Next Article in Journal
Comparative Assessment of the Stress Response of Cattle to Common Dairy Management Practices
Next Article in Special Issue
Modeling Climate Change Effects on Genetic Diversity of an Endangered Horse Breed Using Canonical Correlations
Previous Article in Journal
The Exploitation of Toxic Fish from the Terminal Pleistocene in Maritime Southeast Asia: A Case Study from the Mindoro Archaeological Sites, Philippines
Previous Article in Special Issue
Effects of Eggshell Thickness, Calcium Content, and Number of Pores in Erosion Craters on Hatching Rate of Chinese Alligator Eggs
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 13
Issue 13
10.3390/ani13132114
animals-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Rodents Inhabiting the Southeastern Mu Us Desert May Not Have Experienced Prolonged Heat Stress in Summer 2022

by
Yang-Yang Guo
1,
Shan-Shan Wang
2,
Xinyue Wang
1,
Wei Liu
3,4 and
Deli Xu
1,*
1
College of Life Sciences, Qufu Normal University, Qufu 273165, China
2
Qufu Municipal Bureau of Agriculture and Rural Affairs, Qufu 273165, China
3
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
4
University of Chinese Academy of Sciences, Beijing 100049, China
*
Author to whom correspondence should be addressed.
Animals 2023, 13(13), 2114; https://doi.org/10.3390/ani13132114
Submission received: 27 May 2023 / Revised: 21 June 2023 / Accepted: 24 June 2023 / Published: 26 June 2023
(This article belongs to the Special Issue Adaptive Responses of Vertebrates to Climate Change)
Browse Figures
Versions Notes

Abstract

:

Simple Summary

Rodents in the Mu Us Desert may respond to increasing summer heat through behavioral or physiological adjustments. We studied the ambient temperatures that Meriones meridianus and Meriones unguiculatus might experience in their habitats. The results showed that both the heat-sensitive Meriones meridianus and the heat-tolerant Meriones unguiculatus were threatened by extreme summer heat. In addition, although vegetation and rodent burrows increased the variety of ambient temperature in the habitat, only rodent burrows were effective in providing protection from the stress of extreme summer heat. Therefore, behavioral adjustments may be the major way in which small rodents in this region avoid continuous heat stress in summer.

Abstract

Climate change combined with human activities has altered the spatial and temporal patterns of summer extreme heat in the Mu Us Desert. To determine how those rodents living in the desert respond to increased extreme heat in summer, in July 2022, during the hottest month, we examined the rodent species, vegetation coverage, and small-scale heterogeneity in ambient temperature in the southeastern Mu Us Desert. The results showed that Meriones meridianus, Meriones unguiculatus, and Cricetulus longicaudatus were found in the study area, where the vegetation coverage is 33.5–40.8%. Moreover, the maximum temperature of the desert surface was 61.8 °C. The maximum air temperature at 5 cm above the desert surface was 41.3 °C. The maximum temperature in the burrow at a depth of 15 cm was 31 °C. M. unguiculatus might experience 4–9.3 h of heat stress in a day when exposed outside the burrow, whereas M. meridianus would experience 8.5–10.8 h of heat stress. Yet, inside the burrow, both species were barely exposed to heat stress. In conclusion, adjustments in behavioral patterns can be the main way that rodents in the Mu Us Desert adapt to the extreme heat in the summer.

1. Introduction

Hot summer is becoming a deadly season for many mammals on Earth [1,2]. Many regions of the world experienced record-breaking heat events in 2022 [3,4,5]. Moreover, the frequency and severity of extreme heat events are predicted to increase in the future due to global climate change [6]. It is necessary to understand how mammals in the wild will respond to increasing extreme summer heat.
Generally, facing extreme heat, small mammals will first reduce the stress on their thermoregulatory system through behavioral adjustments. For example, desert rodents tend to search shaded cooler places by moving around flexibly during the hottest part of the day [7]. Furthermore, some thermoregulating behaviors, such as specific postures, panting, and saliva spreading, contribute to the body heat dissipation [8]. In addition, the mammals also cope with extreme heat through physiological adjustments. Some studies indicated that adjustments in peripheral thermoeffectors and the thermoregulatory center allow animals to maintain a stable body temperature by altering the rate of heat production and heat loss [9,10,11]. Moreover, the degree of physiological tolerance to heat has become an important factor affecting the survival of desert rodents, especially when behavior does not effectively regulate the body heat balance.
The Mu Us Desert is located at the northern margin of the Loess Plateau in northwest China, covering an area of about 40,000 km2 [12,13]. The desert is mainly influenced by arid and semi-arid climates, which is a typical fragile ecological zone and very sensitive to climate change [14,15]. On the one hand, climate change is usually considered to be an important driving force of habitat change for desert rodents. For example, increasing extreme heat may have severe impacts on the thermal environment experience of animals [16]. On the other hand, human activities, such as grazing and reclamation, have aggravated the desertification in the 1970s and 1980s [17]. However, with the implementation of restoration policies approved since the 1990s, the transformation of desertification has improved [18,19]. Obviously, multiple and interacting factors create a diverse habitat for rodents in the Mu Us Desert, in which rodents should evolve all kinds of behavioral and/or physiological ways to adjust their heat adaption.
The Mu Us Desert is a common habitat for multiple rodent species, including the Mongolian gerbil (Meriones unguiculates), Midday gerbil (Meriones meridiaus), and Long-tailed hamster (Cricetulus longicaudatus) [20]. M. unguiculatus shows a high degree of tolerance for heat [21]. The range of thermal neutrality extends to 38.9 °C [22], which is perhaps one of the highest reported for small rodents in the literature. Mechanistically, this species can maintain body heat balance through the adjustment of the mitochondrial membrane, aquaporin expression in the kidney, or metabolic heat production when exposed to acute or chronic heat [22,23,24,25]. In addition, evidence from field observations suggests that M. unguiculatus is usually active during the day [26]. In contrast, M. meridianus has relatively low tolerance to heat, with a range of thermal neutrality extending to 30.1 °C [27]. This species is nocturnal [28]. As with M. meridianus, C. longicaudatus is nocturnal, but available data on its tolerance to heat are scarce [29,30]. In fact, the upper critical temperature of thermal neutrality for most of the small rodents in the Mu Us Desert is 30–38 °C [31,32,33,34]. In the present study, we are interested in whether or not the heat-tolerant M. unguiculatus adopted different coping strategy from the heat-sensitive M. meridianus in response to increased extreme summer heat. We found that behavioral adjustments could address the needs of M. unguiculatus and M. meridianus to adapt to extreme summer heat in 2022.

