Extended incubation recesses in sanderlings are
impacted by temperature and body condition

Léa Etchart, Nicolas Lecomte, François-Xavier Dechaume-Moncharmont,
Jérôme Moreau, Johannes Lang, Thomas Pagnon, Benoit Sittler, Maria
Teixeira, Loïc Bollache, Olivier Gilg

<figure><img src="image_1.png" /></figure>

To cite this version:

Léa Etchart, Nicolas Lecomte, François-Xavier Dechaume-Moncharmont, Jérôme Moreau, Johannes Lang, et al.. Extended incubation recesses in sanderlings are impacted by temperature and body condition. Proceedings of the Royal Society B: Biological Sciences, 2024, 291 (2017), pp.20232264. 10.1098/rspb.2023.2264. hal-04488569

HAL Id: hal-04488569

https://ube.hal.science/hal-04488569v1

Submitted on 26 Aug 2024

**HAL** is a multi-disciplinary open access
archive for the deposit and dissemination of sci-
entific research documents, whether they are pub-
lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d'enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.

<figure><img src="image_2.png" /></figure>
PROCEEDINGS B

royalsocietypublishing.org/journal/rspb

<figure><img src="image_3.png" /></figure>

Research

<figure><img src="image_4.png" /></figure>

<figure><img src="image_5.png" /></figure>

Check for
updates

**Cite this article:** Etchart L *et al*. 2024

Extended incubation recesses in sanderlings are
impacted by temperature and body condition.

Proc. R. Soc. B 291: 20232264.

https://doi.org/10.1098/rspb.2023.2264

Received: 6 October 2023

Accepted: 19 January 2024

**Subject Category:**

Behaviour

**Subject Areas:**

behaviour

**Keywords:**

parental care, incubation strategy, parent-
offspring trade-off, sanderling, Greenland

**Author for correspondence:**

Léa Etchart

e-mail: etchart.lea@gmail.com

Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.7068214.

THE ROYAL SOCIETY
PUBLISHING

Extended incubation recesses in
sanderlings are impacted by
temperature and body condition

Léa Etchart<fnref n="1" />,<fnref n="2" />, Nicolas Lecomte<fnref n="2" />, François-Xavier Dechaume-Moncharmont<fnref n="3" />,
Jérôme Moreau<fnref n="4" />,<fnref n="5" />, Johannes Lang<fnref n="5" />,<fnref n="6" />, Thomas Pagnon<fnref n="1" />,<fnref n="5" />, Benoit Sittler<fnref n="5" />,<fnref n="7" />,
Maria Teixeira<fnref n="4" />, Loïc Bollache<fnref n="1" />,<fnref n="5" /> and Olivier Gilg<fnref n="1" />,<fnref n="5" />

<figure><img src="image_6.png" /></figure>

Complex incubation strategies have evolved to solve the trade-off between parent survival and care for their eggs with often brief departures (recesses) that maximize egg survival, and infrequent extended recesses maximizing adult condition. Here we examined incubation behaviour of sanderlings (Calidris alba), a species that exhibits both biparental and uniparental incubation behaviour. During 11 breeding seasons in Greenland, we have quantified incubation variability with thermologgers placed in nests. We estimated the impact of environmental conditions and individual characteristics on the occurrence and the duration of recesses. We found that extended recesses are a unique feature of uniparentals, and their frequency and duration increased in colder temperatures. The relationship was mediated by body condition, with individuals in poor condition performing longer extended recesses in colder temperatures. This suggests that extended recesses may represent a shift towards self-maintenance at the expense of the egg care, allowing birds to continue incubating under unfavourable conditions. Our study illustrates how extended recesses may be a key breeding strategy to overcome high energetic costs associated with incubation. Quantifying such behavioural flexibility paves the way for tracking future behavioural responses of individuals in the face of changing environments.

**1. Introduction**

Reproduction requires an important investment of time and energy, and breeding
individuals must strike a balance between survival and reproduction during this
critical period. In birds, incubation can be one of the most energetically demand-
ing stages of reproduction [1,2], especially in extreme environments [3]. Harsh
and unpredictable Arctic environments can for instance induce a high pressure
on reproductive individuals. First, the thermoregulation costs for parents are
higher than in more temperate regions [4,5]. Second, incubation is more energy-
consuming due to faster cooling of the eggs in cold weather, necessitating
increased effort from the parent to maintain the optimal temperature at the
nest. For income breeders (i.e. unable to rely on energy reserves stored before

© 2024 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution
License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original
author and source are credited.

<footnote n="1">¹UMR 6249 Chrono-environnement, CNRS, Université de Franche-Comté, 25000 Besançon, France</footnote>

<footnote n="2">²Canada Research Chair in Polar and Boreal Ecology and Centre d'Études Nordiques, Université de Moncton, Moncton, New Brunswick, Canada</footnote>

<footnote n="3">³Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, 69622, Villeurbanne, France</footnote>

<footnote n="4">⁴UMR 6282 CNRS, Université de Bourgogne, 6 boulevard Gabriel, 21000 Dijon, France</footnote>

<footnote n="5">⁵Groupe de Recherche en Ecologie Arctique, 21440 Francheville, France</footnote>

<footnote n="6">⁶Working Group for Wildlife Research at the Clinic for Birds, Reptiles, Amphibians and Fish, Justus Liebig University Giessen, 35392 Giessen, Germany</footnote>

<footnote n="7">⁷Chair for Nature Conservation and Landscape Ecology, University of Freiburg, Freiburg, Germany</footnote>

<footnote>LE, 0009-0004-0095-1196; NL, 0000-0002-8473-5375; FXDM, 0000-0001-7607-8224;
JM, 0000-0001-9984-0998; JL, 0000-0002-7387-795X; TP, 0009-0003-1204-5230;
MT, 0000-0003-4571-7462; LB, 0000-0003-0316-6746; OG, 0000-0002-9083-4492</footnote>
incubation), a significant conflict arises between incubating the
eggs and engaging in essential self-maintenance activities
such as foraging [6], drinking [7] or preening [8]. This conflict
becomes particularly pronounced for uniparental birds,
when only one parent cares for the nest [5].

Unlike species with biparental incubation, uniparental incubators cannot benefit from shared nest duties [9] and must leave their nests more frequently, a behaviour known as a recess [10,11]. Their nests are hence more exposed to predators and cooling [10,12–14]. To maintain a positive energy balance in challenging conditions, birds may employ different strategies. They can either increase the frequency of recess [12] or they can extend the duration of their foraging bouts to compensate for energy loss during inclement weather (see [4,5,15,16]; electronic supplementary material, table S1).

