearity between fixed factors was tested by computing variance inflation factors (VIFs) with the package performance [62]. The model significance test (Omnibus test) was performed by comparing the model of interest with the null model (without predictors) by means of Akaike’s Information Criterion values (AICc) [19], preserving the same structure of the random part. All models were fitted with random intercept fixed slopes, which always provided the best fit.

First, to test the effect of weather on crow provisioning rate, we built the data set by establishing three daytime periods, each comprising 5 hours (from 0500 to 1000 hours UTC; from 1001 to 1500, and from 1501 to 2000). Individual feedings rates were calculated as the number of feeds per hour delivered by a carer within a given daytime period. We used a Linear Mixed Model (LMM) fitted by Restricted Maximum Likelihood (REML) to analyse these data. The Box-Cox transformation [14] of the response term (frequency of feeds) improved the normality of the model residuals. The model included group size, chicks age, laying Julian date of the first egg of the clutch (taking first of march as reference), brood size, individual category, daytime period, average hourly air temperature for the corresponding daytime period, and number of days since the last rain as explanatory terms, as well as individual ID nested into group ID as random term to control for repeated measures. To detect possible differences among social categories of carers in their response to meteorology, we run a second model fitting two interactions, i.e., social category * temperature and social category *days since last rain. If significant, post hoc multiple comparisons across different categories of group members were performed with Package Phia using “Test Interactions” with X2 test and p values adjusted by Holm’s method [35].

Second, to investigate the influence of meteorological variables on carers’ turn-taking we used a Generalized Linear Mixed Model (GLMM), with binomial error distribution and logit link function, where two vectors comprising the number of alternate visits and repeated visits represented the response variable. This variable weights the proportion of alternated visits according to the total number of visits [32], which varies between social groups. This model included group size, chicks age, laying Julian date, brood size, daytime period, average hourly air temperature for each daytime period and number of days since the last rain as explanatory terms, and group ID as random term.

Third, to analyse the effect of temperature and lack of rain on nestling production we used a hurdle model, where the response variable is analysed in two steps. Initially, the model addresses the probability of attaining zero values, i.e. nest failure, and, subsequently, the probability of non-zero values (number of nestlings in successful broods). Hurdle models handle zero inflated distributions and are particularly suitable for analysing reproductive success in birds, where brood loss is generally caused by predation, while the number of nestlings in successful nests strongly depend on the quantity and quality of the care that they received [1, 64, 74]. The two steps procedure therefore allows telling apart the factors that influence each mechanism (predation/care) separately. For the present study, the second component is particularly relevant, as it directly relates with provisioning behaviour [24], and it will be the focus of our attention. The hurdle model here consists in a Generalized Linear Mixed Model using Template Model Builder (GLMMTMB) [16] with truncated Poisson distribution and log link function [12]. The number of nestlings was fitted as response variable. Group size, clutch size, laying Julian date, average daily maximum air temperature during the nestling development period (from hatching to fledging) and number of days without rain in that period represented the fixed terms, and group ID the random term (to control for different reproductive attempts in the same territory for a given year).

Fourth, to test whether meteorological variables affected the body condition of the chicks, we run a LMM fitted by REML, where group size, clutch size, laying Julian date, average daily maximum air temperature during the chick rearing period and number of days without rain during that period were fitted as explanatory variables, and brood ID as random term (to group nestlings from the same brood). The body condition index was Box-Cox transformed to improve the normality of the model residuals [14].

Furthermore, to model the change in nestling production and condition over the long-term, we used respectively: a GLMMTMB [16] with year as fixed term and group ID as random term, and a LMM fitted by REML with a Box-Cox transformation of the response variable, year as fixed term and brood ID as random term.


Effect of weather on the provisioning rate

The provisioning rate of cares decreased significatively with rising temperatures (Table 1a, Fig. 1), regardless of the social category of carers (non-significant interaction category*temperature; Table 1b). Provisioning rate was also affected by the time elapsed since the last rain (Table 1a), but, in this case, the effect varied among categories of group members, as shown by the significant interaction category*days since last rain (Table 1b). In particular, the post-hoc analysis revealed significant differences between the breeding females, who slightly increased their contribution under dry conditions and the male helpers, both offspring and immigrant, who instead reduced their feeds (Additional file 1: Table S1, Fig. 2). As expected, based on previous results [22, 24], the provisioning rate differed among social categories, significantly decreased with group size and across daytime periods, and increased with brood size (Table 1a).

Table 1 Variables associated with individual provisioning rate.
Fig. 1
figure 1

Fitted Box-Cox transformed values of provisioning rate (feeds/h) plotted against the average hourly air temperature (°C) for each daytime period. The shadowed area indicates 95% confidence limits.