2. Materials and Methods

2.1. Study Area

Field experiments were conducted in the Daliuta forest conservancy area, which is located in Shenmu County, Shanxi Province, northwest China (Figure 1). The study area (39°18′ N, 110°41′ E, 1180–1224 m above sea level) lies in the southeast of the Mu Us Desert. This region is covered by sand dunes, sand sheets, and herbaceous and small shrub communities. The dominant vegetation type is shrub communities, such as Salix cheilophila, Caragana intermedia, and Artemisia ordosica. The climate there is generally characterized by extreme high temperature, strong sunlight, high evaporation, and erratic rainfall during the summer season [14]. The hottest month is July. All field work in this study was carried out in July 2022.

2.2. Vegetation Analysis

Vegetation surveys were conducted at three study sites. The size of the study site was 90 m × 60 m. A square of 5 m × 5 m was randomly sampled in the site to survey shrub communities. In addition, 3 squares of 1 m × 1 m across the square for herbs were sampled to investigate herbaceous plants [35]. The height and coverage of the plants were measured using a metric tap (to 1 mm). Plant species were identified by their morphologies.

2.3. Rodent Surveys

Rodents were captured using animal live traps [32]. In total, 50 wire-mesh traps (28 cm × 13 cm × 10 cm) were placed at each study site with 2–3 m spacing between traps. They were located close to rodent burrows or where there were animal tracks, such as rodent footprints or feces. For traps not under vegetation, a shade area was created with Salix cheilophila branches and leaves to protect the animals from excessive exposure to sunlight. All traps were set at 6 p.m. with peanuts as bait. The trap was triggered when the rodent ate the bait. All traps were checked on 2 consecutive days at 6 a.m., 12 a.m., and 6 p.m. All captured rodents were placed separately in a clear plastic box (43 cm × 34 cm × 30 cm) to record their body mass and morphology. The species of each rodent was identified based on characteristic morphological features. Finally, all rodents were released at the place where they were caught.

2.4. Determination and Analysis of Ambient Temperature

Near-surface ambient temperatures at the study sites were determined daily and at various heights over a period of two weeks. Ambient temperatures at 50 cm, 5 cm, and 0 cm above the ground (T50cm, T5cm, and T0cm) were measured using temperature loggers (RC-4, Elitech, Xuzhou, China). The ambient temperatures were recorded every 15 min. The data obtained were used for further analysis when the weather conditions were sunny and clear for 36 consecutive hours. The ambient temperature extremes were calculated by averaging 3 consecutive maximum or minimum ambient temperatures over a 24 h period.
At the same time, the desert surface temperature was measured with an infrared thermal imager (C200 Pro, InfiRay, Yantai, China) and temperature logger. The ratio of the desert surface temperature under vegetation (TUV) extremes to the desert surface temperature with no vegetation (TNV) extremes was used to measure the effect of vegetation cover on desert surface temperature. Moreover, correlations between T5cm, TNV, and TUV were evaluated by simple linear regression analysis.
Ambient temperatures inside the burrow (Tburrow) were measured using temperature loggers. The temperature probe was placed at a depth of 15 cm from the desert surface, 20 cm away from the opening of the rodent burrow. The depth of the temperature probe was determined by averaging the 10 rodent burrows surveyed in the field. In addition, to understand the ambient temperature characteristics of the rodent burrow, desert soil temperatures were measured with a digital thermometer (TES-1310, TES Electrical Electronic Corp., Taipei, China).
Linear regression analysis was performed to assess the linearity between air temperature (Tair) and T50cm, T5cm, and T0cm, and TUV. Tair data were obtained from the official website (www.nmc.cn, accessed on 29 July 2022). The mean values of Shenmu and Ejin Horo Banner Tair were used in this study.

2.5. Determination of the Extreme Heat

Extreme heat was determined by the thermoneutral zone (TNZ) of the rodents [31]. The M. unguiculatus has a TNZ of 26 to 38 °C [24]. Therefore, the species was experiencing extreme heat when the ambient temperature was above 38 °C. In addition, the TNZ of the M. meridianus ranges from 25.5 to 30.1 °C [27]. This species was experiencing extreme heat when the ambient temperature was greater than 30.1 °C.

