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Monotreme and therian mammal lineages diverged between 160 and 250 million years ago [1] and monotremes retain many plesiomorphic anatomical, reproductive and physiological traits not shared with therians. Consequently, their biology provides important insights into mammalian evolution, with the short-beaked echidna (Tachyglossus aculeatus) considered a particularly useful living model for proto- or baso-endothermy [2,3]. One ongoing question is whether their perceived poor thermoregulatory ability is primitive or derived. While the echidna’s low and variable core body temperature (Tb) can be considered a primitive trait reflecting their early divergence from therians, other thermoregulatory characteristics such as metabolic rate, thermal conductance and evaporative heat loss (EHL) capacity are typically therian [4] after accounting for their lower Tb. Despite this, laboratory studies suggest that echidnas have a low thermal tolerance, with a Tb of 38°C and air temperature (Ta) of only 35°C considered lethal [5,6].
Early studies suggested that the low thermal tolerance of short-beaked echidnas was a consequence of an inability to enhance heat loss due to a lack of sweating, panting, licking or vasomotor adjustment [5–7] and a reliance on behavioural avoidance of high Ta [5,8]. Indeed their activity patterns suggest they avoid activity at high Ta and switch to primarily nocturnal behaviour during summer [9,10]. However, short-beaked echidnas have been observed sheltering in hollow logs where Ta exceeds the supposed lethal Ta [11] and there is unequivocal evidence that they can increase evaporative water loss and both wet and dry thermal conductance at Ta ≥ 32.5°C [4]. Although the mechanisms for this enhanced heat loss are currently unknown, thermal and evaporative windows may be important.
Thermal windows are regions of an animal’s body surface that vary heat exchange with the environment, being ‘opened’ or ‘closed’ by changes in exposure and/or blood flow; they have been reported for many mammals and birds [12]. Evaporative windows, where endogenous water is behaviourally applied to areas with specialized vasculature, have been reported less often. Forearm licking by kangaroos is one example; saliva is spread over the sparsely furred forearms to evaporatively cool blood in an underlying network of superficial blood vessels [13,14]. Barker et al. [4] observed echidnas blowing bubbles from their nares at high Ta and hypothesized that this enhances EHL. The bubbles broke just behind the nares where the dorsal blood sinus has its maximum blood volume [15]. Here we investigate surface temperatures (Ts) of wild, free-living short-beaked echidnas under a range of environmental conditions to test the hypothesis that the beak tip may act as an evaporative window. We also examine other body regions to evaluate their potential to function as thermal windows.
2. Methods
We used infrared thermography [12,16,17] to remotely measure the Ts of short-beaked echidnas. Echidnas were located at Dryandra Woodland and Boyagin Nature Reserve, in the West Australian wheatbelt, approximately 170 km southwest of Perth. Once sighted, we recorded thermal videos using a FLIR T1050sc infrared camera with an f 83.4 mm 12° telephoto lens, from a distance of 1–20 m. The camera was calibrated against a national standard (FLIR, Oregon, USA). We obtained thermal data in each of 12 months (January to December) for a total of 34 days, during 2020–2021, for 124 echidnas. Most echidnas were not individually identifiable so it was not possible to exclude potentially repeated measurements of some individuals on different days, but recordings were made over a large area in both reserves to minimize the repeated measurement of individuals. Microclimate variables (ambient temperature, Ta; relative humidity, RH; wet bulb globe temperature, WBGT) were collected in a similar location to the echidna under the same conditions of solar radiation, within 0–20 m of the location the echidna was filmed, with a Kestrel 5400 portable weather station.
Thermography videos were analysed using Researcher IR Max4 software, assuming an emissivity of 0.95, with an atmospheric temperature equivalent to Ta, an environmental temperature calculated as the mean of ground and Ta, and the measured RH and camera to echidna distance for each recording (after [17]). Mean Ts were calculated for polygons manually drawn on video frames showing various body parts; body (lateral and dorsal surface), ventral surface, ear, inside leg, mid-spine (sacral), beak base and beak tip (see insets, figure 1). It was not possible to obtain a Ts for every body part for every echidna as visibility depended on the animals’ orientation, behaviour and the terrain. Ground temperature in the immediate vicinity of each echidna was obtained from the thermal videos.
Figure 1. Surface temperature of various body regions plotted against wet bulb globe temperature (WBGT) for 124 active short-beaked echidnas (Tachyglossus aculeatus) filmed with an infrared camera in the West Australian wheatbelt. The solid line represents a slope = 1 for WBGT, the dashed line the observed slope for the relationship; asterisks indicate that the slope is significantly different from 1. The inset thermal image shows the body region represented by each panel, outlined with a green polygon.