Complex strategies may have evolved within this trade-
off between recess frequency and duration. Some species, or
some individuals within a species, may favour frequent short
recesses, while others may exhibit infrequent prolonged
recesses, coined here as ‘extended recesses’. To date, seven
studies have focused on understanding and analysing the
causes of extended recesses in 11 species with uniparental incu-
bation [4,5,15–19]. While these studies provide first insights
into the challenges of detecting and analysing these incubation
events, they have also created opportunities for quantifying
their duration and elucidating the contributing factors in
other species.

Extended recesses refer to instances when incubating
individuals depart from their nests for a relatively long
period of time (length can vary; see section 2d). These
recesses are often considered as rare occurrences or disre-
garded as measurement artefacts. However, a few studies
have already highlighted their occurrence, primarily in
relation to prolonged periods of cold or stormy weather
[5,16,18,19]. With low temperatures, incubating parents may
indeed take longer recesses to fulfil their own energy require-
ments [20]. However, these extended foraging periods also
expose the eggs to fluctuating external temperatures, poten-
tially slowing down or even pausing the embryogenesis
[21,22]. As a consequence, delayed hatching and increased
exposure to predators can occur [23]. Thus, extended recesses
can be viewed as a specific trade-off between adult survival
and maintenance on one hand, and egg development on
the other, when the typical shorter recesses no longer
enable the birds to cope with their environment. In this con-
text, the body condition of the incubating parents may also
play a critical role and further modulate this trade-off.
Additionally, the differential investment in pre-laying activi-
ties between males and females, such as females laying
eggs [12], may also influence incubation strategies.

The aim of the study was to assess the occurrence, predic-
tors, and underlying factors of extended recesses on the daily
incubation behaviour in an Arctic-nesting shorebird using
both bi- and uniparental care during the incubation period,
the sanderling (Calidris alba). We used 11 years of observational
data collected at two high-Arctic study sites. Despite perma-
nent daylight, sanderlings maintain a day-night incubation
rhythm. During the ‘night-time’ (i.e. between 17.00 and
09.00), birds incubate almost continuously, taking only few
recesses [5] while during daytime (i.e. the warmest period of
the day), birds will take advantage of the warm hours to take
more recesses. First, we aimed at determining the environ-
mental conditions and individual characteristics leading to

the occurrence and duration of extended recesses. In addition,
we sought to identify the time interval between the triggering
event and the onset of the extended recess, considering the
daily trade-off between survival and reproduction. We also
conducted a comparative analysis, examining how the environ-
mental conditions and individual characteristics influence the
duration of the classical short recesses. Second, we assessed
the consequences of extended recesses on the interpretation
of the total duration of recesses per day (TDR). TDR is a
commonly used proxy (e.g. [6,13]) for studying incubation
behaviour, as it directly reflects the nest attentiveness [24].
By analysing TDR, we could compare our findings with pre-
vious studies and assess the importance of extended recesses
at the daily scale.

As an income breeder, the sanderling heavily relies on its
immediate environment for breeding and survival [25]. Given
that it breeds in harsh high-Arctic regions and arrives from
long-distance migrations with depleted energy reserves, we
hypothesized that by breeding at the limit of their physio-
logical capabilities, sanderlings perform extended recesses
when under stressful environmental or individual conditions.
We predicted: (i) that extended recesses would predomi-
nantly occur in uniparental nests, as biparental parents
have more time for self-maintenance activities during the
incubation period; (ii) that females would exhibit a higher
likelihood of performing extended recesses compared to
males, considering the energetic demands of eggs-laying;
(iii) that the occurrence and duration of extended recesses
would increase after periods of cold temperatures due to
heightened energetic requirements and reduced activity (i.e.
availability) of arthropod prey; and (iv) that an interaction
between body condition and climatic conditions should
exist, whereby colder periods would have a more pro-
nounced effect on weaker individuals within the population.

## 2. Material and methods

### (a) Study species and sites

The sanderling is a small (44–71 g) long-distance migratory
shorebird breeding in the High Arctic (electronic supplementary
material, figure S1c) [26]. They usually arrive at their northeast
Greenland breeding grounds from late May to mid-June [27].
Upon arrival they switch their diet from small marine invert-
ebrates to terrestrial arthropods (i.e. both insects and spiders).
They are generalist insectivores, with a broader diet than
other species in this guild (e.g. dunlins, *Calidris alpine*; snow
buntings, *Plectophenax nivalis* [28]). This is likely to be beneficial
in high-arctic environments, where the abundance of prey
is highly variable [29]. For example, some arthropods (e.g.
*Tipulidae, Chironomidae*) will peak synchronously in early
summer, providing short resource peaks for arctic shorebirds,
while others (e.g. *Areneae*) are less abundant but available
throughout the breeding season [30].

Sanderlings also exhibit a mixed incubation strategy, with both
biparental and uniparental care observed, and with both sexes
able to incubate and rear chicks [31–33]. We studied sanderlings
during 11 consecutive breeding seasons (2011–2021), from mid-
June to early August, at two locations in Greenland: Hochstetter
Forland (75.15°N 19.70°W) and Karupelv Valley (72.50°N
24°W) (electronic supplementary material, figure S1a). We treated
these sites as one population (no difference among them in
statistical analyses; see sections 3d–3f).

Winters in northeast Greenland are characterized by very
cold temperatures, ranging between -15°C and -25°C. However,
during the sanderling's breeding season, temperatures rise above 0°C, with average monthly temperatures between 2°C and 4°C [34]. Both study sites are within the Northeast Greenland National Park, an area with minimal human impact, and are part of the 'prostrate shrub tundra' bioclimatic subzone [35].

## (b) Nest monitoring, timing of breeding and ground-level temperatures

Nests were searched in suitable habitats and located opportunistically by flushing incubating adults or by following birds with anti-predator behaviour [36]. For nests discovered during laying, we assumed a laying rate of one egg per day to determine the initiation of incubation (with an average of 4 eggs per nest) [37]. To estimate the first day of incubation for nest with complete clutches, we employed three approaches. This involved using the hatching time recorded with thermologgers (see below), direct observations of hatching eggs or young in the nest cup (with the mean incubation period of the species subtracted), or by floating the eggs [38] (electronic supplementary material, figure S2). We used the incubation starting date to estimate the age of the clutch throughout the entire incubation period.

Ground-level temperature was determined as in [11]. We used the temperatures recorded at one-minute intervals from inactive nests, which included nests that were deserted, predated or hatched, within the same site and similar habitat (see following section for details). These records provided representative measurements of the daily and hourly ground-level temperature specific to the sanderling breeding microhabitat at each site.

## (c) Incubation behaviour and incubation strategies

In each nest, we monitored incubation behaviour using a temperature probe (Flylead Thermistor PB 5009 with 60 cm cable) coupled to a data logger (TinyTag Plus2 TGP-4020; Gemini Data Loggers Inc., West Sussex, UK; electronic supplementary material, figure S1d; see method elsewhere, e.g. [10,11]). Probes were set to record temperature every minute.