2.6. Statistical Analyses

All statistical analyses were performed using IBM SPSS.v.20.0 software. Plant heights, the difference between ambient temperature extremes and Tair extremes, the ratio of TUV extremes/TNV extremes, and the ratio of Tburrow extremes/T0cm extremes were provided as mean ± SD. The general linear model was used to regress measures of ambient temperature against Tair. Differences in other indicators between 2 groups were analyzed using the independent sample t-test. p values of less than 0.5 were considered statistically significant.

3. Results

3.1. Plant Species, Height, and Coverage

The plant species recorded at each site are shown in Table 1. In site 1, the vegetation coverage was 40.82%. Salix cheilophila was the major species, with a height of 1.904 ± 0.256 m and coverage of 40.44%. A small amount of Artemisia ordosica was found, with a height of 0.7 m and coverage of 0.38%. In site 2, the vegetation coverage was 33.53%. Caragana intermedia was the major species, with a height of 1.625 ± 0.178 m and coverage of 22.17%. Artemisia ordosica was the minor species, with a height of 0.535 ± 0.176 m and coverage of 11.36%. A small amount of Cynanchum thesioides was distributed in the interspace of shrubs. In site 3, the vegetation coverage was 36.67%. Artemisia ordosica was the minor species, with a height of 0.610 ± 0.188 and coverage of 26.40%. Caragana intermedia was the minor species, with a height of 1.165 ± 0.191 and coverage of 7.85%. Amygdalus pedunculata was another minor species, with a height of 0.700 ± 0.100 and coverage of 2.42%. There were also small amounts of Cynanchum thesioides and Psammochloa villosa mixed among the bushes.

3.2. Small Mammals Living in the Study Area

Mongolian gerbil, Long-tailed hamster, and Midday gerbil were found in the study area (Figure 2). No animals were captured at site 1. Three Midday gerbils and two Long-tailed hamsters were captured at site 2. Two Mongolian gerbils, two Midday gerbils, and one Long-tailed hamster were captured at site 3. All rodents were captured before 6 a.m.

3.3. Ambient Temperature Variation in Near-Surface Space

The daily changes in near-surface ambient temperatures are shown in Figure 3a–c. The near-surface ambient temperatures decreased during the night. They started to increase after sunrise and reach a maximum between 1 and 3 pm. Compared to the Tair from the official website, the near-surface ambient temperatures were lower at night (Figure 3d–f). The difference between the lowest T50cm, T5cm, and T0cm and the lowest Tair were −2.5 °C, −3.3 °C, and −3.5 °C, respectively (Figure 3d). In contrast, during the day, the near-surface temperatures were higher and showed a greater variation (Figure 3d–f). The difference between the highest T50cm, T5cm, and T0cm and the highest Tair were 6.1 °C, 10.17 °C, and 29.6 °C, respectively (Figure 3e,f).

3.4. Effect of Vegetation on Desert Surface Temperature

Vegetation cover had a regulatory function of desert surface temperature (Figure 4a,b). At night, the ratio of the lowest TUV to the lowest TNV was 1.07–1.30 (Figure 4c). During the day, the ratio of the highest TUV to the highest TNV was 0.65–0.69 (Figure 4c). Linear regression between T5cm and TNV and TUV (TNV, Y = 1.763x – 13.79, R2 = 0.9673; TUV, Y = 0.805x + 5.456, R2 = 0.9144) were performed (Figure 4d). Vegetation cover regulated the desert surface temperature and brought it close to T5cm.

3.5. Linear Relationship between Tair and Near-Surface Ambient Temperature

There was a positive linear relationship between Tair and T50cm (Y = 1.438x – 9.564, R2 = 0.8397), T5cm (Y = 1.729x – 15.64, R2 = 0.7931), T0cm (Y = 3.034x – 41.03, R2 = 0.7819), and TUV (Y = 1.516x – 10.13, R2 = 0.8723) (Figure 5). Near-surface ambient temperature could be predicted from the linear regression function with Tair.

3.6. Ambient Temperature in Rodent Burrow

The daily changes in ambient temperature on the desert surface and in the rodent burrow are shown in Figure 6a. At night, the ratio of the lowest Tburrow to the lowest T0cm was 1.35–1.66 (Figure 6b). During the day, the ratio of the highest Tburrow to the highest T0cm was 0.47–0.49 (Figure 6b). Moreover, daily variations in desert soil temperature declined with increasing soil depth (Figure 6c). At 9 a.m. and 7 p.m., the effect of vegetation on the soil temperature was not significant at depths greater than 10 cm (Figure 6d,f). At 2 p.m., the difference in soil temperature due to vegetation cover was less than 2.3 °C at depths greater than 10 cm (Figure 6e).

3.7. Distribution of Extreme Heat

The distribution of extreme heat in the study area over the day is shown in Figure 7. For M. unguiculatus, extreme heat persisted from 11:45 a.m. to 3:45 p.m. at 5 cm from the ground. On the desert surface, the extreme heat lasted from 9:15 a.m. to 6:30 p.m. On the vegetation-covered desert surface, the extreme heat continued from 12:00 a.m. to 4:00 p.m. In the burrow, no extreme heat was measured. In addition, for M. meridianus, extreme heat persisted from 9:15 a.m. to 6:30 p.m. at 5 cm from the ground. On the desert surface, the extreme heat lasted from 8:15 a.m. to 7:00 p.m. On the vegetation-covered desert surface, the extreme heat continued from 10:00 a.m. to 6:30 p.m. In the burrow, no extreme heat was measured.

