Abstract

Climate change is altering the severity and intensity of extreme weather events. Occupying microhabitats that buffer extreme weather may help species avoid harsh environmental conditions. We describe the thermal microclimate of Atlantic Puffin (Fratercula arctica) and Leach’s Storm-petrel (Hydrobates leucorhous) burrows and quantify whether burrows are thermal refuges during extreme cold weather events. We further test for the effect of weather conditions and burrow characteristics on nest microclimate and buffering capacity during extreme cold weather. We find that both species actively breed in burrow microclimates that are below their lower critical temperatures, which may impose significant thermoregulatory costs. However, burrows do act as thermal refuges because nests are kept 7.4–8.0 °C warmer than ambient temperatures during extreme cold weather events. Overall, external temperature and wind speed were strong drivers of burrow temperature, but burrow and habitat characteristics did not explain the variability in burrow buffering capacity during extreme cold weather. Our results suggest that burrows may provide a direct line of defence for seabird chicks against cold events. Given the complex responses of burrow microclimates to extreme events, quantifying how changes in environmental conditions will impact burrow-nesting seabirds in the future is key.

Introduction

The frequency and intensity of extreme weather events, such as heat-waves, cold extremes, storms, and floods, are increasing with climate change (AghaKouchak et al. 2018). These short-term perturbations have strong direct and indirect impacts on marine and terrestrial species (Shoo et al. 2010; Wingfield et al. 2017; Harris et al. 2020). For example, extreme events can cause local species extinctions (Wernberg et al. 2013), pose energetic challenges (Cooper et al. 2019), and decrease breeding success (Martin et al. 2017). It is critical to detect where resilience lies in natural systems and identify which species will need conserving in the future.
Extreme changes in ambient temperature can push species outside of their thermoneutral zone and into constant thermal stress (Khaliq et al. 2014; Murali et al. 2023). The thermoneutral zone represents the range of ambient temperatures between the lower critical temperatures (LCTs) and upper critical temperatures (UCTs) at which an endotherm maintains a stable metabolic rate without regulatory changes in heat production or evaporative heat loss (IUPS 1987). Below the lower critical temperature, a resting thermoregulating animal must increase its rate of metabolic heat production via shivering or nonshivering thermogenesis to maintain thermal balance (IUPS 1987). However, above the UCT the rate of evaporative heat loss or metabolic rate of a resting thermoregulating animal must be increased by panting or sweating to maintain thermal balance (IUPS 1987). Moreover, ambient temperatures will rarely be ideal for both adults and juveniles because juveniles have much higher and narrower thermoneutral zones than adults (Whittow et al. 1987; Mitchell et al. 2018). Subsequently, juveniles are more susceptible to cold and heat stress resulting in significant thermoregulatory costs and consequences for growth (Weathers et al. 2000; Mitchell et al. 2018).
Occupying microhabitats that buffer extreme weather is one behavioural approach that helps many taxa remain within their thermoneutral zone and avoid variable external environmental conditions (Shoo et al. 2010; Pike and Mitchell 2013; Scheffers et al. 2014; de Frenne et al. 2019). Burrows nests can provide a stable thermal microclimate compared to ambient temperatures (Kesler and Haig 2005; Mallory and Forbes 2011; Mersten-Katz et al. 2012; Maziarz and Wesołowski 2013; Kulaszewicz and Jakubas 2018). For example, to address thermal challenges, reptiles facing extreme heat in desert and dune ecosystems (Pike and Mitchell 2013; Moore et al. 2018), and mammals and birds in strongly seasonal environments take refuge in burrows (Nadeau et al. 2015; Milling et al. 2018a). Moreover, such burrows structures can act as thermal refugia against unfavourable conditions by reducing thermoregulatory costs compared to open nests or ambient temperatures (Martin and Li 1992; Durant et al. 2005; Pike and Mitchell 2013; Moore et al. 2018).
The consequences of climate change and severe weather are a serious threat to seabirds because they impact over 170 million individuals worldwide (Dias et al. 2019). Indeed, seabirds face demanding thermal conditions throughout the breeding season and during extreme events that can exceed their UCTs and fall below their LCTs (Moe et al. 2009; Choy et al. 2021). Seabird chicks are particularly vulnerable to extreme weather events because after achieving homeothermy, they typically remain in their nests until fledging. Consequently, chicks are exposed to all adverse weather that occurs during the breeding season regardless of whether they occupy open or burrow nests. For example, thousands of ground-nesting American White Pelican (Pelecanus erythrorhynchos) chicks perished as a result of several extreme events that produced adverse extended cold, wet, and windy weather in North Dakota over a five-year period (Sovada et al. 2014). Colonies of burrowing seabirds are also vulnerable to flooding, cooling, and collapse during extreme weather (Glencross et al. 2021). Yet, similar to other reptile, mammal, and bird burrows, seabird burrow nests can moderate temperatures and provide a stable thermal environment (Manuwal 1974; Kulaszewicz and Jakubas 2018). Despite this thermal protection, chicks have elevated LCTs compared to adults; therefore, burrow temperatures often fall below chick LCTs and incur significant energetic costs (Whittow et al. 1987; Weathers et al. 2000; Moe et al. 2009). Consequently, it is imperative to understand how environmental extremes change seabird nest microclimates, whether burrows provide thermal refuges for chicks and adults, and to monitor the implications if burrow temperatures further deviate outside seabird critical temperatures.
Newfoundland, Canada, hosts globally significant numbers of breeding seabirds (Gaston et al. 2009). In the face of climate change, the area is predicted to experience more storms and extreme cold weather, especially if the Atlantic meridional overturning circulation collapses (Trepanier 2020; He et al. 2022; Ditlevsen and Ditlevsen 2023). Two burrow-nesting species facing the growing threat of such extreme events are the Atlantic Puffin (Fratercula arctica), a ca. 450 g Alcid which is classified as globally Vulnerable by the International Union for Conservation of Nature (IUCN) Red List (BirdLife International 2018a; Lowther et al. 2020), and the Leach’s Storm-petrel (Hydrobates leucorhous), a ca. 45 g Procellariid which is assessed as Vulnerable by the IUCN and threatened by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC 2020; BirdLife International 2018b; Pollet et al. 2021). For example, during the breeding season, extreme cold weather caused a hypothermia-induced mass mortality of Atlantic Puffin chicks in Newfoundland (Wilhelm et al. 2013), while Leach’s Storm-petrels, which breed later than Atlantic Puffins, are regularly exposed to hurricanes and cyclones towards the mid-late breeding season. It is speculated that these extreme events may flood or cool Leach’s Storm-petrel burrows, causing hypothermia or death (Pollet et al. 2023). Yet, there is limited knowledge on the burrow microclimate of both species and whether nests provide a thermal refuge to adults and chicks during extreme cold weather events (Lowther et al. 2020; Pollet et al. 2021). Filling this basic biology knowledge gap can inform on the capacity of burrow systems to buffer temperature change during extreme events for these threatened species. Moreover, Atlantic Puffins and Leach’s Storm-petrels are excellent models to test how different burrow and habitat characteristics improve such resilience because they can nest in close proximity, yet occupy different habitats. In Newfoundland, the Atlantic Puffin predominantly selects nesting sites along steep grass-covered maritime slopes; therefore, burrows have no additional shelter and are exposed to high solar radiation, variable temperatures, and high wind speeds (Lowther et al. 2002). By contrast, Leach’s Storm-petrels nest in a variety of island habitats ranging from open grass meadows to heavily-canopied forests, which may offer additional thermal protection from extreme events (Huntington et al. 1996). Collectively, revealing such patterns could help inform habitat conservation measures that may be needed given increases in extreme events in the future.
Here, we (1) describe the inter- and intra-specific variations in Atlantic Puffin and Leach’s Storm-petrel burrow microclimates, and (2) test for the effect of external weather conditions on internal burrow temperatures. These objectives allow us to (3) quantify the proportion of time that burrows are cold thermal refuges for adults and chicks through the season and during extreme weather events. Finally, we (4) identify the features of burrows with superior buffering capacity during extreme cold events.