Figure 1. Surface temperature of various body regions plotted against wet bulb globe temperature (WBGT) for 124 active short-beaked echidnas (Tachyglossus aculeatus) filmed with an infrared camera in the West Australian wheatbelt. The solid line represents a slope = 1 for WBGT, the dashed line the observed slope for the relationship; asterisks indicate that the slope is significantly different from 1. The inset thermal image shows the body region represented by each panel, outlined with a green polygon.
Statistical analyses were accomplished in RMarkdown [18]. We used a similar approach to Klier et al. [19,20] to evaluate the potential for heat exchange of various body regions, by exploring the linear relationship between the various body regions and environmental temperature. Linear mixed-effect models were used to examine the relationship for Ts with WBGT, body part and observation distance while accounting for individual nested in day as random factors, using the lmer function in lme4 [21] with lmerTest [22] to determine probabilities. Mean Ts was compared for body parts using the lmer model results using lsmeans with WBGT as an interaction term. As there was a significant interaction between WBGT and body part Ts, we then investigated this relationship individually for each body part. We use WBGT as a measure of the thermal environment for comparison with echidna Ts as WBGT includes the contributions of Ta as well as convection, radiation and evaporation to the thermal environment.
3. Results
Videos of echidnas (electronic supplementary material, figure S1) were recorded between 09.56 and 22.41 h, with Ta ranging from 10.7 to 37.4°C and WBGT from 8.4 to 27.8°C (table 1; electronic supplementary material, table S1). Mean Ts of the various body parts ranged from 19.3 ± 0.27°C for the beak tip to 29.2 ± 0.27°C for the ear orifice. The mean Ts of body parts at the mean WBGT (17.3°C) differed (t650–660 ≥ 4.03, p < 0.002), with the exception of ear and mid-spine (t656 = 1.71, p = 0.608), mid-spine and ventral (t658 = 2.44, p = 0.184), ventral and inside leg (t654 = 2.32, p = 0.238), and body and beak base (t656 = 1.65, p = 0.651) regions (figure 2). The Ts was significantly related to both WBGT (F1,121 = 38.7, p < 0.001) and body region (F6,659 = 12.8, p < 0.001) with a significant interaction (F6,659 = 5.41, p < 0.001), but there was no effect of imaging distance (F1,106 = 2.88, p = 0.093) or of animal nested in day (LRT2 = 4.46, p = 0.108).
Table 1. Microclimate variables collected at the time of each echidna thermal recording with a Kestrel 5400 portable weather station placed in a similar location to the echidna under the same conditions of solar radiation.
Figure 2. Mean surface temperature of various body regions for 124 active short-beaked echidnas (Tachyglossus aculeatus) filmed with an infrared camera in the West Australian wheatbelt. Different letters indicate significant differences between body part surface temperatures. The dashed line indicates the mean wet bulb globe temperature at which echidnas were filmed, the grey area the core body temperature range of active echidnas in a semi-arid habitat [9] and the solid line the basal core body temperature for echidnas from this study site [4].
4. Discussion
We observed echidnas active at maximum Tas that were 2.4°C higher than their supposed lethal Ta of 35°C and up to 5.4°C higher than the previously reported maximum active Ta [11,23]. Our data, combined with observations that echidnas can shelter in hollow logs at temperatures up to 40°C [11], provide clear evidence that previous estimates of lethal Ta were underestimates and highlights the value of detailed field studies for evaluating the physiological capabilities of wild animals (e.g. [24–26]). Echidnas can clearly tolerate higher Ta and are less reliant on behavioural thermoregulation than previously appreciated; we propose that the thermal and evaporative windows we identify here contribute to this thermal tolerance.
The surface temperature of animals obtained by thermal imaging can vary considerably from Tb [12]. Ear temperature of echidnas most closely approximated Tb (figure 2); basal Tb for this sub-species is 29.5C [4] and varies from 23–35°C when active in a semi-arid environment at Ta from 15–33°C [9]. Consequently, the slope for ear temperature against WBGT was significantly lower than 1, reflecting the considerable effect of Tb on Ts for this region. Tympanic membrane temperature, accessed via the external auditory canal, provides the anatomically closest non-invasive access for measurement of hypothalamic temperature [27]. As monotremes lack external ear pinnae, the temperature of the auditory canal can be seen by thermography via the external ear opening.
We identify ventral, inside leg and mid-spine areas as avenues of conductive and convective heat loss that can therefore function as thermal windows. Temperatures of these regions approximated ear temperature (and so are also close to Tb), and the WBGT relationship for ventral and inside leg surfaces also had a slope significantly lower than one, indicating limited insulation. Ventral and inside leg surfaces are sparsely furred, lack spines and can be ‘opened’ or ‘closed’ as thermal windows by postural changes and pressing them against cool soil, a potential heat sink identified by previous workers [11,23]. Their ventral position also protects them from incident solar radiation which is important for maximizing their effectiveness [14].