4. Discussion

Rodents inhabiting the Mu Us Desert were influenced by extreme heat events during the summer. Ambient temperatures in the near-surface space showed a clear variance within small scales due to the vegetation cover and burrow system. Moreover, high temperatures beyond thermal tolerance limits were detected in the near-surface space frequented by rodents.

4.1. Vegetation Coverage and Rodent Species in the Mu Us Desert

Desert vegetation provides rodents with a habitat and the resources they need to survive. Our study showed that the vegetation coverage in the study area is 33.5–40.8%. The vegetation was composed of shrubs dominated by Salix cheilophila, Caragana intermedia, and Artemisia ordosica and a small number of herbaceous plants. Moreover, the vegetation cover in most areas of the Mu Us Desert has increased rapidly in the last 30 years, driven by both climate change and human activities [12,17,35]. Climate change may alter the seasonal temperature and precipitation patterns. Studies have shown an increasing trend in precipitation and temperature in northwest China [36,37,38], which will likely favor desert vegetation restoration. In addition, human activities, such as fencing and vegetation construction, are important forces of desert vegetation rehabilitation [39,40]. In conclusion, future trends in the vegetation coverage of the Mu Us Desert may be favorable for rodent survival.
The Mu Us Desert is a habitat for many species of rodents. In the present study, M. meridianus, M. unguiculatus, and C. longicaudatus were found. However, our data do not provide a full picture of the rodent species in this desert. In fact, Phodopus roborovskii, Cricetulus barabensis, Allactaga sibirica, and Spermophilus dauricus also live there [20,41]. In addition, no rodents were caught in simple Salix cheilophila-dominated habitats, while 10 rodents were caught in Caragana intermedia- and Artemisia ordosica-dominated habitats. This may indicate that, together with vegetation coverage, the increased plant species in the habitat also favor the survival of rodents [42]. Moreover, the number of rodents captured in this study was quite low. It is hard to provide effective information on population density. Yet, rodents of all 3 species were captured before 6 am, suggesting that relationships among rodent species may be affected in the face of the combined pressures of climate change and habitat modification [43]. Taken together, although the trends in the vegetation cover of the Mu Us Desert are positive for rodents, changes in the rodent population density and interspecific relationships require further study.

4.2. Temperature Variation of Near-Surface Space in Summer

Extreme heat in the summer is becoming more frequent, longer lasting, and hotter. Evidence can be seen from both climate model predictions and weather station detections [6]. Although the temperature data from weather stations differ from the real ambient temperatures experienced by rodents, data from nearby weather stations can be used to further predict the ambient temperatures in rodent habitats. In this study, we found a significant difference between the near-surface ambient temperature and data from the official website (Tair). The daily maximum Tair was 10.2 °C lower than T5cm and 29.6 °C lower than the desert surface temperature (T0cm) in July 2022. Moreover, a linear relation between Tair and the near-surface ambient temperature was established. These results indicated that the extreme heat experienced by desert rodents in summer was likely underestimated.
In the Mu Us Desert, the vegetation cover and burrow system are effective in regulating the temperature surrounding rodents. In the present study, the vegetation cover reduced the maximum daily desert surface temperature to 65 percent, whereas it had little effect on the air temperature near the desert surface. In addition, the daily maximum temperature in the rodent burrow was 47% of the desert surface temperature. It had a good insulation function at night. However, the study presented measured temperature changes at a depth of 15 cm in the burrow alone. In fact, the structure of rodent burrows is complex. The temperature environment in the burrows is also very diverse. Further research is needed on the role of burrows in rodent summer heat adaptation.

4.3. Strategies for Rodent Response to Summer Heat

TNZ is defined as a range of ambient temperature, at which the metabolic rate is at basal or resting levels [44]. This concept provides us with a lot of information on the ability of species to survive in different ambient temperatures. Rodents will be faced with severe physical and physiological limitations when the ambient temperature is above the TNZ. Here, the concept of the TNZ was used to analyze whether rodents experience heat stress during the summer. M. unguiculatus exhibits a wide TNZ, and its upper critical temperature is 38 ± 1 °C [21,22,24]. Moreover, this species is able to survive for the long term at 37 °C [23,45]. In contrast, the range of the TNZ in M. meridianus is only 38.3% of that in M. unguiculatus, and the upper critical temperature is 30.1 °C. In brief, the small desert rodents vary widely in their sensitivity and regulatory limits to variations in ambient temperature [31].
Desert surface temperature, air temperature near the desert surface, and Tburrow may reflect the true temperature experienced by small desert rodents. In the study area, the maximum desert surface temperature was 61.8 °C, with a diurnal temperature difference of 46.1 °C. The maximum air temperature near the desert surface was 41.3 °C, with a diurnal temperature difference of 26.2 °C. In contrast, the maximum Tburrow was 31 °C, with a diurnal temperature difference of 7.5 °C. Furthermore, outside the burrows, both M. meridianus and M. unguiculatus were at risk from extreme summer heat. Therefore, summer in the Mu Us Desert is a season of stress and survival for rodents, but burrows may provide them with a place to escape the extreme heat.