Uniparental and biparental incubation strategies were assigned to each nest following [39], and only uniparental nests were used in the following analyses (see section 2e). This approach uses a discriminant equation based on the daily number and duration of recesses observed in nests with known strategies. It has been shown to reliably assign the incubation strategy of sanderlings (i.e. 99% after 24 h and 100% after 4 days of temperature recording).

## (d) Quantifying recesses

Incubation recesses have already been investigated in many bird species, including sandpipers [5,10,11,15]. These recesses are fundamental for birds to pause their incubation, allowing them to forage in order to rebuild their energetic reserves. For most species, these recesses tend to occur during the warmest periods of the day [11], i.e. when arthropods availability is the highest [24]. Being ectotherms, arthropods availability is known to be linked with temperatures, wind speed, or precipitations [40,41]. In some instances, long recesses lasting from one to 72 h have been reported (e.g. [42]). However, a standardized method for detecting and quantifying these extended recesses has yet to be established.

In our study we only considered recesses longer or equal to three minutes to account for the possible uncertainty of 1–2 min around the documentation of the exact onset and ending times of a recess. To score and measure the duration of each recess, we employed a modified method based on previous studies. Instead of considering a recess when the nest's temperature had fallen by 3°C or more from the median incubation temperature over a 24 h period [10,11,39,43], for days with median incubation

temperature above 36°C (in order to filter low quality recordings), we defined a recess as a withdrawal characterized by a temperature drop of 4.5°C from the maximum temperature over a 24-hour period. While both methods yield similar results for short recesses (electronic supplementary material, table S2), the first method is in fact inadequate to document extended recesses as the median nest temperature can drop below 36°C during those periods, regardless of the quality of the recording. Our alternative method, based on maximum temperature values, hence allowed us to include extended recesses in the analysis.

To filter out poor-quality records, we retained nests with ≥24 h monitoring and used a threshold of 37.5°C for the maximum daily ground-level temperature (accounting for the 1.5°C difference mentioned earlier). Furthermore, we removed days with erratic patterns, malfunctioning TinyTags (27 nests) and recesses corresponding to the capture of individuals. From this filtered dataset, we extracted each recess, calculated its duration, and then determined the total daily duration of recesses (TDR), which represents the sum of all recess duration recorded over a 24 h period.

The distribution of recess duration exhibited a distinct bimodal pattern, with extended recesses forming a separate mode on the right side of the distribution (figure 1b). To determine an objective threshold (i.e. value above which a recess is considered as 'extended') for distinguishing between 'short' and 'extended' recesses, we used the 'multimode' package [44] and retained the antimode as our discriminating threshold (i.e. approximately 120 min, consistent with a previous analysis [4]; figure 1b). Furthermore, the bimodal distribution of recess duration precluded its use as a continuous variable in our LMMs (see below), a limitation that also runs counter to the assumption of normal distribution required for our analyses. This statistical categorisation of recesses into shorter and longer duration is inherently tied to our data collection approach, and we posit that this method could be applied in various other sites and species as a means of objectively delineating recess duration. Although the demarcation between shorter and longer recesses near the antimode point may appear somewhat arbitrary, it provides a useful framework for grouping recess duration in a standardized manner.

To estimate the 95% confidence intervals (95% CI) for this threshold, we employed 1000 bootstrap iterations for each year and study site. Furthermore, we compared overlapping 95% confidence intervals in the forest plots to assess significant differences in threshold values among years (electronic supplementary material, figure S3) and/or between study sites (HOCH cut-off value = 111.5 min, CI [96.1;123.7], KVPE cut-off value = 113.3 min, CI [93.2;136.7]) [45,46].

## (e) Body condition

When feasible, incubating birds were caught on their nest with a 40 cm-wide clap net set up over the nest. We took the tarsus length, from the tarsal joint to the distal end of the tarso-metatarsus with digital or dial callipers (±0.1 mm) and body mass using spring scales (±1.0 g with 100 g Pesola spring scales, Pesola AG, Baar, Switzerland). We used these measurements to assess the body condition of 71 incubating individuals using the scaled mass index [47]. Birds were only captured once during the incubation period (mostly during the first half of the incubation) therefore not representing the seasonal changes in body condition, but there was no evidence of change in body mass during the season at the population level (electronic supplementary material, figure S4, table S3). Morphometric measurements were also used to determine the sex of individuals for which molecular sexing was not available (see electronic supplementary material).

## (f) Statistical analyses

Although extended recesses were present in a few biparental nests, their occurrence in these nests was anecdotal (see
<figure><img src="image_7.png" /><figcaption>**Figure 1.** Duration and number of extended recesses recorded on sanderling nests in Greenland (2011–2021). (a) Example of a TinyTag recording from Hochstetter site (2019), with two extended recesses of 274 and 544 min between several short recesses of 1–27 min; yellow line: maximum ground-level temperature recorded that day; blue line: temperature threshold (Tmax −4.5°C) used to define recesses. (b) Distribution of recess durations (in log-scale); the purple vertical lines represent the two modes of the distribution, 7.1 and 337.5 min). The orange vertical line represents the antimode, 119.3 min discriminating short and extended recesses (see Material and methods). (c) Annual proportion of extended recesses (over the total number of recesses). (d) Annual proportion of extended recesses’ durations (over the total duration of recesses). In both lower panels, the number of extended recesses is given in the bars and dashed lines represent mean proportions over the period 2011–2021 (including 2017 and 2018 with 0 extended recess, but not shown on the panels).</figcaption></figure>

section 3a). We therefore restricted our analyses to uniparental
nests (including the final uniparental period of ‘swap nests’,
i.e. biparental nests with desertion of one breeder during
the monitoring period) to document the presence, causes and
consequences of this behaviour.

We collected the following individual variables: body con-
dition, sex, nest types (uni/swap), and ground-level temperature
data. Cold ground-level temperatures may compel birds to
remain in the nest until their energy reserves are depleted, leading
to extended recesses. Therefore, the pre-recess temperature values
could potentially explain the nature (short or extended) and
duration of the recess. However, we lacked prior knowledge
regarding the most relevant duration of the time window preced-
ing the recess to record ground-level temperature for predicting
the nature or duration of recesses. To determine the appropriate
response time to ground-level temperature, we conducted two
optimization models using different lengths of time windows
(i.e. average ground-level temperature measured during 1, 2, 6,
12 and 24 h periods before the onset of the recess; electronic sup-
plementary material, figure S5, table S4). We used the Akaike’s
information criterion (AIC) to compare the competing models

and identified the set of time windows that equally captured
our data [48].