Fig. 2
figure 2

Fitted Box-Cox transformed values of provisioning rate (feeds/h) plotted against days since last rain for all categories of group members (Bm: breeder male, Bf: breeder female, Hf off: female offspring helper, Hm imm: male immigrant helper, Hm off: male offspring male). The shadowed areas indicate 95% confidence limits.

Effect of weather on the degree of visit alternation

The degree of alternation of nest visits was negatively affected by rising temperature (Table 2, Fig.3). In contrast, the number of days since the last rain did not show a significant effect. Alternation also increased with group size, confirming previous results [90].

Table 2 Variables associated with alternation of nest visits
Fig. 3
figure 3

Degree of alternation of nest visits in relation to average hourly air temperature (°C) for each daytime period. Fitted values were plotted and the shadowed area indicates 95% confidence limits.

Effects of weather on nestling production and nestling body condition

The probability of nest failure significantly decreased with the size of the clutch (estimate ± SE = − 0.136 ± 0.067, Z = − 2.007, p = 0.045; Additional file 11 Table S2a) and increased with the Julian laying date (estimate ± SE = 0.025 ± 0.009, Z = 2.709, p = 0.007) but did not depend on meteorological conditions. Similarly, the number of nestlings produced in successful nests was affected neither by temperature nor the number of days without rain, but increased with group size (estimate ± SE = 0.089 ± 0.027, Z = 3.239, p = 0.001; Additional file 1: Table S2b) and clutch size (estimate ± SE = 0.189 ± 0.04, Z = 4.718, p < 0.001), and decreased with the Julian laying date (estimate ± SE = − 0.014 ± 0.006, Z = − 2.543, p = 0.011), confirming previous results [24].

Average daily maximum air temperatures during the rearing period were negatively related to nestling body condition (Table 3, Fig. 4), while the number of days without rain showed no effect. No other variables proved significant in this analysis.

Table 3 Variables associated with nestling body condition
Fig. 4
figure 4

Effect of average daily maximum temperature during the chick rearing period on the nestling body condition. Fitted Box-Cox transformed values were plotted and the shadowed area indicates 95% confidence limits.

Nestling production and condition trends over the long term.

The number of nestlings in successful nests did not vary over the 26-year study period (estimate ± SE= 0.001 ± 0.004, z value= 0.152, p value= 0.879). Nestling boy condition, instead, significantly worsened throughout the same period (estimate ± SE= − 0.067 ± 0.027, df= 361.295, t value= − 2.496, p value=0.013; Fig. 5).

Fig. 5
figure 5

Variation of the body condition of chicks during the 26-years study period. Fitted Box-Cox transformed values were plotted and the shadowed area indicates 95% confidence limits.


Our results showed that high temperatures constrained crow provisioning behaviour and carers’ alternation suggesting a cascading effect on reproductive success. Lack of rain was also associated with a reduction in provisioning rate, particularly in helping males.

Effect of temperature on provisioning behaviour and carers’ alternation

Increasing temperature negatively affected individual feeding rate, regardless of social category, and significantly reduced the degree of alternation of group members in provisioning the brood. High temperatures can reduce individual feeding rate in at least two non-exclusive ways: (1) by constraining the activity and mobility of invertebrates [42], which are the main preys of crows during the breeding period [31], (2) by forcing birds to lower their activity [86], spending more time near water supplies or shaded areas [45, 96] and increasing heat dissipation behaviour (wing spreading and panting behaviour, [39]. Indeed, we have frequently observed these behaviours in crows at high temperatures. Moreover, on days of intense hot, crow breeding females spend more time in the nest, shading the offspring.

Our data also showed that the degree of alternation at the nest of group members declines at high temperatures. Although the proximate mechanisms that allow crows to alternate nest visits are not yet fully understood [90], it seems likely that the need of resting in shaded areas, for example in tree canopies, might reduce the ability of crows to monitor each other behaviour and therefore to adjust own timing of nest visitation. In addition, stressful conditions that constraint individual provisioning rates and pose additional costs for thermoregulating might affect group members differently, for example depending on their current body condition, eventually disrupting the coordination of the group. Interestingly, a similar effect has been shown also in chestnut-crowned babblers, which normally synchronize their arrival at the nest to prevent brood predation, but, at high temperature, loose their coordination, particularly in large units [68, 69].

Effect of lack of rain on provisioning behaviour and carers’ alternation

The effect of lack of rain on the provisioning rate was more complex than that of the temperature and significantly depended on the social category of the carer. Both offspring and immigrant male helpers showed the most substantial decreases, particularly compared with the breeding females, who instead slightly increased their effort under dry conditions.