5. Conclusions

Climate change is changing the pattern of distribution of extreme summer heat in the Mu Us Desert. The evidence suggested that both M. meridianus and M. unguiculatus living in the southeastern Mu Us Desert were affected by extreme summer heat. This also implies that the behavior, physiology, and interspecies relationships of rodents in this region are expected to change significantly in the near future. Furthermore, burrows can help rodents escape the stress of summer heat, suggesting that, at least in the present study, desert rodents may respond to increased summer heat extremes primarily through behavioral adjustments.

Author Contributions

Conceptualization, Y.-Y.G. and D.X.; methodology, Y.-Y.G.; software, Y.-Y.G.; formal analysis, Y.-Y.G.; investigation, Y.-Y.G. and S.-S.W.; data curation, S.-S.W. and X.W.; writing—original draft preparation, Y.-Y.G.; writing—review and editing, W.L. and D.X. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Natural Science Youth Foundation of Shandong Province (Grant No. ZR2021QC223) and the Young Talents Invitation Program of Shandong Provincial Colleges and Universities.

Institutional Review Board Statement

The animal study protocol was approved by the Bioethics Committee of Qufu Normal University (protocol code 2022085, May 2022).

Informed Consent Statement

Not applicable.

Data Availability Statement

The data used in this study are available from the first author upon reasonable request.