We collected ground-level temperature data and individual
variables (body condition, sex, uni/swap) for 63 uniparental
nests, totalling 8122 recesses. First, we analysed how these
variables could predict whether a recess was short (coded as 0)
or extended (coded as 1). We used a generalized linear mixed-
effect model (GLMM) with a binomial error distribution, a
logit link function, and the probability of a recess being either
short or extended as the response variable. The fixed variables
included body condition, mean ground-level temperature
before recess, and sex of the incubating parent. We tested for
an interaction between the ground-level temperature and body
condition and selected the best models based on R² values (elec-
tronic supplementary material, table S6). We hypothesized that
there would be a cumulative effect, where cold conditions nega-
tively impact all individuals but have a greater one on those in
poor body condition. In addition, we included three covariates:
incubation date (i.e. number of days since the beginning of incu-
bation) to control for the incubation stage; periods of the day
(day/night) to control for a potential circadian rhythm, and
type of nest (uni/swap) to control for nest strategies. Nest identity was included as a random variable to account for the repeated measure design.

Second, we assessed the effect of environmental and intrinsic variables on the duration of (a) extended (n = 167 recesses for 37 nests) and (b) short recesses (8345 recesses for 64 nests). The response variable (duration of the recess) was integrated in a linear mixed-effect model (LMM) with an identity link function (Gaussian family). The fixed variables included body condition, mean ground-level temperature before recess, and sex of the incubating parent. We tested for an interaction between ground-level temperature and body condition and selected the best model based on R² values (electronic supplementary material, table S6). We also incorporated incubation date and nest type as covariates. Nest identity was included as a random variable to account for the repeated measure design.

In a second set of analyses, we investigated the consequences of extended recesses on the total duration of recesses per day (TDR). Here we discriminated between days with (135 days on 35 nests) or without (156 days on 50 nests) extended recesses. Using LMM with an identity link (Gaussian family), we examined the effects of mean daily ground-level temperature, sex, body condition as fixed factors, along with incubation day and uni/swap as covariates. For both models, we tested for an interaction between ground-level temperature and body condition and selected the best model based on their R² values. Nest identity was included as a random variable to account for the repeated measure design.

In all models with an interaction term (electronic supplementary material, table S6), we estimated the value of body condition upon which the relationship between the response variable and the temperature was no longer significant with the 'simple slopes analysis' of the 'jtools' package and Johnson-Neyman intervals [49]. We used three body condition values (minimal, maximal and population median) to calculate the conditional slope of the temperature predictor. To properly manage Type I and II error rates, we applied the false discovery rate adjustment as suggested in [50].

We conducted statistical analyses using R freeware version 4.1.1 [51]. We used the 'lme4' package [52] for both GLMM and LMMs. p-values for LMMs were obtained using t-tests with the Satterthwaite's method for calculating degrees of freedom (package lmerTest [53]). We used the 'jtools' package [49] to perform the 'simple slopes analysis', with the sim_slopes function. Numerical explanatory variables were scaled (Z-scored) and assumptions of normality and homogeneity of variance were assessed through visual inspection of the residuals.

# 3. Results

## (a) Recess detection, duration and numbers

During the 11 years of the study, we discovered 286 nests and continuously monitored 251 of them using TinyTags. A total of 16 518 recesses were documented from the 170 nests that provided usable data, resulting in a dataset covering 1380 nest-days (electronic supplementary material, table S5). Incubation recesses were ubiquitous as every nest had at least one recorded recess, with 4160 recesses documented in biparental nests (n = 67) and 16 518 in uniparental and swap nests (n = 103). On average, uniparental and biparental sanderlings took 23.6 and 9.6 recesses per 24 h period respectively (ranges 1–68 and 1–32).

We only detected 14 extended recesses (i.e. 0.2% of the total number of recesses) in 10 biparental nests, compared to 340 in uniparental and swap nests (i.e. 2% of the total number of recesses [=16 518]; see dotted line in figure 1c).

Among the 103 uniparental and swap nests, 60 recordings (58%) included at least one extended recess during incubation, whereas only 10 out of 67 biparental nests (15%) did. Extended recesses were observed in all years, except for 2017 when monitoring duration was the shortest, and in 2018, when only few nests were found due to very late snowmelt (electronic supplementary material, table S5).

Extended recesses lasted from 120 (i.e. our fixed minimum; see section 2d) to 1353 min (electronic supplementary material, figure S6; mean: 391; median: 340). Despite being rare (figure 1c), extended recesses greatly contributed to the total duration of recesses documented in most years (figure 1d).

## (b) Optimization models

Our two optimization models returned different time steps. For the probability of extended recesses occurrence, the best model clearly selected ground-level temperatures averaged over the 12 h preceding the recess (electronic supplementary material, figure S5a, table S4a; marginal R² = 0.17, conditional R² = 0.44, i.e. coefficient of determination for generalized linear mixed models [54]). For the duration of extended recesses, the models with ground-level temperatures averaged over the six hours (electronic supplementary material, figure S5b, table S4b; marginal R² = 0.10, conditional R² = 0.30) and over the two hours (marginal R² = 0.098, conditional R² = 0.31) preceding the recess were equally supported (ΔAIC = 2 [48]). The one-hour model was only slightly different from the two-hour model (electronic supplementary material, table S4B). For clarity, we presented the results for six-hour time step, but all steps are discussed below (see section 3d).

## (c) Probability of occurrence of an extended recess

Considering the full range of recorded ground-level temperatures (1.6–26.2°C), our top-ranked GLMM model predicted that the probability of taking an extended recess decreased by an average of 20% for each increase of one degree Celsius (marginal R² = 0.21; conditional R² = 0.46; 8122 recesses for 63 nests; figure 2). The interaction between temperature and body condition was not included in our top-ranked model (electronic supplementary material, table S6). The other model variables (body condition, sex, nest age, uni/swap, period of the day) did not impact the occurrence of extended recesses (electronic supplementary material, table S7).

## (d) Duration of extended recesses

Our top-ranked linear mixed model included the interaction between body condition and ground-level temperature averaged over the 6-hours preceding the recess (electronic supplementary material, table S6). This model predicted that the duration of an extended recess decreased as ground-level temperature and body condition increased (R²_m = 0.15; R²_c = 0.23; 167 extended recesses in 37 nests; figure 3b; electronic supplementary material, table S8). On average, this model also detected a possible interaction between the two predictor variables; and figure 3b presents the model predictions for the minimum (41.3), median (57.8) and maximum (68.2) values of body condition, illustrating the impacts of ground-level temperature on the duration of extended recesses across the range of possible body conditions.
<figure><img src="image_8.png" /><figcaption>**Figure 2.** Probability of sanderlings performing an extended recess over a short recess according to the ground-level temperature averaged for the 12 h preceding the beginning the recess in Greenland (2011–2021). The shaded area shows the 95% confidence interval. R<sup>2</sup><sub>m</sub> and R<sup>2</sup><sub>c</sub> correspond to the marginal and conditional R<sup>2</sup> respectively.</figcaption></figure>

For individuals with the lowest body condition, the model predicted an average decrease of approximately 21 min in the duration of an extended recess for each one-degree Celsius increase in ground-level temperature, spanning a range of 0.6–22.4°C. The decrease was three times smaller (around 7 min per degree Celsius) for individuals with median body condition, while individuals with the highest body condition showed a lengthening of approximately 1 min per degree Celsius.

