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Egg‑laying increases body
temperature to an annual
maximum in a wild bird
Magella Guillemette1,2* & David Pelletier1,2
Most birds, unlike reptiles, lay eggs successively to form a full clutch. During egg‑laying, birds are
highly secretive and prone to disturbance and predation. Using multisensor data loggers, we show
that average daily body temperature during egg‑laying is signicantly increased (1 °C) in wild eider
ducks (Somateria mollissima). Strikingly, this increase corresponds to the annual maximum body
temperature (40.7 °C), representing a severe annual thermogenic challenge. This egg‑laying‑induced
rise in body temperature may prove to be a common feature of wild birds and could be caused by
habitat‑related thermoregulatory adjustments and hormonal modulation of reproduction. We
conclude our ndings with new perspectives of the benets of high body temperature associated with
egg‑laying of birds and the potential eect of heat stress that may occur with the future advent of
heatwaves.
Laying eggs is a sensitive period for any bird species, as the female produces eggs over a few days to produce
a full clutch. During this period, females must ingest sucient amounts of food and nutrients to full the
energetic demand of egg production1–3, while various hormones dictate follicular growth and the occurrence
of ovulation4–6, together with the necessity for any new egg to be fertilised by males during courtship activities.
Studies on the phenology of reproduction and laying dates of birds are becoming one of the hallmarks of bio-
logical research to understand the eects of climate change on bird populations7–10. However, the physiological
mechanism by which ambient temperature inuences the phenology of egg-laying in birds is still unknown11.
e thermal physiology of egg-laying in birds has chiey been described in species raised for farm production,
and there is no information on wild birds. In chickens, quails and turkeys, it is known that laying eggs (oviposi-
tion) and ovulation are tightly synchronised and associated with a transient peak in body temperature12–15. On
the other hand, studies of wild birds have largely been devoted to the estimation of the overall energetic cost of
producing a full clutch. e few that have measured metabolic rate of laying birds, using respirometry, have found
a slight increase (20–30%) of resting metabolic rate16–18. Such an increase in metabolic rate is likely accompanied
by an increase in body temperature during egg-laying.
e physiology of wild birds while laying eggs is notoriously dicult to study as they tend to stop laying
during or aer the experimental measurements16–18, while various species will desert their nest if handled or
disturbed during this period19. Here we present unprecedented data for a wild bird, a large sea duck (Somateria
m. mollissima) coming ashore to breed every spring to lay 3–6 eggs successively to form a full clutch. We cir-
cumvented the methodological hurdle by using year-round monitoring of heart rate (HR) and body temperature
(Tb) using data-loggers implanted in the body cavity of 12 breeding females for one year and removed them a
year later during subsequent incubation (aer laying). ese measurements were complemented with data from
nest temperature thermistors and regular visual monitoring of activity during the laying process at the breed-
ing colony. We show that egg-laying is associated with a substantial increase in average daily body temperature,
which corresponds to an annual maximum. Laying eggs in a wild bird maximises body temperature and might
be a common physiological avian feature. We therefore postulated the proximate causes of the observed rise in
Tb to be related to thermoregulatory adjustments and hormonal modulation in this species and oer a novel
hypothesis stipulating why such a phenomenon would occur from an evolutionary perspective.
Materials and methods. Study Site, Model Species and denitions. is study was performed on Chris-
tiansø Island (55°19’N, 15°12’E), an old Danish fortress located in the southern Baltic Sea, 18km from the Dan-
ish island of Bornholm. About 120 people live on the island along with a colony of about 2600 breeding pairs of
OPEN
1Département de Biologie, Université du Québec à Rimouski, 300, Allée des Ursulines, Rimouski, QC G5L 3A1,
Canada. 2Département de Biologie, Cégep de Rimouski, 60, Rue de L’Évêché Ouest, Rimouski, QC G5L 4H6,
Canada. *email: magella_guillemette@uqar.ca
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Common Eiders20. One of the reasons we chose this colony is that habituation of the birds to human presence
has developed over the years, facilitating monitoring at the colony, handling and re-capturing the experimental
birds. Our study required daily visits to the colony to monitor clutch size and laying phenology, the installa-
tion of temperature thermistors at the nests and the implantation of data loggers into incubating females. We
obtained a license from Dyreforsøgtilsynet (Royal Veterinarian Corporation) in Denmark, where the data log-
gers were deployed. All birds were cared for in accordance with the principles and guidelines of the Canadian
Council on Animal Care (# CPA 16-03-07-01).