Dry weather can cause a decrease in food availability [83] affecting foraging efficiency, but it may pose a less stringent physiological cost to crow activity, compared with high temperature. This may explain why some group members seem to cope with the lack of rain and can maintain (or even slightly increase) their feeding rates. A previous study, where food availability was experimentally manipulated, showed the helpers are more flexible in their investment in nestling care as compared with breeders, who maintained constant feeding rates [20] regardless on the current conditions. According to this, we found that male helpers, unlike breeders, responded to an increasing number of dry days by reducing their provisioning rate. Interestingly, however, female helpers maintained their effort under the same conditions. A recent study has shown that female helpers signal their contribution to brood provisioning to the dominant breeders and that their permanence in the territory depend on the perceived amount of help that they provide [89]. Assuming that the costs of lack of rain could be affordable for crows, female helpers might therefore be pressured to maintain their provisioning effort constant in order to retain group membership.

Unlike temperature, the time since the last rain showed no significant effect on the degree of carers’ alternation, indicating that, in spite of the reduced effort of some group members, carers might keep on monitoring each other behaviour and adjusting their own nest visit timing accordingly.

Effect of weather on reproductive success

Meteorological stressors are known to affect nestling care in some biparental bird species, like the common fiscal Lanius collaris [34] and the southern yellow-billed Hornbill Tockus leucomelas. Complex effects have been reported in cooperatively breeding species that live in harsh environments, like the pied babbler, where breeders, unlike helpers, reduce their effort with increasing temperatures [94], and the chestnut-crowned babblers, where the social rank plays the opposite effect [69]. High temperatures also affect cooperative species that live at temperate latitudes, like the long-tailed tit [63], where all carers respond to heat by reducing their feeding rates.

Despite of the effect of weather on crow provisioning behaviour, the number of nestlings in successful nests did not significantly correlate with the temperature and the number of rain days during the nestling period. However, our data showed that the body condition worsened for nestlings that were raised during hot periods. This is consistent with the fact that high temperatures hinder carers’ alternation (this study) and hence the regularity of chick provisioning, which is known to affect the development of the nestlings [90]. High temperatures might also have influenced nestling growth more directly, generating a higher demand of energy and water for thermoregulation that carers might have not been able to satisfy [70].

In summary, crows proved sensitive to high temperature and lack of rain both at individual (food provisioning rate) and group level (alternation of nest visits), with immediate consequences on the body condition of their nestlings. Although caution should be taken given the correlative nature of our study, the results raise the question whether human induced global warming is already affecting crow reproduction, causing changes that may affect population persistence.

A recent meta-analysis [50] has revealed that climate change has been affecting avian offspring production only slightly at global scale, with migratory and larger-bodied species being more vulnerable than sedentary and smaller-bodied species. This suggest that the dramatic decline of many bird species around the globe [71, 79] reflects changes in adult/juvenile survival or a reduction of the proportion of the populations that breed [50]. Our data on carrion crows fit the former hypothesis. While offspring production did not vary significatively over the 26-years study period, we found a measurable negative trend in nestling body condition, which is, in this species, a key predictor of juvenile survival [25, 90]. Interestingly, crow populations are decreasing in Spain [2, 84], especially in the northern Mediterranean region, where our study population lives. Other corvid species are declining in the same area, particularly the jackdaw Corvus monedula, the magpie Pica pica and the raven Corvus corax [84], which instead has been reported to increase in desertic areas of North America [57]. These trends support the prediction that climate change will be especially adverse in the Mediterranean regions [48].

The effect of heat on nestling growth and conditions has been reported in several avian species [33, 34, 80, 85, 91], but long-term data are rarely available (see [13] for a notable exception). Our data on the carrion crows, strongly suggest a causal link between global warming and population dynamic, mediated through the effect of high temperature on brood caring behaviour and, ultimately, offspring conditions. More data are urgently needed to understand whether this could be a general process among birds.

Availability of data and materials

Analyses reported in this article can be reproduced using the data provided by Trapote et al., 2023 in Dryad.


  1. Alerstam T, Högstedt G, Evolution of hole-nesting in birds. Ornis Scand 1981;188-193.

  2. Arce LM, Corneja negra Corvus corone. En, B. Molina, A. Nebreda, A. R. Muñoz, J. Seoane, R. Real, J. Bustamante y J. C. del Moral: III Atlas de las aves en época de reproducción en España. SEO/BirdLife. Madrid 2022.

  3. Arnold KE, Owens IPF, Goldizen AW. Division of labour within cooperatively breeding groups. Behaviour. 2005;142(11–12):1577–90.