The ‘simple slopes analysis’ and the Johnson–Neyman intervals, which accounts for the false discovery rate adjustment, revealed that the relationship between duration of extended recesses and ground-level temperature was no longer significant above a body condition of 58.5. This indicates that ground-level temperature impacts the duration of extended recesses for more than half of the breeding adults in this population (i.e. body condition less than 57.8). The other model variables (sex, nest age, uni/swap) included in the model did not influence the duration of extended recesses (electronic supplementary material, table S8).

### (e) Duration of short recesses

To assess whether recess duration was related to preceding ground-level temperatures, we first ran models using ground-level temperature averaged at three different time scales: 1, 2 and 6 h preceding the beginning of the recess. However, the results showed no significant differences. Consequently, we focused on the six-hour model, aligning with the extended recesses’ model mentioned earlier. Our top-ranked linear mixed model excluded the interaction between ground-level temperature and body condition (electronic supplementary material, table S6). This model predicted only small variations in the duration of short recesses (R<sup>2</sup><sub>m</sub> = 0.003; R<sup>2</sup><sub>c</sub> = 0.12; 8354 recesses for 64 nests; figure 3a; electronic supplementary material, table S9). Only nest age influenced the duration of recesses. For each incubation day, recess duration lengthened by ca 5 s. The other model variables (temperature, body condition, sex, uni/swap) had no

impact on short recesses duration (electronic supplementary material, table S9).

### (f) Total duration of recesses per day

On average, the TDR was approximately 596 min for the days with extended recesses, but half as long for days without (approximately 288 min; figure 3c,d). The top-ranked TDR LMM model for days with both short and extended recesses (135 days, 35 nests) included the interaction between ground-level temperature and body condition (R<sup>2</sup><sub>m</sub> = 0.23; R<sup>2</sup><sub>c</sub> = 0.47; electronic supplementary material, table S6; table S10; figure 3d). This model predicted a decrease in TDR with the mean daily ground-level temperature, especially for birds with poor body condition.

Throughout the full range of recorded ground-level temperatures (2.6–16.87°C), the TDR for the lowest recorded body condition (41.3) decreased by an average of approximately 29 min for every one-degree Celsius increase of temperature (figure 3d). By contrast, for birds with a median body condition (57.8), the TDR decreased by only 9 min per degree Celsius, while it increased by approximately 3 min for the highest body condition (68.2), although it was not statistically significant.

The ‘simple slopes analysis’ and the Johnson–Neyman intervals, which accounts for the false discovery rate, indicated that the relationship between the TDR and ground-level temperature was no longer significant for birds with a body condition above 57.6 (i.e. close to the median value of the population). Without adjusting for the false discovery rate, the body condition threshold was 58.1. Hence, for nearly half of the population performing extended recesses, ground-level temperature impacted the TDR. Additionally, the TDR increased by approximately 11 min on average for each incubation day. The other model variables (sex, uni/swap) did not have a significant impact on the TDR (electronic supplementary material, table S10).

Our top-ranked TDR LMM model for days without extended recesses (156 days, 50 nests) did not include the
<figure><img src="image_9.png" /><figcaption>**Figure 3.** Changes in the duration of sanderling recesses for the range of ground-level temperatures measured in Greenland (2011–2021). Upper panels present the effect of the ground-level temperature averaged over the 6-hours preceding the beginning of a recess on the duration of (a) short recesses and (b) extended recesses in sanderling. Lower panels present the effect of the mean daily ground-level temperature on the total duration of recesses per day (TDR) for: (c) days with only short recesses and (d) days with a mix of short and extended recesses. The model fit is in solid line, 95% CI in shading, and dots are raw data. Panels (b) and (d) are the results of an interaction between the respective ground-level temperature and the body condition. Three different body conditions (min, median, max) are represented to describe the range of body conditions existing in the population. Dashed lines in panels (b) and (d) present nonsignificant interactions between ground-level temperature and body condition (for individuals with highest body condition). Annotated $R_m^2$ and $R_c^2$ correspond to marginal $R^2$ and conditional $R^2$, respectively.</figcaption></figure>

interaction between ground-level temperature and the body condition (electronic supplementary material, table S6). For each increase of one degree Celsius throughout the full range of recorded ground-level temperatures (2.6–19.2°C; figure 3c), this model predicted that the TDR lengthened by approximately 4 min on average for days without extended recesses and for each incubation day (Model $R_m^2$ = 0.14; $R_c^2$ = 0.57; 156 days for 50 nests; electronic supplementary material, table S11). The other model variables (body condition, sex, uni/swap) did not have a significant impact on the TDR (electronic supplementary material, table S8).

## 4. Discussion

Our 11-year study highlights the variability occurring in recess type and duration influenced by environmental and body conditions. Extended recesses are a regular feature in the incubation behaviour of uniparental sanderlings,

supporting our first prediction. While our study shows 58% of uniparental nests exhibiting extended recesses, the few other published estimates varied widely, from 7% to 100% (electronic supplementary material, table S1).

Our study also revealed that the likelihood of performing an extended recess decreased by 10% across the entire range of ground-level temperatures (1–26°C), irrespective of body condition. Two other species of shorebirds (i.e. white-rumped sandpiper; *Calidris fuscicollis*; red phalarope; *Phalaropus fulicarius*) showed a similar change of up to 14% for a range of windchill temperatures of –15 to 8.5°C [15]. In spite of variable responses to temperature, our species illustrate the potential for heightened reproductive costs. This assertion gains support from our findings of a combined impact of body condition and temperature on extended recess duration, supporting our predictions. We quantified these individual responses, revealing that individuals with poorer body condition exhibited longer recesses, especially at lower temperatures. Conversely, short recesses duration remained unaffected by both body
condition and temperature across a temperature range of 1 to
26°C (figure 3a).