Female Common Eiders Somateria mollissima are large sea ducks (1.8–2.8kg) and lose about 35% of their
post-laying body mass by fasting during incubation21. Pre-laying females are hyperphagic22,23and accumulate fat
and protein reserves near the breeding colony and increase their body mass by 32% over winter levels prior to
reproduction24. e daily time spent diving (DTSD) during the pre-laying period averaged 159.6min compared
to an annual average of 91.4 min25. Diving decreased to 70min during laying and became almost negligible at
the onset of incubation.
We dene egg laying as the time interval that spans from laying the rst to the last egg. We also used the term
oviposition as the act of expulsing the egg from the cloaca. Pre-laying and post-laying dene the time interval
from 0 to 10days before and aer the laying period, the former being associated with rapid follicular growth
(see below).
Reproductive success and breeding phenology. We established a study plot of about 0.5ha contain-
ing 80 nests on the island. We visited the study plot every day, between 16h 00 and 17h 00, and 1 April to 31
May from 2003 to 2006 to determine laying dates and incubation periods of females. Our visits did not cause
the incubating females to leave their nests unattended. e rst and second egg is very oen le unattended in
this species21, and the beginning of laying was dened as the day when the rst egg was laid. e total number
of eggs laid was determined at the beginning of the incubation period when the female was caught for weigh-
ing, banding or band reading. e laying period was dened by clutch size, assuming that one egg was laid each
day26. is assumption was veried for some females by putting our hands below the attending female to count
the number of eggs laid.
Capture and data logger implantation. We surgically implanted data loggers (DLs) in the body cav-
ity of experimental females (see27 for details). All nests and breeding females were identied before implanting
the data loggers. In line with previous surgical procedures in this species27, we predicted a recovery period of
2–3days post-implantation to be sucient and chose experimental females for implantation of data loggers past
the 23rd day of their incubation period (incubation time in this population is 26–27days 28). e monitored
females were approached slowly andimmobilisedby putting a black hood over their head, making sure the
females did not leave the nest. en, we removed the experimental females from their nest for implantation.
All surgical procedures were conducted indoors, 100m from the experimental plot. e 45 DLs were 36mm
long (± SD = 0.5) × 28mm (0.2) wide × 11mm thick (0.3) and weighed 21g (0.3), which is 1.2% of body mass
at implantation29. irty-nine (87%) experimental females returned to the study area 1year later, similar to the
previously reported survival rate in this species30. e last result is most likely related to the fact that implanted
DLs do not alter the aerodynamic and hydrodynamic properties of experimental individuals27. One year aer the
implantation, 36 females were re-captured. Only 12 individuals had data logged for a full year, including infor-
mation about laying behavior and incubation (except for one, for which the logger stopped aer laying the rst
egg). ese twelve data loggers recorded (hydrostatic) pressure and heart rate every 2s and body temperature
every 16s.
Ambient temperature and nest attendance. Within the same breeding colony, unattended nests with
one or two eggs were tted with a temperature-recording device made up of a dummy resin egg with a tempera-
ture sensor embedded on top. is articial egg was placed in the centre of the nests and xed to their base with
two metal pins. ermistors were linked to a data logger (Hobo Four-channel External) through a one-meter
wire (Onset Computer Corporation, Pocasset, Massachusetts). Loggers were kept in a waterproof casing and
buried in the ground to avoid detection by the birds. We programmed loggers to register nest and ambient tem-
peratures every 3min. irteen nest loggers were deployed at the colony in 2004–2006 and recorded data until
eggs hatched, aer which we removed the device from the nest. From temperature patterns, we extracted the
presence at the nest and recess periods of females according to the method described by Sabourin31. Recesses
lasted from the rst time the temperature dropped to the rst time the temperature rose. e presence of females
at the nest was identied by a decrease or an increase of at least 2°C within 3min.We only accounted for recesses
longer than 6min because (1) we considered shorter interruptions were likely representative of on-nest move-
ments and (2) due to the limitation of the sampling frequency. Experimental disturbances of incubating eiders
have shown this time interval to be long sucient to properly record recesses31. Moreover, lab experiments with
natural nests, aiming at testing the eect of down cover on ambient temperature, describe drops in Tb from
38°C to 20°C. ese experiments also showed that comparison of nests with and without down result in a dif-
ference in the cooling rate of only 0.4°C over 6min (0.07°C/min)31. e ambient thermistor was located about
1m away from the nest and synchronised with the nest thermistor data. We thus computed the ambient air
temperature when the female was on and o its nest to detect if the female had any preference for air temperature
when leaving its nest. Sea surface temperature (SST) data were obtained for our location for spatial squares of
50 × 50km from the SST50 database of the NOAA (https:// www. avl. class. noaa. gov/ gloss ary/ SST50. htm). e
SST50 is dened as the daily mean sea surface temperature in degrees Celsius at 1m depth.