Acknowledgments

We gratefully acknowledge Dehua Wang for his support and valuable advice.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Stillman, J.H. Heat waves, the new normal: Summertime temperature extremes will impact animals, ecosystems, and human communities. Physiology 2019, 34, 86–100. [Google Scholar] [CrossRef]
  2. Khaliq, I.; Hof, C.; Prinzinger, R.; Böhning-Gaese, K.; Pfenninger, M. Global variation in thermal tolerances and vulnerability of endotherms to climate change. Proc. R. Soc. B Biol. Sci. 2014, 281, 20141097. [Google Scholar] [CrossRef] [Green Version]
  3. Lu, R.; Xu, K.; Chen, R.; Chen, W.; Li, F.; Lv, C. Heat waves in summer 2022 and increasing concern regarding heat waves in general. Atmos. Ocean. Sci. Lett. 2023, 16, 100290. [Google Scholar] [CrossRef]
  4. Morit, A. Extreme heatwaves: Surprising lessons from the record warmth. Nature 2022, 608, 464–465. [Google Scholar]
  5. Rousi, E.; Kornhuber, K.; Beobide-Arsuaga, G.; Luo, F.; Coumou, D. Accelerated western European heatwave trends linked to more-persistent double jets over Eurasia. Nat. Commun. 2022, 13, 3851. [Google Scholar] [CrossRef]
  6. Fischer, E.M.; Sippel, S.; Knutti, R. Increasing probability of record-shattering climate extremes. Nat. Clim. Chang. 2021, 11, 689–695. [Google Scholar] [CrossRef]
  7. Terrien, J.; Perret, M.; Aujard, F. Behavioral thermoregulation in mammals: A review. Front. Biosci.-Landmark 2011, 16, 1428–1444. [Google Scholar] [CrossRef] [Green Version]
  8. Mota-Rojas, D.; Titto, C.G.; Orihuela, A.; Martínez-Burnes, J.; Gómez-Prado, J.; Torres-Bernal, F.; Flores-Padilla, K.; Fuente, V.C.; Wang, D. Physiological and behavioral mechanisms of thermoregulation in mammals. Animals 2021, 11, 1733. [Google Scholar] [CrossRef]
  9. Sareh, H.; Tulapurkar, M.E.; Shah, N.G.; Singh, I.S.; Hasday, J.D. Response of mice to continuous 5-day passive hyperthermia resembles human heat acclimation. Cell Stress Chaperones 2011, 16, 297–307. [Google Scholar] [CrossRef] [Green Version]
  10. Sawka, M.N.; Wenger, C.B.; Pandolf, K.B. Thermoregulatory responses to acute exercise-heat stress and heat acclimation. Compr. Physiol. 2010, 157–185. [Google Scholar] [CrossRef]
  11. Horowitz, M. From molecular and cellular to integrative heat defense during exposure to chronic heat. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2002, 131, 475–483. [Google Scholar] [CrossRef]
  12. Sun, Z.; Mao, Z.; Yang, L.; Liu, Z.; Han, J.; Wanag, H.; He, W. Impacts of climate change and afforestation on vegetation dynamic in the Mu Us Desert, China. Ecol. Indic. 2021, 129, 108020. [Google Scholar] [CrossRef]
  13. Wang, X.; Chen, F.H.; Dong, Z.; Xia, D. Evolution of the southern Mu Us Desert in North China over the past 50 years: An analysis using proxies of human activity and climate parameters. Land Degrad. Dev. 2005, 16, 351–366. [Google Scholar] [CrossRef]
  14. Zhang, D.; Deng, H. Historical human activities accelerated climate-driven desertification in China’s Mu Us Desert. Sci. Total Environ. 2020, 708, 134771. [Google Scholar] [CrossRef]
  15. Zhang, M.; Wang, K.; Liu, H.; Zhang, C.; Yue, Y.; Qi, X. Effect of ecological engineering projects on ecosystem services in a karst region: A case study of northwest Guangxi, China. J. Clean. Prod. 2018, 183, 831–842. [Google Scholar] [CrossRef]
  16. Li, X.; Ren, G.; Wang, S.; You, Q.; Sun, Y.; Ma, Y.; Wang, D.; Zhang, W. Change in the heatwave statistical characteristics over China during the climate warming slowdown. Atmos. Res. 2021, 247, 105152. [Google Scholar] [CrossRef]
  17. Wang, X.; Cheng, H.; Li, H.; Lou, J.; Hua, T.; Liu, W.; Jiao, L.; Ma, W.; Li, D.; Zhu, B. Key driving forces of desertification in the Mu Us Desert, China. Sci. Rep. 2017, 7, 3933. [Google Scholar] [CrossRef] [Green Version]
  18. Li, S.; Wang, T.; Yan, C. Assessing the role of policies on land-use/cover change from 1965 to 2015 in the Mu Us Sandy Land, northern China. Sustainability 2017, 9, 1164. [Google Scholar] [CrossRef] [Green Version]
  19. Wang, T.; Wu, W.; Xue, X.; Zhang, W.M.; Han, Z.W.; Sun, Q.W. Time-space evolution of desertification land in northern China. J. Desert Res. 2003, 23, 230. [Google Scholar]
  20. Limin, W.; Yanlin, Z.; Lijun, Z. Component analysing for rodents of Erdos plateau sandland. Acta Sci. Nat. Univ. Neimonggol (Nat. Sci. Ed.) 1999, 30, 377–379. [Google Scholar]
  21. Robinson, P.F. Metabolism of the Gerbil, Meriones unguiculatus. Science 1959, 130, 502–503. [Google Scholar] [CrossRef]
  22. Pan, Q.; Li, M.; Shi, Y.L.; Liu, H.; Speakman, J.R.; Wang, D.H. Lipidomics reveals mitochondrial membrane remodeling associated with acute thermoregulation in a rodent with a wide thermoneutral zone. Lipids 2014, 49, 715–730. [Google Scholar] [CrossRef]
  23. Guo, Y.Y.; Hao, S.; Zhang, M.; Zhang, X.; Wang, D. Aquaporins, evaporative water loss and thermoregulation in heat-acclimated Mongolian gerbils (Meriones unguiculatus). J. Therm. Biol. 2020, 91, 102641. [Google Scholar] [CrossRef]
  24. Wang, D.; Wang, Y.; Wang, Z. Metabolism and thermoregulation in the Mongolian gerbil Meriones unguiculatus. Acta Theriol. 2000, 45, 183–192. [Google Scholar] [CrossRef] [Green Version]
  25. Xu, M.M.; Wang, D.H. Water deprivation up-regulates urine osmolality and renal aquaporin 2 in Mongolian gerbils (Meriones unguiculatus). Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2016, 194, 37–44. [Google Scholar] [CrossRef]
  26. Agren, G.; Zhong, W.; Zhou, Q. Activity pattern in Mongolian gerbils (Meriones unguiculatus) in summer. In Reports from the Inner Mongolia Grassland Ecosystem Research Station of Academia Sinica (1979–1988); Yu, B., Peng, K.L., Eds.; Science Press: Beijing, China, 1990; pp. 239–246. [Google Scholar]