Methods

Field methods

Study site

We conducted fieldwork on Gull Island (47°15′35.4″N, 52°46′35.0″W), located within Witless Bay Ecological Reserve off the coast of Newfoundland and Labrador, Canada (Fig. 1a). The ecological reserve supports internationally important numbers of breeding seabirds, including the largest known colony of Atlantic Puffins in North America, and second largest colony of Leach’s Storm-petrels in the world (Robertson et al. 2004). In particular, Gull Island hosts approximately 180 000 breeding pairs of both species (Canadian Wildlife Service 2023).
Fig. 1.
Fig. 1. (a) Locations of the Atlantic Puffin (circles) and Leach’s Storm-petrel (triangles) study plots, and weather stations (stars) on Gull Island, Witless Bay Ecological Reserve, Newfoundland and Labrador, Canada. Dark grey represents forested habitat and light grey characterises grassy slope habitat. (b) Schematic diagram representing a chick in a burrow and positioning of temperature loggers. Mean (±SD) measurements of characteristics across 30 Atlantic Puffin (ATPU) and 30 Leach’s Storm-petrel (LESP) burrows. Examples of (c) Atlantic Puffin burrows on a grassy slope, and (d) a Leach’s Storm-petrel burrows in a forest. Map modified from Collins et al. (2023). Habitat images by Sydney Collins. Bird illustrations by Cerren Richards.
This research was provided full approval by the Memorial University Animal Care Committee (protocol number: 20200476). To undertake fieldwork on Gull Island within the Witless Bay Ecological Reserve in 2021, we received a Wilderness and Ecological Reserves Scientific Research Permit from the Government of Newfoundland and Labrador.