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Nest attendance was quantied as the sum of the time spent at the nest for each female using the nest thermis-
tor data. However, egg dumping and nest parasitism are common in eiders (reviewed by Waltho and Coulson32),
which could bias our estimate of nest attendance during the laying period. In addition, only 2 implanted females
(out of 12) were associated with nest thermistors (out of 13). We thus used a second method (called the behav-
ioural method) based on body temperature variation and diving patterns to quantify the time at the nest for the
12 implanted females. Female eiders spend a considerable time foraging before and at the beginning of laying25.
Body temperature rose, and variation decreased upon arrival at the colony, approximatively at the same time as
diving behaviour ceased (see Fig. S1). We used this information to determine the time spent at the nest and time
spent on the water. More specically, for each day and female, we simply subtracted the time spent feeding plus
the time spent “resting” between two feeding bouts from 1440min (24h) to estimate the time spent at the nest.
Resting bouts, that occur between feeding bouts, are considered an obligatory component of foraging in this
species as they digest food while swimming and preening on the water33. From visual observations, resting bouts
following feeding bouts lasted on average 14.9 ± (SD) 14.2min (range 3.3–64.7min, n = 52). When resting bouts
were longer than one hour between feeding bouts, these events were considered to be spent at the colony. For
two nests, we matched data from temperature thermistors with those of the implanted loggers (Fig S1). Results
of the two (thermistor and behavioural) methods were highly correlated (R2 = 0.881) with a slope of 1.2, for the
two implanted females associated with nest thermistors.
Data analysis and statistics. First, we quantied thermogenesis during egg-laying by calculating daily
body temperature (Tbdaily) for each day of laying as the average of all Tb data (5400 per day) of each individual. A
similar approach was used for heart rate with the dierence that resting heart rate (RHR) was used as a proxy for
resting metabolic rate and computed from a 5min running average for which the minimum value was extracted
for that day and specic bird29. ese quantities were then compared with RHR during pre and post laying,
dened respectively as ve days before laying the rst egg and ve days aer laying the last egg. We used ve-day
periods since the most common clutch size was composed of ve eggs, representing 5days of laying. Once aver-
aged over ve-day periods for each bird, the laying period was compared to the pre and post laying periods at the
intra-individual level in a before-aer fashion using subtraction, giving two deltas per individual. ese deltas
were averaged across the 12 females, for which condence intervals (CI) were computed using the bootstrap
method. When the (95%) CI of the average delta was excluding zero, the comparison was declared signicant.
Condence intervals (CI) of means and deltas were performed using R version 4.0.3 (R Core Team, 2020)
with boot package34. CIs were calculated from 10 000 nonparametric bootstrap replicates. e 95% bias-corrected
and accelerated method (BCa) intervals are reported. e BCaintervals are the most recommended of the main
types of bootstrap condence intervals35. Because many of the CI resulting from the bootstrap method were
asymmetric, we reported lower and upper values for each average value.
Results
Tb and egg‑laying. Daily body temperature (Tbdaily) of laying female eiders varied, on average, by 1°C for
the twelve females during a 25day period, covering rapid follicular growth (= pre-laying), laying and post-laying
(= beginning of incubation). Tbdaily was 39.9°C, ten days before the rst egg was laid, peaked at 40.9°C while
laying the h egg and decreased to 40.3°C ten days aer the last egg was laid (post-laying period, Fig.1a).
Comparing the laying period to the ve days before (Pre-Lay I) and to the ve days aer laying (Post-Lay I) in a
before-aer approach (Fig.1c), Tbdaily is signicantly higher during laying compared to the pre-laying1 (average
delta = 0.53 (CI: 0.43 & 0.63) °C) and post-laying periods (average delta = 0.12 (CI: 0.05 & 0.20) °C).