    Article  Google Scholar 

  4. Atlas Agroclimático de Castilla y León -ITACYL-AEMET-. 2013.

  5. Baglione V, Canestrari D, Chiarati E, Vera R, Marcos JM. Lazy group members are substitute helpers in carrion crows. Proc R Soc B Biol Sci. 2010;277(1698):3275–82.

    Article  Google Scholar 

  6. Baglione V, Canestrari D, Marcos JM, Ekman JB. Kin selection in cooperative alliances of carrion crows. Science. 2003;300(5627):1947–9.

    Article  CAS  PubMed  Google Scholar 

  7. Baglione V, Canestrari D, Marcos JM, Griesser M, Ekman J. History, environment and social behaviour: experimentally induced cooperative breeding in the carrion crow. Proc R Soc Lond Ser B Biol Sci. 2002;269(1497):1247–51.

    Article  Google Scholar 

  8. Baglione V, Marcos JM, Canestrari D. Cooperatively breeding groups of carrion crow (Corvus corone corone) in northern Spain. The Auk. 2002;119(3):790–9.

    Article  Google Scholar 

  9. Baglione V, Marcos JM, Canestrari D, Ekman J. Direct fitness benefits of group living in a complex cooperative society of carrion crows, Corvus corone corone. Anim Behav. 2002;64(6):887–93.

    Article  Google Scholar 

  10. Bates D, Maechler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67(1):1–48.

    Article  Google Scholar 

  11. Bebbington K, Hatchwell BJ. Coordinated parental provisioning is related to feeding rate and reproductive success in a songbird. Behav Ecol. 2016;27(2):652–9.

    Article  Google Scholar 

  12. Bolker B. Getting started with the glmmTMB package. Vienna: R foundation for statistical computing. Software; 2016.

    Google Scholar 

  13. Bourne AR, Cunningham SJ, Spottiswoode CN, Ridley AR. Hot droughts compromise interannual survival across all group sizes in a cooperatively breeding bird. Ecol Lett. 2020;23(12):1776–88.

    Article  PubMed  Google Scholar 

  14. Box GE, Cox DR. An analysis of transformations. J R Stat Soc Ser B (Methodol). 1964;26(2):211–43.

    Google Scholar 

  15. Briga M, Verhulst S. Large diurnal temperature range increases bird sensitivity to climate change. Sci Rep. 2015;5(1):16600.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Brooks ME, Kristensen K, Van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Martin M, Bolker BM. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 2017;9(2):378–400.

    Article  Google Scholar 

  17. Brown JL, Helpers at bird's nests. A worldwide survey of cooperative breeding and related behavior 1988.

  18. Bulluck L, Huber S, Viverette C, Blem C. Age-specific responses to spring temperature in a migratory songbird: older females attempt more broods in warmer springs. Ecol Evolut. 2013;3(10):3298–306.

    Article  CAS  Google Scholar 

  19. Burnham KP, Anderson DR, Huyvaert KP. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol. 2011;65:23–35.

    Article  Google Scholar 

  20. Canestrari D, Chiarati E, Marcos JM, Ekman J, Baglione V. Helpers but not breeders adjust provisioning effort to year-round territory resource availability in carrion crows. Anim Behav. 2008;76(3):943–9.

    Article  Google Scholar 

  21. Canestrari D, Marcos JM, Baglione V. False feeding at the nests of carrion crows Corvus corone corone. Behav Ecol Sociobiol. 2004;55:477–83.

    Article  Google Scholar 

  22. Canestrari D, Marcos JM, Baglione V. Effect of parentage and relatedness on the individual contribution to cooperative chick care in carrion crows. Behav Ecol Sociobiol. 2005;52:422–8.

    Article  Google Scholar 

  23. Canestrari D, Marcos JM, Baglione V. Costs of chick provisioning in cooperatively breeding crows: an experimental study. Anim Behav. 2007;73(2):349–57.

    Article  Google Scholar 

  24. Canestrari D, Marcos JM, Baglione V. Reproductive success increases with group size in cooperative carrion crows Corvus corone corone. Anim Behav. 2008;75(2):403–16.

    Article  Google Scholar 

  25. Canestrari D, Marcos JM, Baglione V. Helpers at the nest compensate for reduced maternal investment in egg size in carrion crows. J Evol Biol. 2011;24(9):1870–8.

    Article  CAS  PubMed  Google Scholar 

  26. Canestrari D, Trapote E, Vila M, Baglione V. Copulations with a nestling by an adult care-giver in a kin-living bird. Behaviour. 2023;160:191–9.,191-199.

    Article  Google Scholar 

  27. Canestrari D, Vera R, Chiarati E, Marcos JM, Vila M, Baglione V. False feeding: the trade-off between chick hunger and caregivers needs in cooperative crows. Behav Ecol. 2010;21(2):233–41.

    Article  Google Scholar 

  28. Clutton-Brock TH. The evolution of parental care. Press: Princeton University; 1991.

    Book  Google Scholar 

  29. Clutton-Brock T. Cooperation between non-kin in animal societies. Nature. 2009;462(7269):51–7.

    Article  CAS  PubMed  Google Scholar 

  30. Cockburn A. Evolution of helping behavior in cooperatively breeding birds. Ann Rev Ecol Systemat. 1998;29(1):141–77.

    Article  Google Scholar 

  31. Cramp, S., Perrins, C. M. (1994). Handbook of the bird of Europe the middle east and North Africa. The birds of the Western Palearctic. Volume VIII Crows to Finches. Oxford University Press. Oxford

  32. Crawley MJ. The R book. Wiley; 2012.

    Book  Google Scholar 

  33. Cunningham SJ, Gardner JL, Martin RO. Opportunity costs and the response of birds and mammals to climate warming. Front Ecol Environ. 2021;19(5):300–7.

    Article  Google Scholar 

  34. Cunningham SJ, Martin RO, Hojem CL, Hockey PA. Temperatures in excess of critical thresholds threaten nestling growth and survival in a rapidly-warming arid savanna: a study of common fiscals. PLoS One. 2013;8(9):e74613.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. De Rosario-Martinez H (2015) phia: post-hoc interaction analysis. R package version 0.2-1. Computer Software

  36. del Río S, Fraile R, Herrero L, Penas A. Analysis of recent trends in mean maximum and minimum temperatures in a region of the NW of Spain (Castilla y León). Theoret Appl Climatol. 2007;90(1):1–12.

    Article  Google Scholar 

  37. del Río S, Herrero L, Penas Á. Recent climatic trends in Castilla and León (Spain) and its possible influence on the potential natural vegetation. Acta Botanica Gallica. 2009;156(4):625–36.

    Article  Google Scholar 

  38. Dickinson J, Hatchwell B. Fitness consequences of helping. In: Koenig WD, Dickinson JL, editors. Ecology and evolution of cooperative breeding in birds. Cambridge University Press; 2004. p. 48–66.

    Chapter  Google Scholar 

  39. du Plessis KL, Martin RO, Hockey PAR, Cunningham SJ, Ridley AR. The costs of keeping cool in a warming world: implications of high temperatures for foraging, thermoregulation and body condition of an arid-zone bird. Glob Change Biol. 2012;18(10):3063–70.

    Article  Google Scholar 

  40. Dunn PO. Changes in timing of breeding and reproductive success in birds. In: Dunn PO, Møller AP, editors. Effects of climate change on birds. Oxford: Oxford University Press; 2019. p. 108–19.

    Chapter  Google Scholar 

  41. Dyrcz A, Halupka L. The response of the great reed warbler Acrocephalus arundinaceus to climate change. J Ornithol. 2009;150(1):39–44.

    Article  Google Scholar 

  42. Edwards EK, Mitchell NJ, Ridley AR. The impact of high temperatures on foraging behaviour and body condition in the western australian magpie Cracticus tibicen dorsalis. Ostrich. 2015;86(1–2):137–44.

    Article  Google Scholar 

  43. El Kenawy A, López-Moreno JI, Vicente-Serrano SM. Trend and variability of surface air temperature in northeastern Spain (1920–2006): linkage to atmospheric circulation. Atmos Res. 2012;106:159–80.

    Article  Google Scholar 

  44. Emlen ST. Evolution of cooperative breeding in birds and mammals. In: Krebs JR, Davies NB, editors. Behavioural ecology: an evolutionary approach. New York: Blackwell Science; 1991. p. 301–35.

    Google Scholar 

  45. Funghi C, McCowan LSC, Schuett W, Griffith SC. High air temperatures induce temporal, spatial and social changes in the foraging behaviour of wild zebra finches. Anim Behav. 2019;149:33–43.

    Article  Google Scholar 

  46. Ghalambor CK, Martin TE. Parental investment strategies in two species of nuthatch vary with stage-specific predation risk and reproductive effort. Anim Behav. 2000;60(2):263–7.

    Article  CAS  PubMed  Google Scholar 

  47. Ghalambor CK, Martin TE. Fecundity-survival trade-offs and parental risk-taking in birds. Science. 2001;292(5516):494–7.

    Article  CAS  PubMed  Google Scholar 

  48. Giorgi F, Lionello P. Climate change projections for the Mediterranean region. Glob Planet Change. 2008;63(2–3):90–104.

    Article  Google Scholar 

  49. Griffiths R, Double MC, Orr K, Dawson RJG. A DNA test to sex most birds. Mol Ecol. 1998;7(8):1071–5.

    Article  CAS  PubMed  Google Scholar 

  50. Halupka L, Arlt D, Tolvanen J, Millon A, Bize P, Adamík P, Albert P, Arendt WJ, Artemyev AV, Baglione V, Bańbura J, Bańbura M, Barba E, Barrett RT, Becker PH, Belskii E, Bolton M, Bowers EK, Bried J, Brouwe L, Bukacińska M, Bukaciński D, Bulluck L, Carstens KF, Catry I, Charter M, Chernomorets A, Covas R, Czuchra M, Dearborn DC, de Lope F, Di Giacomo AS, Dombrovski VC, Drummond H, Dunn MJ, Eeva T, Emmerson LM, Espmark Y, Fargallo JA, Gashkov SI, Golubova EY, Griesser M, Harris MP, Hoover JP, Jagiełło Z, Karell P, Kloskowski J, Koenig WD, Kolunen H, Korczak-Abshire M, Korpimäki E, Krams I, Krist M, Krüger SC, Kuranov BD, Lambin X, Lombardo MP, Lyakhov A, Marzal A, Møller AP, Neves VC, Nielsen JT, Numerov A, Orłowska B, Oro D, Öst M, Phillips RA, Pietiäinen H, Polo V, Porkert J, Potti J, Pöysä H, Printemps T, Prop J, Quillfeldt P, Ramos JA, Ravussin PA, Rosenfield RN, Roulin A, Rubenstein DR, Samusenko IE, Saunders DA, Schaub M, Senar JC, Sergio F, Solonen T, Solovyeva DV, Stępniewski J, Thompson PM, Tobolka M, Török; J., van de Pol, M., Vernooij, L., Visser, M. E., Westneat, D. F., Wheelwright, N. T., Wiącek, J., Wiebe, K. L., Wood, A. G., Wuczyński, A., Wysocki, D., Zárybnická, M., Margalida, A., Halupka, K. The effect of climate change on offspring production in 201 avian populations: a global meta-analysis. Proc Natl Acad Sci. 2023.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Halupka L, Borowiec M, Neubauer G, Halupka K. Fitness consequences of longer breeding seasons of a migratory passerine under changing climatic conditions. J Anim Ecol. 2021;90(7):1655–65.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Halupka L, Czyż B, Macias Dominguez CM. The effect of climate change on laying dates, clutch size and productivity of eurasian coots Fulica atra. Int J Biometeorol. 2020;64(11):1857–63.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Halupka L, Dyrcz A, Borowiec M. Climate change affects breeding of reed warblers Acrocephalus scirpaceus. J Avian Biol. 2008;39(1):95–100.

    Article  Google Scholar 

  54. Hartig F, DHARMa: residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.5, 2022.

  55. Hoover JP, Schelsky WM. Warmer april temperatures on breeding grounds promote earlier nesting in a long-distance migratory bird, the prothonotary warbler. Front Ecol Evol. 2020;8:1–12.

    Article  Google Scholar 

  56. Husby A, Kruuk LEB, Visser ME. Decline in the frequency and benefits of multiple brooding in great tits as a consequence of a changing environment. Proc R Soc B Biol Sci. 2009;276(1663):1845–54.

    Article  Google Scholar 

  57. Iknayan KJ, Beissinger SR. Collapse of a desert bird community over the past century driven by climate change. Proc Natl Acad Sci. 2018;115(34):8597–602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. IPCC, 2021: Summary for Policymakers. In: Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change [Masson-Delmotte, V., P. Zhai, A. Pirani, S.L. Connors, C. Péan, S. Berger, N. Caud, Y. Chen, L. Goldfarb, M.I. Gomis, M. Huang, K. Leitzell, E. Lonnoy, J.B.R. Matthews, T.K. Maycock, T. Waterfield, O. Yelekçi, R. Yu, and B. Zhou (eds.)]. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, pp. 3−32, doi:

  59. IPCC, 2022 Summary for Policymakers. In: Climate Change 2022: Mitigation of Climate Change. Contribution of Working Group III to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change [P.R. Shukla, J. Skea, R. Slade, A. Al Khourdajie, R. van Diemen, D. McCollum, M. Pathak, S. Some, P. Vyas, R. Fradera, M. Belkacemi, A. Hasija, G. Lisboa, S. Luz, J. Malley, (eds.)]. Cambridge University Press, Cambridge, UK and New York, NY, USA. doi:

  60. Labocha MK, Hayes JP. Morphometric indices of body condition in birds: a review. J Ornithol. 2012;153(1):1–22.

    Article  Google Scholar 

  61. Lejeune L, Savage JL, Bründl AC, Thiney A, Russell AF, Chaine AS. Environmental effects on parental care visitation patterns in blue tits Cyanistes caeruleus. Front Ecol Evol. 2019;7:356.

    Article  Google Scholar 

  62. Lüdecke D, Ben-Shachar MS, Patil I, Waggoner P, Makowski D. Performance: an R package for assessment, comparison and testing of statistical models. J Open Source Soft. 2021.

    Article  Google Scholar 

  63. MacColl ADC, Hatchwell BJ. Sharing of caring: nestling provisioning behaviour of long-tailed tit, Aegithalos caudatus, parents and helpers. Anim Behav. 2003;66(5):955–64.

    Article  Google Scholar 

  64. Martin TE. Avian life history evolution in relation to nest sites, nest predation, and food. Ecol Monogr. 1995;65(1):101–27.

    Article  Google Scholar 

  65. McKechnie AE, Effects of climate change on birds. In: Dunn PO, Møller AP (eds) Effects of climate change on birds (Second). Oxford University Press 2019.

  66. McKechnie AE, Wolf BO. Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biol Lett. 2010;6(2):253–6.

    Article  PubMed  Google Scholar 

  67. Mumme RL, Koenig WD, Pitelka FA. Individual contributions to cooperative nest care in the acorn woodpecker. The Condor. 1990;92(2):360–8.

    Article  Google Scholar 

  68. Nomano FY, Browning LE, Nakagawa S, Griffith SC, Russell AF. Validation of an automated data collection method for quantifying social networks in collective behaviours. Behav Ecol Sociobiol. 2014;68:1379–91.

    Article  Google Scholar 

  69. Nomano FY, Savage JL, Browning LE, Griffith SC, Russell AF. Breeding phenology and meteorological conditions affect carer provisioning rates and group-level coordination in cooperative chestnut-crowned babblers. Front Ecol Evol. 2019;7:423.

    Article  Google Scholar 

  70. Oswald KN, Smit B, Lee AT, Peng CL, Brock C, Cunningham SJ. Higher temperatures are associated with reduced nestling body condition in a range-restricted mountain bird. J Avian Biol. 2021.

    Article  Google Scholar 

  71. Pollock HS, Toms JD, Tarwater CE, Benson TJ, Karr JR, Brawn JD. Long-term monitoring reveals widespread and severe declines of understory birds in a protected Neotropical forest. Proc Natl Acad Sci. 2022;119(16): e2108731119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Raihani NJ, Ridley AR. Variable fledging age according to group size: trade-offs in a cooperatively breeding bird. Biol Lett. 2007;3(6):624–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. R Core Team, R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria (2021).

  74. Ricklefs RE, An analysis of nesting mortality in birds 1969.

  75. Rios Cornejo D, Penas Merino Á, Del Río González S. Comparative analysis of mean temperature trends in continental Spain over the period 1961–2010. Int J Geobotanical Res. 2012;2:41–85.

    Article  Google Scholar 

  76. Rios Cornejo D, Penas Merino Á, del Río González S. Comparative analysis of precipitation trends in continental Spain over the period 1961–2010. Int J Geobotanical Res. 2013;3:1–18.

    Article  Google Scholar 

  77. Rodríguez-Fernández A, Blanco-Alegre C, Vega-Maray AM, Valencia-Barrera RM, Molnár T, Fernández-González D. Effect of prevailing winds and land use on Alternaria airborne spore load. J Environ Manag. 2023;332:117414.

    Article  Google Scholar 

  78. Rodríguez-Fernández A, Oteros J, Vega-Maray AM, Valencia-Barrera RM, Galán C, Fernández-González D. How to select the optimal monitoring locations for an aerobiological network: a case of study in central northwest of Spain. Sci Total Environ. 2022;827:154370.

    Article  CAS  PubMed  Google Scholar 

  79. Rosenberg KV, Dokter AM, Blancher PJ, Sauer JR, Smith AC, Smith PA, Marra PP. Decline of the North American avifauna. Science. 2019;366(6461):120–4.

    Article  CAS  PubMed  Google Scholar 

  80. Salaberria C, Celis P, López-Rull I, Gil D. Effects of temperature and nest heat exposure on nestling growth, dehydration and survival in a Mediterranean hole-nesting passerine. Ibis. 2014;156(2):265–75.

    Article  Google Scholar 

  81. Savage JL, Browning LE, Manica A, Russell AF, Johnstone RA. Turn-taking in cooperative offspring care: by-product of individual provisioning behavior or active response rule? Behav Ecol Sociobiol. 2017;71(11):162.

    Article  PubMed  PubMed Central  Google Scholar 

  82. Savage JL, Hinde CA. What can we quantify about carer behavior? Front Ecol Evolut. 2019;7:418.

    Article  Google Scholar 

  83. Seely MK, Louw GN. First approximation of the effects of rainfall on the ecology and energetics of a Namib Desert dune ecosystem. J Arid Environ. 1980;3(1):25–54.

    Article  Google Scholar 

  84. SEO, BirdLife,. Resultados del programa Sacre 1996–2013. Madrid: SEO/BirdLife; 2013.

    Google Scholar 

  85. Sharpe L, Cale B, Gardner JL. Weighing the cost: the impact of serial heatwaves on body mass in a small Australian passerine. J Avian Biol. 2019;50(11).

  86. Smit B, Harding CT, Hockey PAR, McKechnie AE. Adaptive thermoregulation during summer in two populations of an arid-zone passerine. Ecology. 2013;94(5):1142–54.

    Article  CAS  PubMed  Google Scholar 

  87. Sofaer HR, Sillett TS, Peluc SI, Morrison SA, Ghalambor CK. Differential effects of food availability and nest predation risk on avian reproductive strategies. Behav Ecol. 2013;24(3):698–707.

    Article  Google Scholar 

  88. Tieleman BI, Williams JB. Effects of food supplementation on behavioural decisions of hoopoe-larks in the arabian desert: balancing water, energy and thermoregulation. Anim Behav. 2002;63(3):519–29.

    Article  Google Scholar 

  89. Trapote E, Canestrari D, Baglione V. Female helpers signal their contribution to chick provisioning in a cooperatively breeding bird. Anim Behav. 2021;172:113–20.

    Article  Google Scholar 

  90. Trapote E, Moreno V, Canestrari D, Rutz C, Baglione V, [Fitness benefits of alternated chick provisioning in cooperatively breeding carrion crows]. Submitted 2022

  91. Van de Ven TM, McKechnie AE, Er S, Cunningham SJ. High temperatures are associated with substantial reductions in breeding success and offspring quality in an arid-zone bird. Oecologia. 2020;193:225–35.

    Article  PubMed  Google Scholar 

  92. Vicente-Serrano SM, Rodríguez-Camino E, Domínguez-Castro F, ElKenawy A, Azorín-Molina C. An updated review on recent trends in observational surface atmospheric variables and their extremes over Spain. Geograph Res Lett. 2017;43(1):209–32.

    Google Scholar 

  93. Visser ME, van Noordwijk AJ, Tinbergen JM, Lessells CM. Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc R Soc Lond Ser B Biol Sci. 1998;265(1408):1867–70.

    Article  Google Scholar 

  94. Wiley EM, Ridley AR. The effects of temperature on offspring provisioning in a cooperative breeder. Anim Behav. 2016;117:187–95.

    Article  Google Scholar 

  95. Wingfield JC, Pérez JH, Krause JS, Word KR, González-Gómez PL, Lisovski S, Chmura HE. How birds cope physiologically and behaviourally with extreme climatic events. Philos Trans R Soc B Biol Sci. 2017;372(1723):20160140.

    Article  Google Scholar 

  96. Wolf B. Global warming and avian occupancy of hot deserts: a physiological and behavioral perspective. Revista Chilena de Historia Natural. 2000;73:395–400.

    Article  Google Scholar 

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We are grateful to the many field assistants and students who helped with crow banding and video recording. We also thank the group “ATMOSENV” of the University of León for helpful advice. The Agencia Estatal de Meteorología, Ministerio de Agricultura, Alimentación y Medio Ambiente (AEMET) kindly provided the meteorological data that had been used in this article.


This work was funded by the Spanish Ministerio de Economía y Competitividad (Grant CGL2016 – 77636-P to VB).

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All authors conceived the ideas, designed methodology and collected the data; ET and VB analyzed the data and wrote the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

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Correspondence to Eva Trapote.

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Data were collected as part of a long-term population study. All procedures followed ASAB/ABS guidelines and Spanish regulations for animal behavioural research and were approved by Junta de Castilla y León (reference of first released licenses: EP/LE/177-1999; last released licence: EP/LE/681-2019).

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Trapote, E., Canestrari, D. & Baglione, V. Effects of meteorological conditions on brood care in cooperatively breeding carrion crow and consequences on reproductive success. Front Zool 20, 24 (2023).

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  • Cooperative breeding
  • Brood care
  • Reproductive success
  • Meteorological conditions
  • Climate change