Beyond our fine temporal analyses, we employed the TDR proxy to assess incubation behaviour, allowing comparison with previous studies e.g. [5,10,11]. First, sanderlings do not replace short recesses by one long recess per day. The TDR for days with extended recesses was nearly twice as long as the TDR for days without, indicating that extended recesses affect daily nest attendance. Second, our daily-scale findings echoed those at the recesses scale (i.e. warmer temperatures influenced the TDR negatively for days featuring extended recesses). While quantifying TDR is common, limited studies have accounted for extended recesses and recess duration (e.g. [6]). In line with our findings, previous study reported a negative association between air temperature and TDR (albeit without reporting effect sizes) by considering extended recesses, along with a positive relationship without extended recesses, across four arctic shorebird species. To our knowledge, our study is the first to demonstrate a relationship between TDR and body condition across varying air temperatures. This could help re-evaluate TDR metric in previous studies

(a) Drivers of extended recesses

Ground-level temperature alone could explain the occurrence of extended recesses, but both ground-level temperature and body condition influenced their duration. Cold spells increase energetic pressure for both the parent and the eggs, as parents lose more energy and eggs cool faster when unattended [4,5]. Birds can withstand harsh conditions for some time before initiating extended recesses. Unlike short recesses, mostly taken during daytime, extended recesses happened at any time, both daytime and night-time. Therefore, the exact time of departure for an extended recess may be related to the current energy balance and energy loss during incubation bouts (i.e. two variables that we could not measure), which are reflected in temperature measurements. It is also possible that a certain degree of mass loss due to cold temperatures triggers an extended recess, regardless of the bird's body condition.

While temperature impacts the energy balance, it also impacts food availability via its influence on arthropod abundance and activity [55]. Therefore, under cold conditions, sanderlings may need more time for energy replenishment, especially to compensate for the low availability of arthropods. However, this effect is likely mediated by the body condition, with individuals in better conditions having more energy to invest in reproduction [56,57] and experience fewer energetic constraints than those in poorer condition. While declining temperatures trigger extended recesses regardless of body condition, the duration of extended recesses only increases for individuals below a given threshold of body condition (see section 3d; figure 3b). Extended recesses have been poorly studied especially in shorebirds in the past but are likely linked to body condition. Blue petrels (Halobaena caerulea) for example, exhibited extended recesses when a certain mass threshold was reached, but when food availability was low, the birds returned to their nest with a reduced body mass [58]. If extended recesses do not provide sufficient gain, individuals face the dilemma of returning to their nest in even poorer condition, lengthening their foraging bouts, or ultimately abandoning their nest. In this case, extended recesses could be detrimental for the adults that did not meet their energetic needs, but also

for the eggs. While no study described a potential impact on
the chicks' development, extended recesses likely lengthen
the incubation period, mechanistically increasing the risk of
predation, but probably also reduce embryo viability [16].
Extended recesses are probably not always sufficient for
birds to fully replenish depleted reserves and could explain
why some individuals in our study performed successive
extended recesses. Finally, the presence and duration of
extended recesses were not influenced by sex nor nest type
(uniparental versus swap) in our study, suggesting that pre-
incubation behaviour costs could be balanced between sexes.
The absence of difference between the two types of uniparental
nests included in our analyses (i.e. uniparental and swap nests)
supports our methodological choice to merge these two types
of nests in our analyses.

(b) Timestep influence on extended recesses

In all the studies quoted above, the occurrence and tempera-
tures related to extended recesses were analysed at a daily
time scale. In our study, we also investigated the speed of
individual responses to temperatures. Although our results
can be compared with previous studies, it is important to
bear these scaling differences in mind. We demonstrated
that the average ground-level temperature measured in the
12 h prior to the start of an extended recess best predicted
its occurrence, while a shorter timestep (6 h, 2 h or 1 h) best
predicted its duration. The 12 h timestep suggests that some
birds can endure harsh conditions for a relatively long
period (i.e. 6–12 h) before initiating long recesses. On the
other hand, the duration of extended recesses appears to be
a more immediate response, with a 6 h timestep being the
best predictor (and being not competitively different with
the 2 h and 1 h timesteps; electronic supplementary material,
figure S5b, table S4b). While their scales were different (incu-
bation, daily and recess), Diez-Méndez et al. [59] already
stated the importance of studying incubation behaviour at
different time scales, as it provides insights into various
aspects of this behaviour.

(c) Perspectives

Extended recesses could allow parents to pursue the incubation, despite harsh environmental and poor body conditions. While some papers described a lengthening of the incubation because of extended recesses (e.g. [17]), and therefore a longer exposition to predation pressure, our dataset did not allow us to explore this question. It would be worth studying this potential lengthening in more detail, as well as the potential impact of extended recesses on predation pressure. To go further in understanding the fluctuations in energy reserves during incubation bouts, we identify the need for quantifying the foraging patterns and distances of adults during recesses along with their body reserves.

Finally, our study highlights the importance of extended recesses as a significant component of the incubation strategy in sanderlings and potentially in other species as well. Investigating this behaviour in other species with different life-history traits, such as body masses, would facilitate species comparisons and contribute to a better understanding of how this behaviour is linked to the biology and physiology of each species.
J.L.: writing—review and editing; T.P.: data curation; B.S.: writing—review and editing; M.T.: methodology, writing—review and editing; L.B.: funding acquisition, project administration, supervision, validation, writing—review and editing; O.G.: conceptualization, data curation, methodology, supervision, validation, writing—review and editing.

All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

**Funding.** This work was supported by the ANR (ANR-21-CE02-0024 PACS to L.B.) as well as the IPEV (French Polar Institute-IPEV ‘Interactions 1036’ programme). N.L. and L.E. were supported by the Canada Research Chair program and NSERC. This work is part of L.E.’s PhD thesis co-supervised by O.G., L.B. and N.L.

**Acknowledgements.** The authors are grateful to all people who helped collect the field data across the years. We also thank Nicolas Meyer for his help with the scripts and data management.

**Ethics.** Separate annual research permits were granted by the Government of Greenland for the Hochstetter site (permit numbers: C-11-4-12, C-12-4-17, C-13-4-29, C-14-4-23, C-15-4-10, C-16-4-15, C-17-3-28, C-18-3-11, C-19-3-03, C-20-3-19, C-21-3-22) and Karupelv site (permit numbers: C-11-14, C-12-28, C-13-11, C-14-16, C-15-14, C-16-20, C-17-23, C-18-24, C-19-36, C-20-33, C-21-33).

**Data accessibility.** Data are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.v41ns1s3q [60]. Electronic supplementary material is available online [61].

**Declaration of AI use.** We have not used AI-assisted technologies in creating this article.

**Authors' contributions.** L.E.: conceptualization, data curation, formal analysis, investigation, methodology, writing—original draft, writing—review and editing; N.L.: methodology, supervision, validation, writing—review and editing; F.X.D.M.: methodology, writing—review and editing; J.M.: writing—review and editing;

## References

1. Turner JS. 1997 On the thermal capacity of a bird's egg warmed by a brood patch. *Physiol. Zool.* **70**, 470–480. (doi:10.1086/515854)

2. Williams JB. 1996 Energetics of avian incubation. In *Avian energetics and nutritional ecology* (ed. C Carey), pp. 375–416. London, UK: Chapman and Hall.

3. Camfield AF, Martin K. 2009 The influence of ambient temperature on Horned Lark incubation behaviour in an alpine environment. *Behaviour* **146**, 1615–1633. (doi:10.1163/156853909X463335)

4. Holt S. 2002 Uniparental incubation in a cool climate: behavioural adaptations in the Eurasian dotterel. See http://hdl.handle.net/1893/3248.

5. Tulp I, Schekkerman H. 2006 Time allocation between feeding and incubation in uniparental arctic-breeding shorebirds: energy reserves provide leeway in a tight schedule. *J. Avian Biol.* **37**, 207–218. (doi:10.1111/j.2006.0908-8857.03519.x)

6. Conway CJ, Martin TE. 2000 Effects of ambient temperature on avian incubation behavior. *Behav. Ecol.* **11**, 178–188. (doi:10.3963/j.issn.2095-3844.2016.05.029)

7. Lecomte N, Gauthier G, Giroux J-F. 2009 A link between water availability and nesting success mediated by predator-prey interactions in the Arctic. *Ecology* **90**, 465–475. (doi:10.1890/08-0215.1)

8. Criscuolo F, Gauthier-Clerc M, Gabrielsen GW, Le Maho Y. 2000 Recess behaviour of the incubating common eider *Somateria mollisima*. *Polar Biol.* **23**, 571–574. (doi:10.1007/s003000000123)

9. Steiger SS, Valcu M, Spoelstra K, Helm B, Wikelski M, Kempenaers B. 2013 When the sun never sets: diverse activity rhythms under continuous daylight in free-living arctic-breeding birds. *Proc. R. Soc. B* **280**, 20131016. (doi:10.1098/rspb.2013.1016)

10. Meyer N et al. 2020 Nest attentiveness drives nest predation in arctic sandpipers. *Oikos* **129**, 1481–1492. (doi:10.1111/oik.07311)

11. Meyer N et al. 2021 Behavioural responses of breeding arctic sandpipers to ground-surface temperature and primary productivity. *Sci. Total Environ.* **755**, 142485. (doi:10.1016/j.scitotenv.2020.142485)

12. Cantar RV, Montgomerie RD. 1985 The influence of weather on incubation scheduling of the White-Rumped sandpiper (*Calidris fuscicollis*): a uniparental incubator in a cold environment. *Behaviour* **95**, 261–289. (doi:10.1163/156853985X00154)

13. Smith PA, Tulp I, Schekkerman H, Gilchrist HG, Forbes MR. 2012 Shorebird incubation behaviour and its influence on the risk of nest predation. *Anim. Behav.* **84**, 835–842. (doi:10.1016/j.anbehav.2012.07.004)

14. Tulp I, Schekkerman H, Leeuw J de. 2012 Eggs in the freezer: energetic consequences of nest site and nest design in Arctic breeding shorebirds. *PLoS ONE* **7**, e38041. (doi:10.1371/journal.pone.0038041)

15. Smith PA, Dauncey SA, Gilchrist HG, Forbes MR. 2012 The influence of weather on shorebird incubation. In *Video surveillance of nesting birds* (eds C Ribic, RF Thompson III, PJ Pietz), pp. 89–104. Berkeley, CA: University of California Press.

16. Macdonald EC, Camfield AF, Jankowski JE, Martin K. 2013 Extended incubation recesses by alpine-breeding Horned Larks: A strategy for dealing with inclement weather? *J. Field Ornithol.* **84**, 58–68. (doi:10.1111/jofo.12006)

17. Bueno-Enciso J, Barrientos R, Ferrer ES, Sanz JJ. 2017 Do extended incubation recesses carry fitness costs in two cavity-nesting birds? *J. Field Ornithol.* **88**, 146–155. (doi:10.1111/jofo.12194)

18. Fu Y, Dai B, Wen L, Chen B, Dowell S, Zhang Z. 2017 Unusual incubation behavior and embryonic tolerance of hypothermia in the Sichuan partridge (*Arborophila ruיפectus*). *J. Ornithol.* **158**, 707–715. (doi:10.1007/s10336-016-1422-7)

19. Jia CX, Sun YH, Swenson JE. 2010 Unusual incubation behavior and embryonic tolerance of hypothermia by the Blood Pheasant (*Ithaginis cruentus*). *Auk* **127**, 926–931. (doi:10.1525/auk.2010.09254)

20. Coe BH, Beck ML, Chin SY, Jachowski CMB, Hopkins WA. 2015 Local variation in weather conditions influences incubation behavior and temperature in a passerine bird. *J. Avian Biol.* **46**, 385–394. (doi:10.1111/jav.00581)

21. Martin TE, Auer SK, Bassard RD, Niklison AM, Lloyd P. 2007 Geographic variation in avion incubation periods and parental influences on embryonic temperature. *Evolution* **61**, 2558–2569. (doi:10.1111/j.1558-5646.2007.00204.x)

22. Nord A, Nilsson JÅ. 2011 Incubation temperature affects growth and energy metabolism in blue tit nestlings. *Am. Nat.* **178**, 639–651. (doi:10.1086/662172)

23. Higgott CG, Evans KL, Hatchwell BJ. 2020 Incubation in a temperate passerine: do environmental conditions affect incubation period duration and hatching success? *Front. Ecol. Evol.* **8**, 542179. (doi:10.3389/fevo.2020.542179)

24. Norton DW. 1972 Incubation schedules of four species of calidrine sandpipers at Barrow, Alaska. *Condor* **74**, 164–176. (doi:10.2307/1366280)

25. Klaassen M, Lindström Å, Meltofte H, Piersma T. 2001 Arctic waders are not capital breeders. *Nature* **413**, 794. (doi:10.1038/35101654)

26. Cramp S, Simmons KEL. 1983 *Handbook of the birds of Europe, the Middle East and north Africa, volume III: waders to gulls*. Oxford, UK: Oxford University Press.

27. Reneerkens J et al. 2009 Sanderlings using African-Eurasian flyways: a review of current knowledge. *Wader Study Group Bulletin* **116**, 2–20.

28. Wirta HK, Vesterinen EJ, Hambäck PA, Weingartner E, Rasmussen C, Reneerkens J, Schmidt NM, Gilg O, Roslin T. 2015 Exposing the structure of an Arctic food web. *Ecol. Evol.* **5**, 3842–3856. (doi:10.1002/ece3.1647)

29. Høye TT, Forchhammer MC. 2008 Phenology of high-Arctic arthropods: effects of climate on spatial, seasonal, and inter-annual variation. *Adv. Ecol. Res.* **40**, 299–324. (doi:10.1016/S0065-2504(07)00013-X)

30. Saalfeld ST et al. 2019 Phenological mismatch in Arctic-breeding shorebirds: Impact of snowmelt and unpredictable weather conditions on food availability and chick growth. *Ecol. Evol.* **9**, 6693–6707. (doi:10.1002/ece3.5248)

31. Reneerkens J, Grond K, Schekkerman H, Tulp I, Piersma T. 2011 Do uniparental Sanderlings *Calidris*
*alba* increase egg heat input to compensate for low nest attentiveness? *PLoS ONE* **6**, e16834. (doi:10.1371/journal.pone.0016834)

32. Reneerkens J, Van Veelen P, Van Der Velde M, Luttikhuizen P, Piersma T. 2014 Within-population variation in mating system and parental care patterns in the Sanderling (*Calidris alba*) in northeast Greenland. *Auk: Ornithol. Adv.* **131**, 235–247. (doi:10.1642/AUK-13-247.1)

33. Tomkovich PS, Soloviev MY. 2001 Social organization of Sanderlings breeding at northern Taimyr, Siberia. *Ornithologia* **29**, 125–136.