HR and egg‑laying. Like Tbdaily, resting heart rate (RHR) steeply increased during the pre-laying period
and peaked once the third egg was laid (Fig.1b). A major dierence is that RHR fell precipitously aer the fourth
egg was laid and while Tbdaily was still rising. is fall in RHR continued for the two rst days post-laying, only
to increase again and to reach a plateau at about 105bpm between days 6 and 10. As a result, when average
values are used over 25days there is no correlation between mean RHR and mean Tbdaily (Pearson’s r = 0.117,
n = 25, p > 0.05). is result holds true when an intra-individual correlation is calculated for each female sepa-
rately and then averaged over the 12 females (average rpearson = 0.030 ± (SD) 0.030, n = 12, p > 0.05). When laying
(116.2bpm) is compared to the Pre-Lay I period (115.9bpm) and Post-Lay I (89.6bpm) periods in a before-aer
approach (Fig.1d), RHR is not signicantly higher than Pre-Lay I (average delta = 0.3 (CI −9.6 & 9.9) bpm)
whereas the Post-Lay I period is signicantly lower (average delta = 28.1 (CI: 13.5 & 38.4) bpm).
Proximate causes of Tb variations. ere are two possible causes for the observed Tbdaily variations.
e rst potential cause is the passage from an aquatic environment to a terrestrial one. Fig. S2a summarises
the ambient temperature a female eider experiences when moving from water (4.67°C) to land (6.21°C). We
know from the work by Jenssen etal.36 that the lower critical temperature (LCT) of this species is higher in
water at 15°C (LCTwater) than in air at 0°C (LCTair). Using the equations provided by Jenssen etal. predicting
resting metabolic rate for these two habitats, we conclude that a laying female (2.64kg) spends 1147kJ day−1 in
the water compared to 839kJ day−1 on land, representing a relative dierence of 28% in thermogenic require-
ments. is estimate is corroborated by our measurements of RHR while laying eggs, being on average 145.8
(CI 131.7–161.1) bpm in the water and 117.5 (CI 104.8–126.8) bpm in air, yielding an average and signicant
dierence of − 28.3 (CI − 38.3 & − 19.4) bpm, or 19%. ese observations and calculations led us to conclude
that the passage from water to land to lay eggs was associated with energy savings, allowing an up-regulation of
Tb (see “Discussion”). is, in turn, could explain the increase of Tb while laying eggs, as the time spent on land
incubating increases with the laying sequence (Fig. S2b).
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Figure1. Daily variation of average (24h) body temperature (a) and heart rate (b) in relation to the laying
sequence of 12 female Common Eiders. e time series shown starts 10days before (rapid follicular growth)
laying of the rst egg and ends 10days aer (rst third of incubation) laying the last (5th) egg. Each biological
stage is shown in a dierent color and subdivided further on a ve-day basis (pre-lay I and II, post-lay I and II),
where the average dierence between biological stages (triangle) is shown for each period (c and d). When the
bootstrap condence intervals of the average dierence exclude zero, we concluded that a signicant dierence
(5% level) exists between the two time periods. Panels e) and f) show body temperature and resting heart rate
variation relative to the female’s presence on land and water, respectively (see Methods). When exclusively on
water, body temperature (spearman rs = 0.967) and RHR (rs = 0.767) are positively related (p < 0.05) to days in the
laying sequence. In contrast, when exclusively on land, body temperature (rs =− 0.770) and RHR (rs = − 0.781) are
negatively related (p < 0.05) to days in the laying sequence.
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However, this mechanism cannot explain all the variation observed in daily Tb during laying. Female eiders
spend 95% of their time on land when laying the h egg, which increases to a constant value of about 99% aer
the 5days of incubation. us, from the end of the laying period to about ten days of incubation, Tbdaily drops
by 0.6°C, indicating that another factor contributes to Tb variation while laying eggs (Fig.1a). During the lay-
ing period, females are moving back and forth between terrestrial and aquatic environments. Quantifying Tb
separately while on land vs Tb while on water for the twelve instrumented females (see Methods and Fig. S1), we
show that when individuals were solely on water, body temperature increases signicantly (spearman rs = 0.967,
p < 0.05) from day -5 of the pre-laying period to the end of the laying period by about 0.5°C (Fig.1e). A similar
observation was made for females exclusively on land, where body temperature decreases signicantly (spear-
man rs = − 0.770, p < 0.05) by 0.6°C (Fig.1e) from the end of laying to the h day of post-laying. erefore, our
method conrms that another factor is causing the observed increase in Tb while laying eggs.