  27. Ding, B.Y.; Chi, Q.S.; Liu, W.; Shi, Y.L.; Wang, D.H. Thermal biology of two sympatric gerbil species: The physiological basis of temporal partitioning. J. Therm. Biol. 2018, 74, 241–248. [Google Scholar] [CrossRef]
  28. Kai, S.O.N.G.; Rongtang, L.I.U. The ecology of midday gerbil (Meriones meridianus Pallas). Acta Theriol. Sin. 2011, 4, 291. [Google Scholar]
  29. Lebedev, V.S.; Maslova, N.S.; Lisenkova, A.A.; Bannikova, A.A.; Sheftel, B.I.; Feoktystova, N.Y.; Qu, J.; Zhu, Y.; Fang, Y.; Sun, Y.; et al. Phylogeographic pattern and Pleistocene range reconstruction in the long-tailed hamster Cricetulus longicaudatus (Rodentia, Cricetidae) support its Tibetan origin. Mammal Res. 2021, 66, 635–648. [Google Scholar] [CrossRef]
  30. Giraudoux, P.; Quéré, J.P.; Delattre, P.; Bao, G.; Wang, X.; Shi, D.; Vuitton, D.; Craig, P.S. Distribution of small mammals along a deforestation gradient in southern Gansu, central China. Acta Theriol. 1998, 43, 349–362. [Google Scholar] [CrossRef] [Green Version]
  31. Gordon, C.J. Thermal physiology of laboratory mice: Defining thermoneutrality. J. Therm. Biol. 2012, 37, 654–685. [Google Scholar] [CrossRef]
  32. Liu, W.; Wan, X.; Zhong, W. Population dynamics of the Mongolian gerbils: Seasonal patterns and interactions among density, reproduction and climate. J. Arid Environ. 2007, 68, 383–397. [Google Scholar] [CrossRef]
  33. Zhao, Z.J.; Cao, J.; Meng, X.L.; Li, Y.B. Seasonal variations in metabolism and thermoregulation in the striped hamster (Cricetulus barabensis). J. Therm. Biol. 2010, 35, 52–57. [Google Scholar] [CrossRef]
  34. Zhan, X.M.; Wang, D.H. Energy metabolism and thermoregulation of the desert hamster (Phodopus roborovskii) in hunshandake desert of inner mongolia, China. Acta Theriol. Sin. 2004, 24, 152–159. [Google Scholar]
  35. Guo, Z.C.; Wang, T.; Liu, S.L.; Kang, W.P.; Chen, X.; Feng, K.; Zhang, X.; Zhi, Y. Biomass and vegetation coverage survey in the Mu Us sandy land-based on unmanned aerial vehicle RGB images. Int. J. Appl. Earth Obs. Geoinf. 2021, 94, 102239. [Google Scholar] [CrossRef]
  36. Chen, F.; Chen, J.; Huang, W. Weakened East Asian summer monsoon triggers increased precipitation in Northwest China. Sci. China Earth Sci. 2021, 64, 835–837. [Google Scholar] [CrossRef]
  37. Li, B.; Chen, Y.; Chen, Z.; Xiong, H.; Lian, L. Why does precipitation in northwest China show a significant increasing trend from 1960 to 2010? Atmos. Res. 2016, 167, 275–284. [Google Scholar] [CrossRef]
  38. Yang, P.; Xia, J.; Zhang, Y.; Hong, S. Temporal and spatial variations of precipitation in Northwest China during 1960–2013. Atmos. Res. 2017, 183, 283–295. [Google Scholar] [CrossRef]
  39. Huang, S.; Zheng, X.; Ma, L.; Wang, H.; Huang, Q.; Leng, G.; Meng, E.; Guo, Y. Quantitative contribution of climate change and human activities to vegetation cover variations based on GA-SVM model. J. Hydrol. 2020, 584, 124687. [Google Scholar] [CrossRef]
  40. Liu, Q.; Zhang, Q.; Yan, Y.; Zhang, X.; Niu, J.; Svenning, J.C. Ecological restoration is the dominant driver of the recent reversal of desertification in the Mu Us Desert (China). J. Clean. Prod. 2020, 268, 122241. [Google Scholar] [CrossRef]
  41. Wilson, D.E.; Reeder, D.M. Mammal Species of the World. In Rodentia; Johns Hopkins University Press: Baltimore, MD, USA, 2005. [Google Scholar]
  42. Liu, W.; Deng, K. Population Dynamics of Wild Mongolian Gerbils: Quadratic Temperature Effects on Survival and Density-Dependent Effects on Recruitment. Diversity 2022, 14, 586. [Google Scholar] [CrossRef]
  43. Scheibler, E.; Wollnik, F.; Brodbeck, D.; Hummel, E.; Yuan, S.; Zhang, F.S.; Zhang, X.D.; Fu, H.P.; Wu, X.D. Species composition and interspecific behavior affects activity pattern of free-living desert hamsters in the Alashan Desert. J. Mammal. 2013, 94, 448–458. [Google Scholar] [CrossRef]
  44. Commission, I.T. Glossary of terms for thermal physiology. Jpn. J. Physiol. 2001, 51, 245–280. [Google Scholar]
  45. Guo, Y.Y.; Chi, Q.S.; Zhang, X.Y.; Liu, W.; Hao, S.Y.; Wang, D.H. Brown adipose tissue plays thermoregulatory role within the thermoneutral zone in Mongolian gerbils (Meriones unguiculatus). J. Therm. Biol. 2019, 81, 137–145. [Google Scholar] [CrossRef]
Animals 13 02114 g001 550
Figure 1. Location of the study area, Shenmu County, China. The red graph in the upper right of the figure, the location of Shenmu City.
Figure 1. Location of the study area, Shenmu County, China. The red graph in the upper right of the figure, the location of Shenmu City.
Animals 13 02114 g001
Animals 13 02114 g002 550
Figure 2. Rodents captured in the study area. (a) Midday gerbils; (b) Mongolian gerbils; (c) Long-tailed hamsters. All captured rodents were found during the 6 am checks.
Figure 2. Rodents captured in the study area. (a) Midday gerbils; (b) Mongolian gerbils; (c) Long-tailed hamsters. All captured rodents were found during the 6 am checks.
Animals 13 02114 g002
Animals 13 02114 g003 550
Figure 3. Near-surface ambient temperature variation. (a–c) Changes in near-surface ambient temperature at 3 study sites (measured on different dates) over 24 h; (d–f) The difference (mean ± SD) between ambient temperature extremes (n = 3) and Tair extremes. Txcm (x = 50, 5, 0), ambient temperature measured at x cm above the ground; Tair, air temperature from the official website.
Figure 3. Near-surface ambient temperature variation. (a–c) Changes in near-surface ambient temperature at 3 study sites (measured on different dates) over 24 h; (d–f) The difference (mean ± SD) between ambient temperature extremes (n = 3) and Tair extremes. Txcm (x = 50, 5, 0), ambient temperature measured at x cm above the ground; Tair, air temperature from the official website.