Internal burrow temperature

To record the temperature within Atlantic Puffin and Leach’s Storm-petrel burrows, 30 burrows with an egg and adult present were selected for each species. We placed one encased ElectricBlue EnvLogger (model 2.4) within each burrow above the nest, which is typically located at the back of the burrow (Fig. 1b). The EnvLoggers recorded temperatures every 30 min at ≤0.1 °C precision. To reduce disturbance and chances of egg abandonment, temperature loggers were deployed between mid-incubation to chick fledging, specifically from June to August 2021 for Atlantic Puffins and from August to October 2021 for Leach’s Storm-petrels. Seven loggers placed within Atlantic Puffin burrows were lost, likely displaced by adult birds; therefore, temperature data from 23 internal loggers remained for our analyses. All 30 loggers were successfully retrieved from Leach’s Storm-petrel burrows.

External environmental conditions

To gain a conservative estimate of temperature and wind outside of the burrows, we acquired ambient air temperature and wind speed data measured at 1.3 m above ground-levels on Gull Island with mobile weather stations (Kestrel 5500 Weather LiNK) positioned 10–60 m from the study plots (Fig. 1a). One weather station was placed in the open grassy habitat and a second was placed in the forested habitat. The weather stations were programmed to record data every 30 min. To understand the temperatures that Atlantic Puffin and Leach’s Storm-petrels experience at ground-level near their burrows, we further measured the temperature 1 cm above the ground close to the entrance of each burrow with ElectricBlue EnvLoggers (Fig. 1b). All external loggers were programmed to the same specifications as the internal temperature loggers. Only one external logger that was placed outside an Atlantic Puffin burrow was lost.
Fig. 2.
Fig. 2. Mean temperature (±SD) through the day (a and c) and through the season from mid-incubation to fledging (b and d) within (n = 23) and outside (n = 29) Atlantic Puffin burrows over 35 days and within (n = 30) and outside (n = 30) Leach’s Storm-petrel burrows over 49 days. Blue and light brown lines represent the external and internal logger temperatures, respectively, while green represents the temperatures recorded at weather stations. Extreme cold events are indicated by blue arrows, and the hurricane with a black arrow. Bird illustrations by Cerren Richards.

Burrow and plot characteristics

We measured multiple internal dimensions of each burrow chamber (Fig. 1b): depth—distance from the burrow entrance to end; width—distance between both adjacent burrow walls; and height—distance from floor to roof of burrow. To represent the thermal mass required to be heated or cooled, we calculated the burrow volume using the elliptical cylinder volume equation (eq. 1). We further quantified the entrance area using ImageJ software which calculates a surface area from a photograph (Schneider et al. 2012).
Volume = π × Height2 × Width2 × Depth
(1)
We selected Leach’s Storm-petrel burrows from plots with varying foliage coverage, from open grass meadows to dense forests (Fig. 1). To estimate the percentage of tree canopy cover, a square photograph was taken of the sky facing north at chest height above each burrow, and the area covered by trees was later calculated using ImageJ (Schneider et al. 2012). Atlantic Puffin nests were selected in a plot across a single grassy slope (Fig. 1). On Gull Island, Atlantic Puffins nest exclusively on grassy slopes; therefore, tree canopy cover data were not collected for this species.

Data analysis

Internal and external thermal environment

To compare the inter- and intraspecific variation in burrow thermal environments, we summarised the mean, ranges, and average daily minimum and maximum temperatures over the study period. To understand variations in ambient temperatures outside Atlantic Puffin and Leach’s Storm-petrel habitats at different heights, we further summarised the difference in the ground-level (1 cm) and above-ground (1.3 m) ambient temperatures through the season and during extreme events. To define extreme cold events during the species’ breeding seasons, we extracted the 99th percentile of external air temperatures recorded at the weather stations, based on a common definition of an extreme event (McPhillips et al. 2018). For Atlantic Puffins, the extreme cold event occurred in mid-August, while the Leach’s Storm-petrel extreme cold event occurred during Subtropical-Cyclone Odette in late September. We further summarise the temperature variations during Hurricane Larry which hit Gull Island in mid-September during the Leach’s Storm-petrel breeding season.