Based on various studies conducted on domestic fowl (see “Discussion”), we hypothesised that a part of the
body temperature variation observed during the laying period is due to the ovulation or the very process of
ejecting an egg (= oviposition). Ovulation is associated with a transient increase of Tb in domestic fowl occur-
ring 30–90min aer oviposition. One feature of this system is that ovulation occurs a little bit later every day. In
this study, we measured the timing of Tb peak during egg-laying of the twelve females and found that it ranged
from 41.3 to 41.6°C (Fig.S2c), lasting between 18 and 30min. Moreover, peaks in Tb happened signicantly
later during the laying sequence, although the dierence is not signicant at the end of this process (Fig. S2c).
One additional strength of our study is that we can compare the observed body temperature during laying
with the full annual cycle (Fig.2) to gauge the magnitude of this phenomenon. Using a ve-day running aver-
age of Tbdaily, for each individual, the average annual maximum Tbdaily is 40.70°C (CI: 0.24), which is 0.13°C
(CI: 0.07) higher than the standard average computed for the laying period. However, this annual maximum
running average occurred during egg-laying in 8 females out of the 12, underlining that the egg-laying period
contributes largely to the annual maximum observed.
Discussion
Fiy years ago, the process of laying eggs and ovulation had been associated with an increase in body tempera-
ture in domestic fowl12,13,15,37–40;. In contrast, data on the thermophysiology of egg-laying in wild birds is entirely
lacking. Given that birds are highly secretive, easily disturbed and prone to predation while laying eggs, it may
explain the absence of data for wild birds. is is especially true if we consider that a rise in body temperature
(Tb) aer ovulation and during the luteal phase occurs in various species of domestic (reviewed by41) and wild
(marsupials:42,43; chimpanzees44–46:) mammals, including humans (see47 for review). In the present study, we
report data for heart rate and Tb before, during and aer egg-laying of undisturbed wild birds. Not only do we
show that egg-laying induces a rise in daily body temperature similar to other vertebrate species, but we also
nd that daily Tb (Tbdaily) corresponds to an annual maximum, representing an annual thermogenic challenge
for these birds. Here we propose that habitat-related thermoregulatory adjustments and hormonal modulation
of reproductive activities cause the observed peak of thermogenesis during laying and then discuss the implica-
tions of our ndings.
The energetic cost of egg‑laying. Resting metabolism increases during reproduction in various verte-
brates, including placental and marsupial mammals, reptiles and birds48,49. In this paper, we have shown that
resting heart rate (RHR), oen used as a proxy for resting metabolic rate50,51, increases steadily during the pre-
laying and laying period in eiders (until the fourth egg is laid), in concert with Tbdaily. We interpret such an
increase in RHR due to the growth of new tissues, such as the oviduct and ovary, which add to the laying hen’s
metabolic activity (productive costs). Birds are known to build up reproductive organs rapidly, and from pre-
laying eiders dissected at various stages22,52,53, it was estimated that the ovary and oviduct increases by a factor of
5 in two weeks, increasing whole body mass by 7%. In addition, it has been estimated that eiders require about
6days to fully develop a follicle3, a period called rapid follicular growth (RFG), and about ten days to produce a
clutch of ve eggs. e observation that RHR fell precipitously aer the fourth egg was laid supports the notion
of an increased energetic cost during the growth of the oviduct and preovulatory follicles, while RFG should
be completed at this stage (Fig.2b). However, there is a competing interpretation for the reduction in RHR
towards the end of egg-laying; it may be caused by the increased time spent on land and the associated reduc-
tion in thermoregulatory costs (see below). Clearly, the isolation of the key mechanism behind the energetics of
egg-laying in wild, laying birds is highly complex (even in an experimental setting, see16,18). ere is a diverse
array of factors that may inuence resting metabolism, such as the thermogenic eects of hormones, body mass
uctuations while laying28, behavioural and physiological compensation54 and, for aquatic birds, habitat-related
variation in thermoregulatory costs36. Only an experimental approach and a detailed quantication of all these
variables would lead to a full understanding of energy allocation during egg-laying in birds, which is outside of
the scope of this paper.