34. Cappelen J, Jørgensen BV, Laursen EV, Stannius LS, Thomsen RS. 2001 *The observed climate of Greenland, 1958–99: with climatological standard normals*. Copenhagen, Denmark: Danish Meteorological Institute.

35. Walker DA et al. 2005 The Circumpolar Arctic vegetation map. *J. Veg. Sci.* **16**, 267–282. (doi:10.1111/j.1654-1103.2005.tb02365.x)

36. Humphreys RK, Ruxton GD. 2020 Avian distraction displays: a review. *Ibis* **162**, 1125–1145. (doi:10.1111/ibi.12814)

37. Parmelee DF, Payne RB. 1973 On multiple broods and the breeding strategy of arctic Sanderlings. *Ibis* **115**, 218–226. (doi:10.1111/j.1474-919X.1973.tb02638.x)

38. Mabee TJ, Wildman AM, Johnson CB. 2006 Using egg flotation and eggshell evidence to determine age and fate of Arctic shorebird nests. *J. Field Ornithol.* **77**, 163–172. (doi:10.1111/j.1557-9263.2006.00037.x)

39. Moreau J, Perroud L, Bollache L, Yannic G, Teixeira M, Schmidt NM, Reneerkens J, Gilg O. 2018 Discriminating uniparental and biparental breeding strategies by monitoring nest temperature. *Ibis* **160**, 13–22. (doi:10.1111/ibi.12507)

40. Bolduc E et al. 2013 Terrestrial arthropod abundance and phenology in the Canadian Arctic: Modelling resource availability for Arctic-nesting insectivorous birds. *Can. Entomol.* **145**, 155–170. (doi:10.4039/tce.2013.4)

41. McKinnon L, Picotin M, Bolduc E, Juillet C, Bêty J. 2012 Timing of breeding, peak food availability, and effects of mismatch on chick growth in birds nesting in the High Arctic. *Can. J. Zool.* **90**, 961–971. (doi:10.1139/z2012-064)

42. Wang JM, Beissinger SR. 2009 Variation in the onset of incubation and its influence on avian hatching success and asynchrony. *Anim. Behav.* **78**, 601–613. (doi:10.1016/j.anbehav.2009.05.022)

43. Bulla M et al. 2016 Unexpected diversity in socially synchronized rhythms of shorebirds. *Nature* **540**, 109–113. (doi:10.1038/nature20563)

44. Ameijeiras-Alonso J, Crujeiras RM, Rodríguez-Casal A. 2018 Multimode: an R package for mode assessment. *arXiv preprint arXiv:1803.00472*. (doi:10.18637/jss.v097.i09)

45. Cumming G, Finch S. 2005 Inference by eye: confidence intervals and how to read pictures of data. *Am. Psychol.* **60**, 170–180. (doi:10.1037/0003-066X.60.2.170)

46. Cumming G. 2007 Inference by eye: pictures of confidence intervals and thinking about levels of confidence. *Teaching Statistics* **29**, 89–93. (doi:10.1111/j.1467-9639.2007.00267.x)

47. Peig J, Green AJ. 2009 New perspectives for estimating body condition from mass/length data: The scaled mass index as an alternative method. *Oikos* **118**, 1883–1891. (doi:10.1111/j.1600-0706.2009.17643.x)

48. Burnham KP, Anderson DR. 2002 *Model selection and multimodel inference: a practical information-theoretic approach*. Berlin, Germany: Springer Berlin.

49. Long JA. 2022 *jtools: Analysis and presentation of social scientific data*. R package version 2.2.0.

50. Esarey J, Sumner JL. 2018 Marginal effects in interaction models: determining and controlling the false positive rate. *Comparative Political Studies* **51**, 1144–1176. (doi:10.1177/0010414017730080)

51. R Core Team. 2018 *R: a language and environment for statistical computing*. Vienna, Austria: R Foundation for Statistical Computing.

52. Bates D, Maechler M, Bolker B, Walker S. 2014 *lme4: Linear mixed-effects models using Eigen and S4*. R package version 1.1-7.

53. Kuznetsova A, Brockhoff PB, Christensen RHB. 2017 *lmerTest Package: tests in linear mixed effects models*. *J. Stat. Softw.* **82**, 1–26. (doi:10.18637/jss.v082.i13)

54. Nakagawa S, Schielzeth H. 2013 A general and simple method for obtaining R² from generalized linear mixed-effects models. *Methods Ecol. Evol.* **4**, 133–142. (doi:10.1111/j.2041-210x.2012.00261.x)

55. Danks HV. 2004 Seasonal adaptations in Arctic insects. *Integr. Comp. Biol.* **44**, 85–94. (doi:10.1093/icb/44.2.85)

56. Aldrich TW, Raveling DG. 1983 Effects of experience and body weight on incubation behavior of Canada Geese. *Auk* **100**, 670–679. (doi:10.1093/auk/100.3.670)

57. Grimaudo AT, Hope SF, DuRant SE, Kennamer RA, Hallagan JJ, Hopkins WA. 2020 Ambient temperature and female body condition are related to night incubation behavior in Wood Ducks *Aix sponsa*. *J. Avian Biol.* **51**, 5. (doi:10.1111/jav.02379)

58. Chaurand T, Weimerskirch H. 1994 Incubation routine, body mass regulation and egg neglect in the Blue Petrel *Halobaena caerulea*. *Ibis* **136**, 285–290. (doi:10.1111/j.1474-919X.1994.tb01097.x)

59. Diez-Méndez D, Cooper CB, Sanz JJ, Verdejo J, Barba E. 2021 Deconstructing incubation behaviour in response to ambient temperature over different timescales. *J. Avian Biol.* **52**, 1–16. (doi:10.1111/jav.02781)

60. Etchart L. 2023 Data from: Extended incubation recesses in Sanderlings are impacted by temperature and body condition [Dataset]. Dryad Digital Repository. (doi:10.5061/dryad.v41ns1s3q)

61. Etchart L et al. 2024 Extended incubation recesses in sanderlings are impacted by temperature and body condition. Figshare. (doi:10.6084/m9.fishshare.c.7068214)