Correlates of burrow thermal microclimate

To test for correlation between external weather conditions and burrow thermal environment, we constructed a generalized additive mixed model (GAMM) for each species using package “mgcv” and function gamm (Wood 2004, 2017). Internal burrow temperature was included as the response variable. For the predictor variable, the interaction between air temperature and wind speed was scaled and modelled as a smooth term. Predictors were fitted with thin plate regression splines (bs = “ts”), which is equivalent to the default gam smooth (bs = “tp”) but with a modification to the smoothing penalty, so that the null space is also penalized slightly and the whole term can therefore be shrunk to zero (Wood 2004, 2017). Burrow ID was included as a random effect and we modelled a within-burrow corAR1 structure to account for autocorrelation (Models S2.6 and S2.12).

Burrow thermal refuge and buffering capacity

To identify the thermoneutral range of Atlantic Puffin and Leach’s Storm-petrel chicks and adults, we extracted values for the lower and UCTs from the literature (Table 1). Given the UCTs of both species’ remains largely unreported, we focus all further analyses on the LCTs. For each burrow, we calculated the proportion of time through the season, during extreme cold events, and the hurricane that: (1) internal temperatures fell below the adult and chick LCTs; and (2) burrows provided a thermal refuge from cold i.e., internal burrow temperatures were warmer than ambient above-ground temperatures. Next, to quantify the thermal buffering capacity of burrows while they function as thermal refuges, we calculated the temperatures inside the burrows minus the ambient above-ground temperatures. Therefore, higher positive values reflect superior buffering capacity. The weather station temperatures (1.3 m above-ground) were selected for these calculations because they provide a conservative estimate of temperature in the environment. We then compare the inter- and intraspecific variations in the time that internal temperatures of Atlantic Puffin and Leach’s Storm-petrel burrows fell below their LCTs, act as a thermal refuge from cold, and the buffering capacity of burrows during extreme events and across the whole season.
Table 1.
Table 1. Known lower critical temperature (LCT) and upper critical temperature (UCT) of Atlantic Puffin and Leach’s Storm-petrel chicks and adults.
SpeciesAgeLatitudeLCT (°C)UCT (°C)
Atlantic PuffinBreeding Adult*47°N13.4 (95% CI: 15.9, 11.0)Not reported
 0–2 day old Chick65°N3235
Leach’s Storm-petrelIncubating Adult,§47°N24Not reported
 0–10 day old Chick||44°N32Not reported

Note: All temperatures are measured in the field, except for the LCT of adult Atlantic Puffins which was extrapolated from a regression between latitude and mass.

Correlates of burrow buffering capacity

To identify the unique features of burrows that relate to buffering capacity during extreme cold temperatures, we built a GAMM model (Wood 2004, 2017) for each species (Models S2.14 and S2.16). Buffering capacity of each burrow during cold extreme events (99th percentile) was included as the dependent variable. The burrow characteristics of entrance area and volume were scaled with default settings and included as predictor variables and modelled as smooth terms. Canopy cover was also scaled and included as a smooth term predictor within the Leach’s Storm-petrel models. Atlantic Puffins nest exclusively on grassy slopes; therefore, canopy cover was not included in the model for the species. All predictors were fitted with thin plate regression splines (bs = “ts”). Burrow ID was added as a random effect and we modelled a within-burrow corAR1 structure to account for autocorrelation. All model structures and selection procedures are available at https://github.com/CerrenRichards/Burrow-Microclimate and Supplementary Material 2. All analyses were conducted with R version 4.0.4 (R Core Team 2021).