Coming ashore to lay eggs: thermoregulatory adjustments. During the breeding season, any
marine bird species has to move from an aquatic to a terrestrial environment where heat conduction in the air
is reduced by a factor of 20–24 compared to water. us, moving temporarily from an aquatic medium to a ter-
restrial one requires thermoregulatory adjustments. We observed that Tb in laying female eider ducks is 0.6°C
higher on land than when on water. is rise in Tb is similar to former studies monitoring Tb of birds while
moving from the water to land55–59 (but see60), but also of semi-aquatic mammals like muskrats61, beavers62 and
seals57. We also observed that RHR decreased by 19% during laying when moving from water to land. Because
RHR in female eiders falls when leaving water at the same time as Tb rises, we conclude that female eiders are
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saving energy due to the conductive/insulative advantages, allowing the regulation of Tb to a higher level. How-
ever, once the last egg is laid and most of the time (95%) is spent on land, Tbdaily drops by 0.5°C, indicating that,
in addition to the habitat shi described above, another factor is playing a vital role in the observed Tb variation.
Hormonal modulation of egg‑laying: eect of progesterone? We consider the hormonal cascade
associated with reproduction a key factor causing the observed rise in Tb of female eiders. It has been shown
experimentally in humans63 and domestic mammals41 that a rise in Tb is caused by a progesterone surge during
the luteal phase aer ovulation, although such evidence is lacking in birds14. Ovulation in birds, as in mammals,
is hormonally controlled by the hypothalamus–pituitary–gonadal axis (reviewed by64,65). e preovulatory surge
of progesterone (PG) and luteinising hormone (LH) occurs 4–6h before ovulation with a positive feedback
mechanism in domestic birds6,66,67, whereas the secretion of PG and LH seems to occur coincidently in wild
ducks68,69. At the time scale of a full clutch, the progesterone level of wild mallards in captivity, canvasbacks68,69
and canaries70 is much higher during laying when compared to the pre and post-laying periods. A similar obser-
vation was made for domestic hens in which progesterone decreased markedly during laying pauses71,72. Because
progesterone is associated with thermogenic eects73,74, we hypothesise PG to be partly responsible (together
with the habitat-related shi described above) for the high Tbdaily observed during laying. However, prostaglan-
Figure2. Average daily body temperature (Tbdaily) and resting heart rate (RHR) during pre-laying (blue,
n = 12), laying (yellow, n = 12) and incubation (red, n = 11) of female Common Eiders compared to the annual
average (pale grey, n = 12) and the annual maximum running average (dark grey, n = 12). When the bootstrap
condence intervals (95%) of the average dierence (triangles) between two adjacent variables exclude zero,
it was concluded that a signicant dierence exists between the two variables compared. Note that the ve-
day annual maximum running average of Tbdaily occurred during laying in 8 females out of 12, whereas none
occurred during laying for RHR.
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din (PGF2 and PGE2), another hormone that causes a thermogenic eect75,76, can be produced in various tissues,
including preovulatory follicles. Prostaglandins are responsible for egg movement under oviduct contractions
and oviposition (ejection) of the new egg in domestic fowl77–79. In addition, thyroid hormones (THs) are also
known to vary between reproductive and non-reproductive states of birds and is also associated with thermo-
genic eects80–82. For example, it has been hypothesised that triiodothyronine (T3) secretion triggers photosen-
sitivity by increasing in the medial basal hypothalamus (MBH) under long photoperiods and interacting with
gonadotropin-releasing hormone (GnRH) production81. However, such a hypothesised eect would occur a
long time before egg-laying. Another eect of THs is that it would trigger photorefractoriness under the inu-
ence of long days, thus putting an end to reproduction64,80. Gabrielsen etal.83 have measured the level of T3 in
breeding Common Eiders, which show a low level of T3 during the laying and pre-laying state, which increases
regularly then during the incubation period. is suggests that T3 is unlikely to be the hormone that triggers a
rise in body temperature while laying eggs in this species, although further examinations are warranted.