The echidnas’ dorsal and lateral body Ts was significantly lower than the body parts identified as thermal windows and scaled with WBGT (slope = 1; albeit with a substantial intercept) suggesting that its surface is well insulated from Tb and is influenced by environmental conditions such as warming with solar radiation. The body surface is insulated by a combination of a fat layer overlain by a large sub-cutaneous muscle into which the spines are embedded [2]. These three layers clearly provide excellent insulation and explain why Tasmanian echidnas (T. a. setosus), with considerable fur between the spines, have similar insulation at low Ta to the dorsally furless T. a. acanthion [28]. However, T. a. acanthion can achieve higher thermal conductance at high Ta than T. a. setosus [28] suggesting that the spines provide greater insulative flexibility than fur. The mobility of the spines means that they can be flattened to cover the dorsal surface, ‘closing’ the thermal window and reducing heat loss, or erected, exposing the underlying skin, especially along the sacral (mid-spine) region and ‘opening’ this thermal window. The mid-spine sacral region Ts was statistically indistinguishable from the ear temperature and significantly higher than the body Ts, but had an intermediate and more variable relationship with WBGT compared to that of the body surface and the ear (figure 1). Incorporating all the dorsal fur into spines provides T. a. acanthion with a flexible thermal window to control heat loss in the highly variable thermal environments this sub-species inhabits.
We identify the beak tip of short-beaked echidnas as a unique type of evaporative window. The beak tip, containing a large dorsal blood sinus [15], is kept moist to facilitate electroreception [29]. An additional role of this moist surface is evaporative cooling of the underlying blood within the sinus; with a slope equivalent to 1 and minimal intercept, the beak tip functions as a wet bulb globe thermometer. At high Ta echidnas blow mucus bubbles, adding moisture to the beak tip [4]. This unique nasal evaporative window is of particular value for echidnas (which do not pant, lick or sweat [5–7]) especially under conditions where environmental temperature exceeds Tb and evaporation is the only avenue available for heat loss. Although application of exogenous water to the body surface is a widely employed thermoregulatory strategy for mammals, especially those that lack or have few sweat glands [28], there have been few descriptions for endotherms of specialized evaporative windows where endogenous water is behaviourally applied to areas with specialized vasculature. The classic examples of evaporative windows are for storks and turkey vultures, which urinate on their legs that contain extensive subcutaneous vascularization, facilitating EHL [30–32]. Seals on rocks similarly urinate to wet their ventral surface and vascularized flippers to enhance EHL [33], while the licking of vascularized forearms by macropods [13,14] is the best-known mammalian example. Here we demonstrate the utility of the echidnas’ novel nasal evaporative window, moistened by nasal mucus bubbles at high Ta [4], in functioning as a wet bulb that maximally dissipates evaporative heat.
5. Conclusion
Echidnas have a more sophisticated suite of thermoregulatory strategies than has been generally appreciated, and we add to this evidence of a novel nasal evaporative window, along with postural thermal windows, and spines that provide for flexible insulation. These physiological strategies explain observations of echidnas active over a much wider range of thermal conditions than has been previously reported and provide mechanisms for how they survive temperatures above their supposed lethal limits. These thermoregulatory traits enable echidnas to inhabit all terrestrial habitats on the Australian continent; they are the most widespread native Australian mammal and have not suffered the same pattern of decline as other critical weight-range (35–5000 g; [34,35]) and arid-zone terrestrial mammals [9].
Experiments followed the Australian Code of Practice for the care and use of animals for scientific purposes, approved by Curtin University animal ethics committee (AEC_2019_23).
Data accessibility
The datasets supporting this article have been uploaded as electronic supplementary material [36].
Authors’ contributions
C.E.C.: conceptualization, data curation, formal analysis, investigation, methodology, resources, visualization, writing—original draft; P.C.W.: conceptualization, investigation, methodology, resources, writing—review and editing.
All authors gave final approval for publication and agreed to be held accountable for the work performed therein.
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.
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Two Pretoria women have turned a rubbish dump into a thriving little vegetable garden, growing spinach and mutshaina (African spinach).
During the Covid-19 lockdown in 2020, Lufuno Doyoyo and Sinah Mudau decided to use a vacant piece of municipal land to grow and sell food in the community. With approval from the local councillor, they planted seeds on the small plot in Salvokop, just outside central Pretoria.
“We wanted to do something positive and be active,” said Doyoyo. “We were tired of just sitting and doing nothing.”
According to the City of Tshwane, about 1 000 people live in Salvokop, and many of them are unemployed.
With help from Doyoyo’s brother, the two women started clearing up the land and removing rubbish and soon they were surprised when a group of men joined in.
Doyoyo said:
They got inspired to help clean up.
They had to caution people to stop throwing rubbish in the area and later managed to put up a small fence in the front. Water to maintain their garden is connected straight from the street underground pipe.
They employ an assistant, Eugene Govi, who works in the garden while the two women do their own work. Mudau runs a food business just next to the garden, where some of the spinach is also being cooked.
They want to finish clearing the land and fencing it. They would also like to grow other vegetables. They sell about 20 batches of spinach and mutshaina per week, making roughly R200.
The money needed for Govi’s salary, seedlings and other costs comes from their own savings.
Doyoyo said they would like to learn more about growing food and intend to apply for help through the Department of Agriculture, Land Reform and Rural Development’s Comprehensive Agricultural Support Programme.
Eventually, they hope to create more jobs and to sell vegetables outside Salvokop.
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Participant seen holding a sign at the School Strike for Climate in New York City. (Photo by Erik McGregor / LightRocket via Getty Images)
For more than a decade, The Nation has highlighted the work of aspiring journalists in StudentNation, an online section of the magazine written by young people. With generous support from the Puffin Foundation, StudentNation has published hundreds of talented young writers covering a wide range of issues through local reporting, firsthand accounts, interviews, and personal essays. The following material is adapted from three recent StudentNation articles. To see the original stories, go to TheNation.com/students.
What Keith Ellison’s Reelection Means for Tough-on-Crime Rhetoric
By Theia Chatelle (December 19, 2022)
If Democrats hope to fend off future Republican attacks on vulnerable representatives, they could draw on Keith Ellison’s playbook. He faced a difficult challenge to his reelection bid from Jim Schultz, who, like many other GOP candidates across the country, was looking to win the votes of suburban voters by inflaming fears of rising crime in America’s urban centers. Ultimately, Ellison beat Schultz by only 21,000 votes, enough to avoid a recount. What worked for Ellison might not work in other areas of the country, but his message on crime as a broader phenomenon that hurts consumers and communities resonated with Minnesota voters.
Ellison was able to point to his substantive record of fighting profiteering and white-collar crime and protecting consumers as Minnesota’s attorney general. However, in a state scarred by division in the wake of the Black Lives Matter protests of 2020, Republicans were able to capitalize on voters’ fears and create a very close race for an otherwise popular Democratic incumbent.
Students Tell Their Universities: Keep Fossil Fuel Companies Out of Climate Research
By Ilana Cohen (November 22, 2022)
Bringing pizza and wearing T-shirts that read “No More Fossil Fuel Money,” they came well-prepared. On November 14, nine students at George Washington University occupied the main office of the Regulatory Studies Center for 12 hours to kick off the international days of action. The center has received at least $6 million from ExxonMobil and far-right charitable organizations heavily associated with climate denialism, including the Koch Family Foundation, the Searle Freedom Trust, and the Sarah Scaife Foundation.
For Bella Kumar, a coordinator for Sunrise GW, the 2022 midterm elections crystallized the desire to hold the center accountable. “Our government has failed to deliver on climate change and our representatives are in the pockets of the fossil fuel industry, and we know it,” said Kumar, who expressed frustration with her university’s inaction. “Universities occupy a unique space in their ability to vastly alter the social license of an industry through research. Demanding fossil-free research is not only giving us the opportunity to take back our institutions, but setting standards for our academic freedom and our futures.”
Illinois Voters Just Made Collective Bargaining a Constitutional Right
By Tomas Miriti Pacheco (November 17, 2022)
On November 8, voters in Illinois took to the polls to approve the addition of Amendment 1, also known as the Workers’ Rights Amendment, to their state Constitution. The amendment guarantees the fundamental right to organize and collectively bargain for Illinois workers. ”No law shall be passed that interferes with, negates, or diminishes the right of employees to organize and bargain collectively,” it states.
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At the University of Chicago, the largest employer in the city’s low-income South Side, organizers have spent weeks reflecting on the impact that the amendment will have and the struggles that led to this moment. On November 2, the UChicago Graduate Students United–UE passed a joint endorsement of the amendment with organizers at Northwestern University during a meeting attended by more than 200 members. “This amendment is a milestone in establishing the right to organize as a fundamental right of workers,” said Joe Rathke, a member of UChicago’s GSU who studies labor history.
Rathke is not alone in his excitement over the win. The passage of the amendment is a historic achievement for organized labor, particularly in the Midwest, which had been a hostile environment for workers. Recently, the country—and Illinois specifically—has seen a dramatic resurgence of unions. In May 2022, Chicago became home to the first Starbucks in the Midwest to request a union election, and since then multiple locations in the city have followed. According to WBEZ Chicago, workers in the city filed 45 percent more NLRB petitions in 2022 than in the previous year: “Chicagoans are organizing their workplaces at a rate the city hasn’t seen in more than a decade.”
Illinois has set an example for how organizers in other states can secure meaningful labor victories. “We have the history of a labor movement that fought tooth and nail for these rights and to protect them from being undermined,” Rathke said. “This is a very Midwestern story.”
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