Results

Internal and external thermal environment

We found that the overall mean internal burrow temperature through the breeding season of each species was 17.9 °C (SD = 1.7 °C) for Atlantic Puffins and 15.8 °C (SD = 1.3 °C) for Leach’s Storm-petrels (Fig. 2). Atlantic Puffin burrow temperatures ranged between 13.0 and 25.1 °C, while the Leach’s Storm-petrel burrow temperature range was 9.7 to 22.2 °C. The average daily minimum and maximum across Atlantic Puffin burrows was 16.8 °C (SD = 0.8 °C) and 19.6 °C (SD = 1.2 °C), respectively. For Leach’s Storm-petrel burrows, the average daily minimum was 15.2 °C (SD = 0.7 °C) and maximum was 16.5 °C (SD = 0.9 °C). We also found considerable variability in the intra-burrow temperatures for both species (Fig. 3). The mean intra-burrow temperatures ranged from 16.3 to 20.6 °C for Atlantic Puffins and from 14.3 to 17.8 °C for Leach’s Storm-petrels, indicating that some burrows were consistently warmer while others were consistently cooler.
Fig. 3.
Fig. 3. The temperature range and mean temperature (black dots) across 23 Atlantic Puffin burrows over 35 days (a) and within 30 Leach’s Storm-petrel burrows over 49 days (b). The dark blue dashed line represents the adult lower critical temperatures (LCTadult) and the light blue dashed line represents the chick lower critical temperatures (LCThatchling). Grey box represents the range of LCTs experienced by the species. Burrows are ordered by mean temperature. Bird illustrations by Cerren Richards.
Across the breeding season for each species, the average temperature at 1 cm above ground-level outside Atlantic Puffin burrows was 19.7 °C (SD = 7.0 °C), and 15.5 °C (SD = 3.6 °C) outside Leach’s Storm-petrel burrows. Moreover, the average daily maximum temperature outside Atlantic Puffin burrows was 31.7 °C (SD = 3.5 °C) and outside Leach’s Storm-petrel burrows it was 21.2 °C (SD = 2.8 °C). The average daily minimum temperature outside Atlantic Puffin burrows was 13.8 °C (SD = 0.4 °C), and outside Leach’s Storm-petrel burrows was 12.7 °C (SD = 0.4 °C). The ambient temperature at 1.3 m above ground-level was consistent between the two weather stations, with an average temperature of 15.8 °C (SD = 3.5 °C) and range from 5 to 27.8 °C.
During cold extremes, the coldest temperatures measured outside Atlantic Puffin burrows in mid-August fell to 9.4 °C (SD = 1.6 °C) measured at 1 cm above ground-level and to 9.1 °C (SD = 0.7 °C) measured at 1.3 m above ground-levels. The coldest temperatures for Leach’s Storm-petrels were measured during Subtropical-Cyclone Odette in late-September, and fell to 6.5 °C (SD = 0.9 °C) measured at 1 cm above ground-level and to 6.0 °C (SD = 0.3 °C) at 1.3 m above ground-level. During Hurricane Larry in mid-September, the average ambient temperatures outside Leach’s Storm-petrel burrows at 1 cm above ground-level (17.7 °C, SD = 1.7 °C) and 1.3 m above ground-level (18.2 °C, SD = 1.3 °C) was slightly warmer than the average temperatures throughout the season. Atlantic Puffin chicks had fledged prior to the hurricane.

Correlates of burrow thermal microclimate

We found that the thermal microclimate of Atlantic Puffin and Leach’s Storm-petrel burrows changed due to weather conditions. There was a nonlinear interaction effect between wind speed and temperature (p < 0.001 for Atlantic Puffins and Leach’s Storm-petrels, from GAMM models, see Supplementary Material 2, Models S2.6 and S2.12 for coefficient values). For both species, internal burrow temperature was lowest at low values of external air temperature and wind speed. Across all wind speeds, the internal temperature of Atlantic Puffin burrows was highest when air temperature was the highest. For Leach’s Storm-petrel burrows, internal temperature was highest when wind speed was low and air temperature was high.

Burrow thermal refuge and buffering capacity

Here we found that all burrow temperatures were considerably colder than the lower critical temperature for hatchlings of both species and adult Leach’s Storm-petrels, indicating that they were outside of their thermoneutral zone throughout the breeding season and during extreme events (Fig. 3 and Table 2). In contrast, burrow temperatures were cooler than the lower critical temperature of adult Atlantic Puffins only 0.2% (SD = 0.5%) of the season and 0.2% (SD = 1.2%) of the time during cold temperature extremes (Fig. 3 and Table 2).
Table 2.
Table 2. The proportion of time that internal temperatures of Atlantic Puffin and Leach’s Storm-petrel burrows fell below their lower critical temperatures (LCT), act as a thermal refuge from cold, and the buffering capacity of burrows during extreme events and across the whole season.
  Time below chick LCT (%)Time below adult LCT (%)Time as cold refuge (%)Buffering capacity (°C)
SpeciesTime PeriodGlobal meanGlobal meanIntra-specific rangeGlobal meanIntra-specific rangeGlobal meanIntra-specific mean range
Atlantic PuffinCold extreme1000.20–6100 8.05.5–10.5
 Whole season1000.20–26650–843.21.7–5.1
Leach’s Storm-petrelCold extreme (subtropical cyclone)100100 100 7.44.4–9.3
 Hurricane100100 140–630.80.1–1.1
 Whole season100100 5332–772.51.7–3.4

Note: Time as a cold refuge represents the proportion of time that internal burrow temperatures are higher than external temperatures. Buffering capacity is the difference in temperature between internal and external burrow temperatures. Global mean is the average across all burrows, while the intraspecific range represents the variation between burrows.

Through the breeding season, there was large intraspecific variation in the extent that burrows provided a cold thermal refuge for chicks and adults (i.e., internal burrow temperatures were warmer than ambient above-ground temperatures), and in the burrow buffering capacity whilst burrows were thermal refuges (i.e., temperatures inside the burrows minus the ambient above-ground temperatures) (Fig. 2 and Table 2). Atlantic Puffin burrows provided a cold thermal refuge for 50% to 84% of the season and the mean buffering capacity in each burrow ranged from 1.7 to 5.1 °C. Leach’s Storm-petrel burrows acted as thermal refuges from cold for 32% to 77% of the season and the intraspecific buffering capacity ranged from 1.7 to 3.4 °C.
During cold weather events, both Atlantic Puffin and Leach’s Storm-petrel burrows provided a thermal refuge for adults and chicks because burrows were always warmer than environmental temperatures (Table 2). The burrows further provided the greatest buffering during the extreme cold weather, with Atlantic Puffin burrows 8.0 ± 1.5 °C warmer overall than external temperatures and the average intraspecific burrow temperature ranged from 5.5 to 10.5 °C. Similarly, Leach’s Storm-petrel burrows were 7.4 ± 1.2 °C warmer overall during the extreme cold measured during the extratropical cyclone with a large average intraspecific burrow temperature variation (4.4 to 9.3 °C). By contrast, the hurricane produced warmer temperatures than the average outside seasonal temperatures; therefore, most burrows were colder than external temperatures, and were only thermal refuges for 14% of the hurricane’s duration with a 0.8 ± 0.7 °C buffering capacity.

Correlates of burrow buffering capacity

Unique features of burrows that might create more buffering during extreme cold weather did not emerge for Atlantic Puffins (see Supplementary Material 2, Model S2.16) nor for Leach’s Storm-petrels (see Supplementary Material 2, Model S2.14).

Discussion

Here we revealed that both the Atlantic Puffin and Leach’s Storm-petrel actively breed in burrow microclimates that are below their LCTs. Specifically, burrow temperatures always fell below the LCTs of both adult and chick Leach’s Storm-petrels, and Atlantic Puffin chicks throughout the season. Yet, for adult Atlantic Puffins, the burrow temperatures were higher than their LCTs. Similar observations have been found in other burrowing auk and tubenose species in polar and tropical regions. For example, burrow temperatures of Dovekie (Alle alle) breeding in the high arctic fell below adult lower critical temperature (Gabrielsen et al. 1991). Similarly, in Antarctica, burrows of Snow Petrel (Pagodroma nivea) were significantly colder than the lower critical temperature of both adults and chicks (Weathers et al. 2000). Meanwhile, in the topics, burrow temperatures were within the thermoneutral zone of adult Wedge-tailed Shearwater (Puffinus pacificus); however, burrow temperatures fell below chick LCTs (Whittow et al. 1987).
Nesting in microclimates that are outside of the species’ thermoneutral zone may have energetic consequences for both of the seabird species. For example, based on our findings, Leach’s Storm-petrel adults and chicks, and Atlantic Puffin chicks may divert considerable amounts of energy toward thermoregulation. Indeed, endotherms incur significant thermoregulatory costs to maintain body temperatures when environmental conditions are outside of their thermoneutral zones (Weathers et al. 2000). In adults, this translates to energy being diverted away from other metabolic processes, such as reproduction, while chicks divert considerable amounts of energy away from growth (Kooijman 2010). Indeed, to maintain normothermy in burrows that are significantly lower than their lower critical temperature, Snow Petrel chicks must increase their resting metabolic rate 212% above thermoneutral levels (Weathers et al. 2000). The diversion of energy towards thermoregulation and away from growth is a contributing factor that leads to burrow nesters often having slower growth and longer nest periods compared to other species, as observed in passerines and fulmarine petrels (Martin and Li 1992; Weathers et al. 2000; Durant et al. 2005).
Little is known about the thermoneutral zone and the energetic cost of thermoregulation for adult and chick Atlantic Puffin and Leach’s Storm-petrels through the breeding season (Ricklefs et al. 1980; Bech et al. 1987; Gabrielsen and Ellis 2001; Ochoa-Acuña and Montevecchi 2002). Here, to understand whether burrow temperatures fall below the species’ LCTs, we used historical experimental measurements of critical temperatures from colonies between 44°N to 65°N which represent a static snapshot of a single day in the breeding season. We also extrapolated the lower critical temperature for adult Atlantic Puffins based on a regression between latitude and mass. Yet, higher latitude seabirds can persist at lower temperatures than species of similar mass from warmer climates, and a chick’s thermoneutral zone decreases with increasing mass through the breeding season (Whittow et al. 1987; Weathers et al. 2000; Gabrielsen and Ellis 2001). Consequently, the static values for LCTs used in the present study may not fully capture the dynamic changes in adult and chick LCTs through the season within Witless Bay Ecological Reserve, located at 47°N. Future research could leverage non-invasive methods, such as a field metabolic rate approach or Dynamic Energy Budget Theory and NicheMapper modelling frameworks, to fill spatio-temporal knowledge gaps on changes in seabird thermoneutral zones through the breeding season and across their breeding ranges (Kooijman 2010; Dunn et al. 2018; van der Meer et al. 2020; Kearney et al. 2021). Such research could help understand the interplay between temperature, energetic costs of thermoregulation, growth and breeding success implications, and identify species with limitations to extreme weather events.
Our findings strongly support that access to suitable burrowing habitat could be important for burrow nesting seabirds during extreme weather events. We find that burrows provide a stable thermal environment and a refuge from cold because burrows acted as buffers that kept nests warmer than ambient temperatures during extreme cold events. Indeed, our results align with other studies on burrow-dwelling seabirds. For example, Cassin’s Auklet (Ptychoramphus aleuticus) burrow temperatures remained stable on Farallon Island, California, despite large fluctuations in outside ambient temperature (Manuwal 1974). Likewise, in the high arctic, Doviekie burrows were warmer than ambient air temperatures (Kulaszewicz and Jakubas 2018). Burrows also provide other endotherms and ectotherms, such as pangolins, insects, and lizards, thermal protection from extreme temperatures by buffering lethal hot and cold exposure (Bao et al. 2013; Moore et al. 2018; Sunday et al. 2014). Moreover, similar to the present study, occupying burrows provides a thermal refuge for a number of other species, and was further identified as an effective strategy to mitigate thermoregulatory costs. For example, while burrow temperatures often fall outside Pygmy Rabbit (Brachylagus idahoensis) and Burrowing Owl (Athene cunicularia) thermoneutral zones, their burrows provide a refuge from extreme temperatures because internal temperatures are closer to their thermoneutral zones than ambient temperatures (Nadeau et al. 2015; Milling et al. 2018b). Consequently, thermoregulation costs are lower within the burrow compared to above ground (Milling et al. 2018b). Given that climate extremes are predicted to increase in frequency and intensity in the future (Wingfield et al. 2017; Harris et al. 2018), burrows may therefore provide a direct line of defence for seabird chicks against current and future extreme cold events, as predicted for other species (Moore et al. 2018).
We found that the thermal response of burrows varied in different extreme weather events. Specifically, burrow buffering capacity was greatest during extreme cold weather events for both species. Yet, during the hurricane, there was minimal buffering within Leach’s Storm-petrels burrows because ambient temperatures were warmer than internal temperatures, thus indicating it will be important to monitor the impacts of variable extreme weather events in the future. Indeed, extreme event variability drives negative ecological responses across taxa and systems (Maxwell et al. 2019). A factor that may be critical to research further in the context of burrowing species is extreme precipitation events. For example, burrows are vulnerable to flooding and collapse during extreme precipitation events which increases breeding failure energetic demands (Wilhelm et al. 2013; Tiller et al. 2000; Glencross et al. 2021).
We further recorded large intraspecific variation in burrow temperatures, the extent that burrows were cold refuges, and burrow buffering capacity through the season and during extreme cold events. For example, there was a 5 °C difference in the average buffering capacity between burrows during extreme cold weather for both species. Similarly, there was around 4 °C difference in the mean burrow temperatures between burrows of both species through their breeding seasons. Indeed, a previous study has similarly reported large inter-nest temperature differences between Dovekie burrows in the high-Arctic (Kulaszewicz and Jakubas 2018). Here, the interplay between air temperature and wind speed emerged as a key driver for the internal thermal microclimate of Atlantic Puffin and Leach’s Storm-petrel burrows, which is consistent with other studies. For example, Cassin’s auklet burrow temperatures fluctuated in proportion to the changes in ambient temperatures, and temperatures were buffered more within soil burrows compared to rock crevice nests (Manuwal 1974). Similarly, external air temperature, wind speed, and wind direction determined the internal temperature of Wilson’s Storm-petrel (Oceanites oceanicus) nests (Michielsen et al. 2019). However, despite the large intraspecific variability in burrow buffering capacity, we found that burrow characteristics and canopy cover do not predict Atlantic Puffin and Leach’s Storm-petrel burrow buffering capacity during extreme cold weather. Given wind speed and ambient temperature were important correlates of internal burrow temperature for both species, a burrow’s insulation and protection from wind exposure may be key for predicting burrow buffering capacity during cold extremes. For example, smaller nest dimensions (entrance area), greater insulation, burrow orientation, and less wind exposure were important for establishing warmer thermal environments for Wilson’s Storm-petrels nesting in extreme cold in Antarctica (Michielsen et al. 2019).
To further explore drivers of burrow microclimates and buffering capacity, future studies could improve nest dimension measurements through 3D scanning the complex internal shapes of seabird burrows, measuring the thermal microclimate throughout the burrow tunnel and nest with an array of temperature loggers, and incorporating additional model parameters, such as nest orientation and slope.
Given the complex responses of burrow microclimates to extreme events, quantifying how changes in a variety of external and internal environmental conditions will impact burrow-nesting seabirds is a key future direction. This will be particularly critical in Newfoundland since the frequency of extreme windy days have increased over the past decade (Government of Canada 2022). Moreover, habitat management approaches may be needed to increase nest temperatures during extreme cold events. Artificial nest boxes show great promise for improving the breeding success of burrowing seabirds (Libois et al. 2012; Sutherland et al. 2014). Insulation or artificial heating of nests when temperatures fall below the species’ LCTs may be a way to protect chicks from future extreme cold events. Even so, special consideration of the nest box design will be imperative to prevent overheating or excessive cooling (Lei et al. 2014; Kelsey et al. 2016; Fischer et al. 2018).

Conclusion

Our study reveals that Atlantic Puffins and Leach’s Storm-petrels nest in burrow microclimates below their optimal temperatures, which may impose significant thermoregulatory costs. Given that internal burrow temperatures are strongly driven by external environmental conditions, Atlantic Puffins and Leach’s Storm-petrels may be pushed even further outside of their thermoneutral zone as extreme events increase in frequency and intensity. However, burrows do act as a thermal refuge during extreme cold events because nests are kept warmer than ambient temperatures, thus indicating burrows may provide some protection to breeding seabirds in the face of climate change. Leveraging non-invasive methods to quantify seabird thermoneutral zones will help understand their energetic limitations to complex extreme weather events. Moreover, it will be important for future studies to identify and manage burrows that promote optimal thermal environments for breeding success with conservation tools, such as artificial nest boxes.

Acknowledgements

We thank Nikole White, Amy Wilson, and Sarah Watkins for assistance with fieldwork. We further thank Sarah Wong for supplying funding though Environment and Climate Change Canada. We also appreciate the valuable feedback from Shawn Leroux.

References

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Supplementary material

Supplementary Material 1 (CSV / 12.8 MB).
Supplementary Material 2 (PDF / 18.2 MB).

Information & Authors

Information

Published In

cover image FACETS
FACETS
Volume 9Number 1January 2024
Pages: 1 - 11
Editor: Mark Mallory

History

Received: 29 July 2023
Accepted: 23 April 2024
Version of record online: 27 August 2024

Data Availability Statement

Data analysed during this study are provided in Supplementary Material 1. R code covering the major analytical steps is available on GitHub at https://github.com/CerrenRichards/Burrow-Microclimate.

Key Words

  1. burrow
  2. extreme event
  3. lower critical temperature
  4. microclimate
  5. seabird
  6. temperature

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Affiliations

Department of Ocean Sciences, Memorial University of Newfoundland, St. John's, NL, Canada
Author Contributions: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Resources, Software, Validation, Visualization, Writing – original draft, and Writing – review & editing.
Cognitive and Behavioural Ecology, Departments of Biology and Psychology, Memorial University of Newfoundland, St. John's, NL, Canada
Author Contributions: Investigation, Methodology, and Writing – review & editing.
Kayla Fisher
Cognitive and Behavioural Ecology, Departments of Biology and Psychology, Memorial University of Newfoundland, St. John's, NL, Canada
Author Contributions: Investigation, Methodology, and Writing – review & editing.
Cognitive and Behavioural Ecology, Departments of Biology and Psychology, Memorial University of Newfoundland, St. John's, NL, Canada
Author Contributions: Investigation, Methodology, and Writing – review & editing.
Wildlife Research Division, Environment and Climate Change Canada, Mount Pearl, NL, Canada
Author Contributions: Conceptualization, Formal analysis, Funding acquisition, Methodology, Supervision, Validation, and Writing – review & editing.
Department of Ocean Sciences, Memorial University of Newfoundland, St. John's, NL, Canada
Department of Biology, University of Victoria, Victoria, BC, Canada
Author Contributions: Conceptualization, Formal analysis, Funding acquisition, Methodology, Project administration, Supervision, and Writing – review & editing.

Author Contributions

Conceptualization: CR, DAF, AEB
Data curation: CR
Formal analysis: CR, DAF, AEB
Funding acquisition: DAF, AEB
Investigation: CR, SMC, KF, RJB
Methodology: CR, SMC, KF, RJB, DAF, AEB
Project administration: CR, AEB
Resources: CR
Software: CR
Supervision: DAF, AEB
Validation: CR, DAF
Visualization: CR
Writing – original draft: CR
Writing – review & editing: CR, SMC, KF, RJB, DAF, AEB

Competing Interests

The authors declare there are no competing interests.

Funding Information

Canada Research Chairs, Grant Number: 950-231832; NSERC Discovery Grants Program, Grant Number: 2019-04987; Environment and Climate Change Canada funding.

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