In support of the hormonal modulation hypothesis of Tb, we observed a transient peak of Tb in female
eiders, when on land and while laying eggs (Fig S1d, Fig S2 cd), as observed for chickens12,13,39 turkeys14 and
quails15, lasting 22min on average. One peculiar aspect of the hormonal control of egg-laying is its circadian
dependency, where a subsequent LH surge must occur slightly later than 24h aer the previous surge (the open
window model, see6). Given that ovulation occurs 15–90min aer oviposition and both processes are tightly
synchronized5, oviposition commences a little bit later every day, as exemplied in hens12,13,40. In the present
study, we observed a daily peak of Tb occurring later every day for eggs 1 to 3, but not for the 4th and 5th egg.
Based on the high frequency of nest monitoring for female eiders breeding in northern Canada, Watson and col-
leagues similarly reported that eggs were increasingly delayed during the laying sequence with an average laying
interval of 28 h26. Altogether, these results support the open window model of egg-laying in common eiders and
suggest that the rise of Tb associated with egg-laying in female eiders to be partly hormonal. However, the peak
of Tb caused by prostaglandin around oviposition in domestic fowl is transient and would not explain the full
magnitude of Tb elevation observed in laying eider ducks. We thus speculate that although both progesterone
and prostaglandin can inuence Tbdaily in female eiders, the eect is predominantly caused by progesterone,
given the prevalence of its secretion while laying eggs in wild ducks68,69 and canaries70.
Hyperthermia or fever? A rise in metabolic activity has been widely observed throughout the vertebrate
lineage, including placental mammals, marsupials as well as ectotherms like lizards and turtles48,49. Not only do
some of these vertebrates increase their metabolic rate during reproductive periods, but Tb and thermoregula-
tion are also altered. Based on these observations, the parental care model of endothermy has been proposed48,49,
suggesting that the high level of metabolic activity associated with breeding in various species of vertebrates
was the main incentive for the evolution of a high and stable body temperature. For instance, high incubation
temperature accelerates embryonic growth and decreases the duration of incubation in birds84–86. e main fac-
tors that assure a high incubation temperature for the embryo are nest attentiveness and a high Tb87. However,
evidence for the latter is rare88. Here we show that Tbdaily at the beginning of incubation in common eiders was
0.5°C higher than the annual average. Although such a dierence may seem small, recent evidence84–86 has
shown that dierences in incubation temperature of this magnitude can aect various aspects of the phenotypic
quality of chicks (locomotor performance, acquired immune responses, thermoregulation abilities, etc.). is is
particularly important in incubating female eider ducks that display one of the highest levels of nest attendance
during incubation amongst birds (95–99%21), leaving variation of Tb as the second most important modulator
of incubation temperature.
However, the above interpretation does not resolve the observation of an even higher level of Tbdaily during
egg-laying in this study. Although a rise in body temperature during ovulation has been described in various
vertebrates, we are not aware of any hypothesis explaining this phenomenon from an evolutionary perspective.
Here we propose that the observed rise in body temperature during egg-laying of female eiders may be analogous
to an infection-induced fever, an up-regulation of Tb as a consequence of a change to the thermoregulatory
set-point. Infection-induced fever is a cardinal response to pathogens that has been preserved in endotherms
and ectotherms over millions of years of evolution (including humans89 and birds76). We, therefore, hypothesise
that the increased thermogenesis during egg-laying in eiders is an anticipatory response governed by the need
to boost the immune system during the fertilisation process. e reproductive tract of birds (oviduct) is prone
to infection even if the oviduct and rectum are separated; they both protrude to the outer orice, the cloaca.
Most male and female birds achieve copulation by the bondage of their cloaca, also known as "cloacal kisses". It
has been shown in several studies that the cloaca of females and males contains a large diversity of bacteria90–92,
while manipulative experiments have shown that males transmit bacteria to females during copulation91 and
that infected females may transmit pathogens to their eggs93. Pathogens transmitted through copulation may
impair the survival of the future zygote, and the increased likelihood of sexual disease transmission can alter
the host’s survival91. erefore, a high body temperature during ovulation and the formation of the egg would
boost the innate immune system in a manner as described by Evans and colleagues89 and reduce the likelihood
of any infectious agents surviving within the oviduct.
Implications: heatwaves, egg quality and laying dates. e impact of environmental temperature
on endotherms is oen envisioned through the concept of critical thermal limits (CTL), being the lethal Tb
boundaries within which an individual is likely to survive94. However, at the population level, lower thermal
limits have to be considered, as reproduction (and other functions) might be compromised under heat stress
before an individual’s survival is jeopardised94,95. is is especially true when "natural" thermal boundaries of
the annual cycle and reproduction coincide, as shown in female Common eiders in this study. For example,
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average peak Tb while laying eggs (ranging from 41.3 to 41.6°C for about 20min, Fig.S2) compared with
intense locomotion during migratory ights (approximately 41.5°C on average for ights > 80 min96), in the
same individuals as in this study, is similar. However, migrating eiders limited the development of ying-induced
hyperthermia by landing on the water surface regularly to cool down96. At the scale of a whole day, the average
Tbdaily during laying ranged from 40.4 to 40.9°C (Fig.2), whereas the average Tbdaily during migration days was
40.4°C. In this context, egg-laying may represent a sensitive period relative to ambient temperature uctuations
that may occur naturally.
Apart from increases in average temperatures, one central prediction of climate change models is that it will
also increase temperature variability in the form of heatwaves, which are predicted to increase in frequency and
duration in the future97. Studies investigating the phenology of egg-laying in birds has attracted considerable
attention and are becoming one of the hallmark eects of climate change on animal populations overall. Despite
correlative evidence showing a negative relationship between ambient temperature and laying dates7,9, there are
only limited experimental studies showing that spring temperatures aect the timing of laying directly8,10. Inter-
estingly, in the sole study, we are aware of that measured the eect of changes in ambient temperature on laying
in wild birds, Schou etal.98 identied a critical thermal window in captive ostrich (Struthio camelus), for which
the rate of egg-laying peaked at 20°C, dropping by 15% and 18% when temperatures increased and decreased
by 5°C, respectively. However, it is unknown which mechanisms contributed to these results.
Here, we suggest that the inverse relationship between laying dates of birds and ambient temperature7,9 is an
avoidance strategy preventing additional heat loads while producing eggs. As ambient temperature increases
under the eect of global warming, birds would show a tendency to lay earlier. However, such a hypothesis
alone would not explain the observation that birds lay eggs later at colder ambient temperatures. In that regard,
Stevensen and Bryant99 have proposed the possibility that ambient temperature may act as a constraint with
colder ambient temperature forcing laying birds to allocate more energy to thermoregulation, thereby reducing
any available energy to reproduction. Nevertheless, these ndings support the notion of fertility thermal limits,
where reproduction and the process of egg-laying might be aected at an ambient temperature much below those
identied as critical thermal limits for survival.
Conclusions
In conclusion, this is the rst study demonstrating that egg-laying in a free-ranging wild bird is associated with
a substantial increase in Tb. Based on the laboratory model of domestic fowl and the general prevalence of
metabolic increases during reproduction in various vertebrates, we suggest that the rise of Tb while laying eggs
may be a general phenomenon in birds. We speculate that the mechanism triggering the increased thermogen-
esis is a regulated process, comparable to fever, in order to upregulate the immune system. Given the panoply
of recent studies into the temperature-dependent phenology of egg-laying in birds, we believe the study of the
specic physiological eects of ambient temperature on egg-laying birds will be an essential and exciting line of
inquiry for the years to come.
Data availability
All data are available in the main text or the supplementary materials.
Received: 8 June 2021; Accepted: 12 January 2022
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Acknowledgements
is study was done in collaboration with the National Environmental Research Institute of Denmark and was
funded through the Canadian Natural Sciences and Engineering Research Council (NSERC) discovery and
equipment grants to M. Guillemette and NSERC Alexander-Graham-Bell fellowship to D. Pelletier. Special
thanks to Elias Polymeropoulos for his kind oer to review our paper.
Author contributions
Conceptualization: M.G. Methodology: M.G. Investigation: M.G., D.P. Visualization: M.G., D.P. Funding acqui-
sition: M.G., D.P. Project administration: M.G. Supervision: M.G. Writing-original dra: M.G. Writing-review
& editing: M.G., D.P.
Funding
National Science and Engineering Research Council 03947 (MG). Alexander Graham Bell Canada Graduate
Scholarship – Doctoral (CGS D) award (#CGSD3505117-2017) (DP).
Competing interests
e authors declare no competing interests.
Additional information
Supplementary Information e online version contains supplementary material available at https:// doi. org/
10. 1038/ s41598- 022- 05516-0.
Correspondence and requests for materials should be addressed to M.G.
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