Animals 13 02114 g003
Animals 13 02114 g004 550
Figure 4. The influence of vegetation cover on desert surface temperature. (a) Desert surface temperature recorded by an infrared thermal imager. (b) Diurnal variation of desert surface temperature at three study sites. (c) Ratio (mean ± SD, n = 3) of TUV extremes/TNV extremes. (d) Linear regression between T5cm and TNV and TUV (TNV, Y = 1.763x – 13.79, R2 = 0.9673; TUV, Y = 0.805x + 5.456, R2 = 0.9144). S1–3, site 1–3. TNV, desert surface temperature without vegetation; TUV, desert surface temperature under vegetation; T5cm, ambient temperature measured at 5 cm above the ground.
Figure 4. The influence of vegetation cover on desert surface temperature. (a) Desert surface temperature recorded by an infrared thermal imager. (b) Diurnal variation of desert surface temperature at three study sites. (c) Ratio (mean ± SD, n = 3) of TUV extremes/TNV extremes. (d) Linear regression between T5cm and TNV and TUV (TNV, Y = 1.763x – 13.79, R2 = 0.9673; TUV, Y = 0.805x + 5.456, R2 = 0.9144). S1–3, site 1–3. TNV, desert surface temperature without vegetation; TUV, desert surface temperature under vegetation; T5cm, ambient temperature measured at 5 cm above the ground.
Animals 13 02114 g004
Animals 13 02114 g005 550
Figure 5. Linear regression between Tair and T50cm (a), T5cm (b), T0cm (c), and TUV (d). Tair, air temperature from the official website; Txcm (x = 50, 5, 0), ambient temperature measured at x cm above the ground; TUV, desert surface temperature under vegetation.
Figure 5. Linear regression between Tair and T50cm (a), T5cm (b), T0cm (c), and TUV (d). Tair, air temperature from the official website; Txcm (x = 50, 5, 0), ambient temperature measured at x cm above the ground; TUV, desert surface temperature under vegetation.
Animals 13 02114 g005
Animals 13 02114 g006a 550Animals 13 02114 g006b 550
Figure 6. Rodent burrow regulation of ambient temperature. (a) Diurnal variation in ambient temperature on the desert surface and in rodent burrows. (b) Ratio (mean ± SD, n = 3) of Tburrow extremes/T0cm extremes. (c) Variation of desert soil temperature with depth at different times of the day. (d–f) Effect of vegetation cover on desert soil temperature (mean ± SD, n = 3) during the day. S1–3, site 1–3. T9am, T2pm, and T7pm desert soil temperature measured at 9 a.m., 2 p.m., and 7 p.m. Tburrow, ambient temperature inside the burrow; T0cm, ambient temperature measured at 0 cm above the ground. Statistical significance is indicated by asterisks.
Figure 6. Rodent burrow regulation of ambient temperature. (a) Diurnal variation in ambient temperature on the desert surface and in rodent burrows. (b) Ratio (mean ± SD, n = 3) of Tburrow extremes/T0cm extremes. (c) Variation of desert soil temperature with depth at different times of the day. (d–f) Effect of vegetation cover on desert soil temperature (mean ± SD, n = 3) during the day. S1–3, site 1–3. T9am, T2pm, and T7pm desert soil temperature measured at 9 a.m., 2 p.m., and 7 p.m. Tburrow, ambient temperature inside the burrow; T0cm, ambient temperature measured at 0 cm above the ground. Statistical significance is indicated by asterisks.
Animals 13 02114 g006aAnimals 13 02114 g006b
Animals 13 02114 g007 550
Figure 7. Distribution of extreme heat in time and space within a day. (a) Extreme heat determined by the upper critical temperature (UCT) of the TNZ in M. unguiculatus. (b) Extreme heat determined by the UCT of the TNZ in M. meridianus. T0cm and T5cm ambient temperature measured at 0 cm and 5 cm above the ground. TUV, desert surface temperature under vegetation; Tburrow, ambient temperature inside the burrow; M. unguiculatus, Meriones unguiculatus; M. meridianus, Meriones meridianus.
Figure 7. Distribution of extreme heat in time and space within a day. (a) Extreme heat determined by the upper critical temperature (UCT) of the TNZ in M. unguiculatus. (b) Extreme heat determined by the UCT of the TNZ in M. meridianus. T0cm and T5cm ambient temperature measured at 0 cm and 5 cm above the ground. TUV, desert surface temperature under vegetation; Tburrow, ambient temperature inside the burrow; M. unguiculatus, Meriones unguiculatus; M. meridianus, Meriones meridianus.
Animals 13 02114 g007
Table
Table 1. Plant species, height, and coverage in the Mu Us Desert.
Table 1. Plant species, height, and coverage in the Mu Us Desert.
Study SiteScientific NamePlant Height (m)Plant Coverage (%)
Site 1Salix cheilophila1.904 ± 0.25640.44
Artemisia ordosica0.70.38
Site 2Caragana intermedia1.625 ± 0.17822.17
Artemisia ordosica0.535 ± 0.17611.36
Cynanchum thesioides--
Site 3Artemisia ordosica0.610 ± 0.18826.40
Caragana intermedia1.165 ± 0.1917.85
Amygdalus pedunculata Pall.0.700 ± 0.1002.42
Cynanchum thesioides--
Psammochloa villosa--
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Guo, Y.-Y.; Wang, S.-S.; Wang, X.; Liu, W.; Xu, D. Rodents Inhabiting the Southeastern Mu Us Desert May Not Have Experienced Prolonged Heat Stress in Summer 2022. Animals 2023, 13, 2114. https://doi.org/10.3390/ani13132114

AMA Style

Guo Y-Y, Wang S-S, Wang X, Liu W, Xu D. Rodents Inhabiting the Southeastern Mu Us Desert May Not Have Experienced Prolonged Heat Stress in Summer 2022. Animals. 2023; 13(13):2114. https://doi.org/10.3390/ani13132114

Chicago/Turabian Style

Guo, Yang-Yang, Shan-Shan Wang, Xinyue Wang, Wei Liu, and Deli Xu. 2023. "Rodents Inhabiting the Southeastern Mu Us Desert May Not Have Experienced Prolonged Heat Stress in Summer 2022" Animals 13, no. 13: 2114. https://doi.org/10.3390/ani13132114

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop