Hongxing JIANG, Fawen QIAN, Chunyue LIU, Xiaoming LI, Yunqiu HOU, Guogang ZHANG, Ming DAI, Dongping LIU. 2012: Impact of marsh changes on breeding cranes in Sanjiang Plain, northeastern China. Avian Research, 3(3): 165-179. DOI: 10.5122/cbirds.2012.0026
Citation: Hongxing JIANG, Fawen QIAN, Chunyue LIU, Xiaoming LI, Yunqiu HOU, Guogang ZHANG, Ming DAI, Dongping LIU. 2012: Impact of marsh changes on breeding cranes in Sanjiang Plain, northeastern China. Avian Research, 3(3): 165-179. DOI: 10.5122/cbirds.2012.0026

Impact of marsh changes on breeding cranes in Sanjiang Plain, northeastern China

More Information
  • In order to measure the impact of changes in the marsh on breeding Red-crowned Cranes (Grus japonensis) and White-naped Cranes (G. vipio) in the Sanjiang Plain, we conducted a complete crane survey in each of the summers of 2007 and 2008, and obtained information on the changes in its marsh through interpretation of satellite images in 1986, 1995, 2000 and 2005. A comparison between the 1984 and 2008 census shows that: 1) the number of Red-crowned Cranes remained stable at about 300 birds, while the number of White-naped Cranes increased markedly; 2) the estimates of nests of Red-crowned cranes are close to the numbers of 1984, while approximately 90% of the nests of these two crane species were distributed over five national nature reserves (NNRs); 3) the two crane species became more concentrated in three regions, i.e., the Fuyuan Delta, the middle reaches of the Naoli and Qixing rivers, and the Xingkai Lake wetlands, rather as formerly in six regions. The area of the marsh decreased by 45% within the 20-year period from 1986 to 2005. The major loss of the marsh area was in the form of a conversion to paddy fields and dry land, which can be primarily attributed to direct human activity under various economic and policy drivers. The disappearance of cranes in the Dulu and Abuqin rivers was induced by large-scale agricultural development. The fragmentation into and isolation of small areas of the marsh became increasingly more serious, which resulted in unsuitable condtions for crane breeding in small patches of the marsh. The number of cranes declined from 1984-1995 but had recovered remarkably by 2008, which may be due to the establishment of a system of nature reserves, in place since 2000. The land ownership of the reserve plays a key role in maintaining the integrity of the wetland ecosystem, especially in Sanjiang, Honghe, Naolihe and Qixinghe NNRs, which together accommodated approximately 80% of the population of cranes. However, we did not discover any nests at all in the provincial and municipal reserves, which may be attributed to high human disturbances in these areas. In the end, we propose some recommendations on reserve management.

  • Abbreviations
    BMR basal metabolic rate
    EWL evaporative water loss
    TNZ thermal neutral zone
    Tb body temperature
    Ta ambient temperature
    Tlc lower critical temperature
    MWP metabolic water production
    Cdry dry thermal conductance

    Animal distributions are constrained by many environmental factors, such as ambient temperature and food availability (Pigot et al., 2010; Rezende and Bacigalupe, 2015). Temperate songbirds, especially residents, experience greater seasonal fluctuations in ambient temperature and food availability, so they evolve different survival strategies compared to their tropical counterparts. Many of morphological, physiological, and behavioral phenotypes of birds are related to their energy budgets (McNab, 2009). Anthropogenic climate change is recognized as one of the most important current threats to biodiversity (Thomas et al., 2004; McKechnie and Wolf, 2010; Milne et al., 2015), and it may result in the ranges of birds and other animals shifting towards higher latitudes and altitudes (Hickling et al., 2006; Sinervo et al., 2010; Tingley et al., 2012; Albright et al., 2017; Delgado-Suazo and Burrowes, 2022). Understory birds have relatively narrow thermal niches, so they suffer greater adverse consequences of climate change than birds in other tropical habitats (Visco et al., 2015).

    Energy is required for physiological and behavioral processes, and as such, it is critical for animals' survival (McNab, 2009). Measuring energy metabolism in different species provides insights into how organisms adapt to their environments (Barceló et al., 2016; Tapia-Monsalve et al., 2018), and it informs our understanding of life-history trade-offs and pacing (Glazier, 2015). Endotherms regulate their body temperatures in a relatively constant range by equilibrating their heat production and heat dissipation. Birds' adaptive strategies can be characterized using the levels of energy metabolism in the thermoregulation process, and plenty of comparative studies support the notion of adaptive variations in thermoregulatory performance in response to climatic conditions (McNab, 2009; Bozinovic et al., 2014; Rezende and Bacigalupe, 2015).

    Metabolic rate is the rate of energy uptake, transformation, and allocation, which in turn determines the rates of almost all biological processes, including growth, development, survival, reproduction, and even fitness (Brown et al., 2004; Clarke, 2006; Glazier, 2015; Rezende and Bacigalupe, 2015). Basal metabolic rate (BMR), which is usually determined via oxygen consumption in birds, is defined as the minimum energy expenditure allowing animal to maintain normal physiological function in awake, inactive, and post-absorptive conditions (McNab, 2009, 2012). Many factors affect BMR within and across species, including diet (Sabat et al., 2010; McNab, 2012; Barceló et al., 2016; Tapia-Monsalve et al., 2018), food abundance (McNab, 2009), ambient temperature (Rezende and Bacigalupe, 2015), body condition (Cooper, 2007; Rezende and Bacigalupe, 2015), among others (McNab, 2012; Rezende and Bacigalupe, 2015). Multiple lines of evidence show that tropical passerines usually have lower BMR than those from temperate areas, as the former need to reduce heat production to avoid hyperthermia (Swanson, 2010; Xia et al., 2013).

    Thermal constraints are often invoked to explain the distribution of animals, and since biomes differ in both their maximum and minimum temperatures, temperate and tropical species have evolved different thermal tolerances (McNab, 2009). The thermal neutral zone (TNZ) is a set of temperature limits that serve as an index for the optimum temperature range of an animal. When the air temperature is within the TNZ range, animals do not need to consume more energy to maintain homeostasis (Bozinovic et al., 2014). The TNZ is related to the ambient temperatures where an animal inhabits, and it varies among small birds, including within the same species in different seasons (Swanson, 2010; Riek and Geiser, 2013). Species that evolved in colder climates have wider TNZs than those in warm and tropical zones (Bozinovic et al., 2014). Species originating in tropical mountains have narrow thermal tolerance, so they have relatively narrow TNZs (Janzen, 1967; Polato et al., 2018). A bird species' thermal tolerance may constrain its geographic distribution (Khaliq et al., 2014).

    Body temperature regulation and water balance are closely related in birds (Manuel and Anna, 2018; Noakes and McKechnie, 2019). Water balance is essential for survival, and it experiences similar selective pressures to energy metabolism. This is especially true in birds from arid environments, where the lack of bodies of water means that it is important to get water from their food and produce it through their metabolism (Clement et al., 2012). Evaporative water loss (EWL) has been widely used as an indicator of economic water use in birds (Williams, 1999; Clement et al., 2012). EWL is often used to compare water use in small birds from different climatic regions in eco-physiological studies, and it has been found that species living in arid habitats exhibit lower total EWL than those in mesic habitats (Williams, 1999; Tieleman et al., 2002; Manuel and Anna, 2018).

    When multiple species live in the same region and habitat, similar selective pressures can result in them evolving similar phenotypes, including their thermogenesis traits (Rundell and Price, 2009; Bothwell et al., 2015). The White-browed Laughingthrush (Pterorhinus sannio), a widely distributed songbird, has historically been found in understory habitats in tropical and sub-tropical areas of East Asia. However, in recent years, the species has expanded northward and set up populations in the western and eastern edges of the Liupan Mountains (Fig. 1). This range shift has put it into overlap with its temperate congener, the Plain Laughingthrush (P. davidi; Cibois et al., 2018), a temperate zone Chinese endemic, which is the most northerly occurring laughingthrush and is broadly distributed in northern China (Liu and Sun, 2018). Why has the White-browed Laughingthrush been able to expand its distribution into temperate regions? Do P. sannio living in this new habitat exhibit similar thermogenic features to the temperate-evolved P. davidi? To answer these questions, the first step is to determine the thermogenic traits of the northwardly expanded P. sannio. Therefore, we compared thermoregulatory traits in northwardly colonized P. sannio with P. davidi and two other locally co-occurring species: the montane bird Elliot's Laughingthrush (Trochalopteron elliotii; Qu et al., 2011), and the Grey-capped Greenfinch (Chloris sinica). We predicted that P. sannio would have the lowest BMR and broadest TNZ of all four species due to its broad, low-latitude distribution. We also predicted that its TNZ would have a lower downstream critical temperature, similar to its temperate congener P. davidi, because the two species are experiencing similar selective pressures at our study site.

    Figure  1.  The new distribution sites found in recent years (filled circles) and historical distributions (filled triangles) of White-browed Laughingthrush (Pterorhinus sannio). The five-pointed star represents our study site. The species has been expanding northward in recent years.

    Our study site is located at Shuiluo village in Zhuanglang County, Gansu Province, Central China (35°19ʹ22″ N 106°11ʹ04″ E; 1640–2060 m a.s.l.), which is by the western edge of the Liupanshan Mountains, inland of the Loess Plateau with a semi-arid climate. Based on 20 years of meteorological data (2000–2019), the minimum temperature for this area is −17.8 ​℃, the maximum temperature is 32.1 ​℃, the annual mean temperature is 8.8 ​℃, the mean minimum temperature is 3.7 ​℃, the mean maximum temperature is 15.4 ​℃, the mean average precipitation is 529.1 ​mm, and the mean relative humidity is 67.8%. At our study site, P. davidi, P. sannio, C. sinica, and T. elliotii are very common and overlap in distribution, especially in the nursery sites of Chinese Pine (Pinus tabuliformis) in winter. Among these four resident species, P. davidi, P. sannio, and C. sinica usually share the same microhabitats (Liu and Sun, 2018), and T. elliotii stays in higher-mountain areas and descends to lower ground in winter, with both its breeding and wintering grounds close to water sources (Liu and Sun, 2016; Liu et al., 2021).

    Thirteen healthy adult males of P. sannio (average body weight: 59.45 ​± ​0.55 ​g) and 17 healthy adult males of P. davidi (average body weight: 49.91 ​± ​0.49 ​g) were captured in October 2020 with walk-in traps and mist-nets in the habitats of these two species at the study site. All captured birds were then transported to the Laboratory of Avian Physiology and Behavior, Longdong University (35°43ʹ45″ N 107°41ʹ03″ E, 1484 ​m a.s.l., at a distance of 165 ​km from the study site). Birds were kept individually in bamboo cages (diameter 35 ​cm ​× ​height 50 ​cm) for one week outdoors under natural conditions and fed commercial Hwamei (Garrulax canorus) pellets (≥18.0% crude protein, ≤ 10.0% crude ash content, ≤ 9.0% crude fiber, 0.6–1.8% calcium, ≥ 0.5% phosphrus, 0.1–0.8% sodium chloride, ≤ 14.0% water, and ≥0.3% methionine; Beijing Kaiyuan Feed Company LTD). Food and water were provided ad libitum. After the thermogenic features of these two species were measured, all birds were released into the wild at the capture site.

    In October 2021, 18 healthy adult males of T. elliotii (average body weight: 48.23 ​± ​0.38 ​g) and 20 healthy adult males of C. sinica (average body weight: 17.22 ​± ​0.13 ​g) were captured at the study site with mist-nets, and then all captured birds were transported to the Laboratory of Avian Physiology and Behavior, Longdong University. T. elliotii were kept individually in bamboo cages (diameter 35 ​cm ​× ​height 50 ​cm) for one week outdoors under natural conditions and fed like the first two laughingthrush species. C. sinica were kept individually in metal cages (length 25 ​cm ​× ​height 35 ​cm ​× ​width 28 ​cm), fed sunflower seeds and millet, and had ad libitum access to food and water. All these birds were released into wild at the capture sites after all physiological measurements were finished. The capture of birds in this study was approved by the Bureau of Forestry and Grassland of Zhuanglang County (Permission code 2020-02). All animal procedures complied with the local and national rules concerning the care and use of animal subjects and were approved by the Animal Care and Use Committee of Longdong University (2020005LU).

    One week after capture, the thermogenic features of all species were measured, including metabolic rate, body temperature (Tb) and EWL, under ambient temperatures (Ta) ranging from 0 to 40 ​℃. For each Ta, eight individuals from each species were randomly selected for measuring these parameters. Experiments in P. sannio and P. davidi began on 11 November 2020 and ended on 15 December 2020, and measurements in T. elliotii and C. sinica began on 14 November 2021 and ended on 19 December 2021.

    To measure the resting metabolic rate (RMR) and determine the TNZ, all randomly selected birds were fasted for 2 ​h before measurements (Karasov, 1990) to ensure that birds were post-absorptive. RMR was measured via oxygen consumption using a continuous flow respirometry system (FoxBox, Sable Systems, Las Vegas, NV, USA) using the standardized protocol (Jacobs and McKechnie, 2014; Whitfield et al., 2015). Individuals were placed in a plastic metabolic chamber (4.6 ​L for laughingthrushes and 2.4 ​L for greenfinches), which itself was placed in a temperature controlled (±0.5 ​℃) cabinet (Artificial climate engine RXM-80A, Ningbo Jiangnan Instrument Factory, China). Two ends of the chamber had air intakes and outlets to ensure that air was pumped through the chamber at a flow rate of 600 ​mL/min for laughingthrushes and 300 ​mL/min for greenfinches. Air temperature in the chamber was continuously measured with thermistor probes (Sable Systems, Las Vegas, NV, USA). The concentrations of O2 and CO2 were recorded every second for each bird over the course of 1 ​h at a given Ta, during the inactivity period of 1900–2300 ​h, local time. O2 consumption was calculated with the equation VO2 ​= ​60 ​× ​FR ​× ​(FiO2 ​− ​FeO2)/(1 ​− ​FeO2), with the selected lowest 5 ​min average O2 ppm readings subtracted from baseline values for each trial and each temperature (Smith et al., 2015). FR is the flow rate through the chamber (mL/min), and FiO2 and FeO2 are the fractional concentrations of O2 flow in and out of the metabolic chamber respectively (Barceló et al., 2016). Each bird was exposed to different Ta, which ranged from 0 to 40 ​℃, and every bird got measurements 5 ​℃ apart. The birds were taken from their cages, immediately placed in cloth bags, enand taken to the respirometry system lab. The chamber in which the birds were placed was completely dark, but we still monitored the birds with a video camera. During the measurement process, we noticed that 40 ​℃ was likely causing P. davidi and T. elliotii to overheat, as the birds constantly opened their beaks to cool down, so we abandoned these trials for both species. We obtained data from two birds per night over a 30-day period in each species.

    Once the O2 consumption was measured from 0 to 40 ​℃, RMR was computed and statistically analyzed. The temperature zone within which the RMR was lowest and not significantly different was determined as TNZ of the species. If RMRs under any two consecutive Ta were significantly different, the midpoint of these two was selected as a new Ta to measure O2 consumption and confirm the TNZ of the birds. The average RMR within the TNZ is the BMR of the species.

    During the RMR measurements, a mineral oil layer was placed at the bottom of the chamber to prevent evaporation from urine and feces. The birds perched on a plastic mesh platform 5 ​cm above the cotton layer. Two bottles (0.4 ​L) containing silica gel were connected to the air intake and outlet of the metabolic chamber, and the bottles were weighed (±0.1 ​mg) before and after each measurement. Because the air pumped into the chamber was dry, and the EWL of each bird was absorbed by the silica gel connected to the chamber's air outlets, we were able to calculate EWL with the equation EWL (mg/h) = (bottle weight after the experiment ​− ​bottle weight before the experiment)/time, where time was the duration of metabolic measurement (Zhu et al., 2010; Xia et al., 2013). Eight randomly selected individuals from each species were used to measure RMR and EWL at any given Ta.

    Body temperature (Tb, ±0.1 ​℃) of each bird was determined before and after each metabolic trial by inserting a digital thermometer (ALC-ET, Shanghai Alcott Biotech Co. LTD, China) into the cloaca of each bird to a depth of 2 ​cm in laughingthrushes and 1 ​cm in greenfinches. Body masses were determined using electrical balance (±0.01 ​g) both before and after each metabolic measurement.

    Thermal conductance [C, mL O2/(g·h·℃)] at any given ambient temperature (Ta) was calculated using the formula C ​= ​RMR/(Tb ​− ​Ta), and dry thermal conductance (Cdry) was calculated using the formula Cdry = (RMR ​− ​EWL)/(Tb ​− ​Ta). Here RMR is the metabolic rate [mL O2/(g·h)], Tb is the body temperature determined after metabolic measurement, Ta is the ambient temperature that was controlled by an artificial climate engine (Aschoff, 1981; Xia et al., 2013). Values of RMR were converted to energy expenditure using 20.09 ​J/mL O2, and values of EWL were converted to energy expenditure using 2.43 ​J/mg H2O (Xia et al., 2013).

    Metabolic water production (MWP) was estimated from the oxygen consumption values at any given Ta. Metabolic water was assumed to indicate energy expenditure at a conversion rate of 0.65 ​mg H2O/mL O2 (Williams, 1999; Xia et al., 2013).

    As eight individuals were randomly selected to measure thermogenic parameters in each species for each trial, we used a one-way analysis of covariance to test the effect of ambient temperature on RMR and EWL and a one-way analysis of variance (one-way ANOVA) to test the effect of ambient temperature on Tb, C, Cdry, and MWP/EWL. Multiple post-hoc comparisons were employed to determine the TNZ using the Duncan method in each species. Linear regressions were used to analyze the relationship between RMR and Ta, and between EWL and Ta. Exponential equation model were fit to analyze the relationship between C and Ta. All statistics were conducted in SPSS 20.0 for Windows. Results were expressed as mean ​± ​SE, with the significance level set as p < 0.05.

    RMR decreased when Ta was lower than 10 ​℃, and increased sharply when Ta was higher than 27.5 ​℃ in P. davidi. For P. sannio, RMR fell when Ta was below 15 ​℃ and increased when Ta was higher than 35 ​℃. For T. elliotii, RMR fell when Ta was below 25 ​℃ and increased when Ta was higher than 30 ​℃. RMR increased when the Ta was lower than 7.5 ​℃ or higher than 32.5 ​℃ in C. sinica (Fig. 2A).

    Figure  2.  Resting metabolic rate (A), body temperature (B), evaporative water loss (C), thermal conductance (D), dry thermal conductance (E) and the ratio of metabolic water production to evaporative water loss (F) measured in the Plain Laughingthrush (Pterorhinus davidi) (black), Elliot's Laughingthrush (Trochalopteron elliotii) (red), under the ambient temperature which ranged from 0 to 35 ℃; in the White-browed Laughingthrush (P. sannio) (green), and Grey-capped Greenfinch (Chloris sinica) (yellow) under the ambient temperature which ranged from 0 to 40 ℃. Results were presented as Mean ± Standard error.

    No significant linear correlation was found between oxygen consumption and Ta, when the Ta ranged from 10 ​℃ to 27.5 ​℃, 25–30 ​℃, 15–35 ​℃, and 7.5–32.5 ​℃ in P. davidi, T. elliotii, P. sannio, C. sinica, respectively (all p ​ > ​0.05; Fig. 2A), and RMR did not significantly differ within the temperature zone. Therefore, the TNZ was 10–27.5 ​℃, 25–30 ​℃, 15–35 ​℃, and 7.5–32.5 ​℃ in P. davidi, T. elliotii, P. sannio, and C. sinica, respectively. When Ta was lower than the lower critical temperature (Tlc), RMR increased with decreasing Ta linearly in all species. In P. davidi, RMR ​= ​216.46–0.145 Ta (R2 ​= ​0.521; p ​ < ​0.001; n ​= ​32); in T. elliotii, RMR ​= ​240.72–0.521 Ta (R2 ​= ​0.272; p ​ < ​0.001; n ​= ​56); in P. sannio, RMR ​= ​81.863–0.512 Ta (R2 ​= ​0.262; p ​= ​0.005; n ​= ​40), in C. sinica, RMR ​= ​102.38–0.475 Ta (R2 ​= ​0.225; p ​= ​0.016; n ​= ​24) respectively.

    Within the TNZ, the average RMR was 166.8 ​± ​13.7 ​mL O2/h (n ​= ​40), 116.5 ​± ​17.4 ​mL O2/h (n ​= ​40), 44.5 ​± ​3.9 ​mL O2/h (n ​= ​40), and 41.3 ​± ​0.14 ​mL O2/h (n ​= ​40) in P. davidi, T. elliotii, P. sannio and C. sinica respectively (Table 1). P. sannio has lowest BMR in three Laughingthrush species, while the P. davidi has the highest BMR in three Laughingthrush species.

    Table  1.  Thermoregulatory features in coexisting Plain Laughingthrush (Pterorhinus davidi), Elliot's Laughingthrush (Trochalopteron elliotii), White-browed Laughingthrush (P. sannio) and Grey-capped Greenfinch (Chloris sinica), measured in experimental facility in central China.
    Thermoregulatory parameters Pterorhinus davidi Trochalopteron elliotii Pterorhinus sannio Chloris sinica
    Body mass (g) 49.91 ± 0.49 48.23 ± 0.38 59.45 ± 0.55 17.22 ± 0.13
    Body temperature (℃) 41.7 ± 0.4 42.5 ± 0.1 41.7 ± 0.2 41.3 ± 0.14
    Basal metabolic rate (mL O2/h) 166.8 ± 13.7 116.5 ± 17.4 44.5 ± 3.9 41.3 ± 0.14
    Expectation ratio (% predicted) 114.8 72.1 22.5 83.5
    Minimal thermal conductance [mL O2/(g·h·℃)] 0.117 ± 0.01 0.112 ± 0.01 0.03 ± 0.01 0.14 ± 0.01
    Expectation ratio (% predicted) 120.6 117.9 34.5 89.7
    Values are given as Mean ± SE, and the expectation ratio of BMR and thermal conductance were predicted from the appropriate equation in Londoño et al. (2015) and Aschoff (1981) respectively. % predicted = (observed/predicted) × 100.
     | Show Table
    DownLoad: CSV

    The body temperature (Tb) of P. davidi increased significantly with Ta below 20 ​℃. When the Ta was higher than 20 ​℃ and lower than 35 ​℃, Tb maintained stably at 41.7 ​± ​0.4 ​℃ (n ​= ​32). However, when the Ta reached 35 ​℃, Tb increased to 43.1 ​± ​0.4 ​℃ (n ​= ​8). Average Tb was 38.1 ​± ​0.4 ​℃ (n ​= ​14) at the Ta of 0 ​℃, 38.8 ​± ​0.5 ​℃ (n ​= ​8) at the Ta of 5 ​℃, and significantly lower than that at Ta of 20 ​℃ (P ​ < ​0.01). Tb in other three species stayed stable when the Ta was lower than 35 ​℃, namely at 42.5 ​± ​0.1 ​℃ (n ​= ​56), 41.7 ​± ​0.2 ​℃ (n ​= ​64), and 41.3 ​± ​0.14 ​℃ (n ​= ​72) in T. elliotii, P. sannio and C. sinica respectively (Table 1). In all species, Tb increased sharply when the Ta was equal to or higher than 35 ​℃. In any given Ta, the Tb of T. elliotii is higher than in the other three species (Fig. 2B).

    The evaporative water loss (EWL) increased significantly with Ta in all species, especially when the ambient temperature was higher than 30 ​℃. EWL increased with Ta according to these relationships: EWL (mg H2O/h) ​= ​6.447 Ta + 267.144 (R2 ​= ​0.300; P ​ < ​0.001; n ​= ​80), EWL (mg H2O/h) ​= ​5.378 Ta + 303.956 (R2 ​= ​0.050; P ​= ​0.032; n ​= ​80), EWL (mg H2O/h) ​= ​4.991 Ta + 237.589 (R2 ​= ​0.108; P ​= ​0.008; n ​= ​88), and EWL (mg H2O/h) ​= ​4.410 Ta + 187.617 (R2 ​= ​0.108; P ​= ​0.002; n ​= ​96) in P. davidi, T. elliotii, P. sannio, and C. sinica respectively. The mean minimum value was 254.2 ​± ​31.9 ​mg H2O/h (n ​= ​8), 348.4 ​± ​14.8 ​mg H2O/h (n ​= ​8), 247.2 ​± ​21.9 ​mg H2O/h (n ​= ​8), and 161.9 ​± ​6.2 ​mg H2O/h (n ​= ​8) when the Ta was 0 ​℃ in P. sannio, T. elliotii, P. davidi, and C. sinica, respectively. T. elliotii lost more water than P. divide and P. sannio, under any given Ta less than 30 ​℃ (Fig. 2C).

    The thermal conductance (C) was stable when the Ta ​ < ​30 ​℃ and increased with Ta when Ta ​ > ​30 ​℃ in all species. The average minimum C values were 0.117 ​± ​0.01 ​mL O2/(g·h·℃) (n ​= ​8), 0.112 ​± ​0.01 ​mL O2/(g·h·℃) (n ​= ​8), 0.03 ​± ​0.01 ​mL O2/(g·h·℃) (n ​= ​8), and 0.14 ​± ​0.01 ​mL O2/(g·h·℃) (n ​= ​8) in P. davidi, T. elliotii, P. sannio, and C. sinica, respectively (Table 1). C increased significantly in P. davidi when Ta ​= ​30 ​℃, and it reached a maximum of 0.47 ​± ​0.04 ​mL O2/(g·h·℃) (n ​= ​8) at 35 ​℃. C increased exponentially from 25 to 35 ​℃ as per the equation: log C ​= ​log 0.091 ​+ ​0.039 log Ta (R2 ​= ​0.622; P ​ < ​0.001; n ​= ​32). In P. sannio, C increased significantly when Ta ​= ​40 ​℃, and it reached a maximum of 0.44 ​± ​0.16 ​mL O2/(g·h·℃) (n ​= ​8). C increased exponentially from 35 to 40 ​℃ as per the equation: log C ​= ​log 0.020 ​+ ​0.043 log Ta (R2 ​= ​0.479; P ​ < ​0.001; n ​= ​16; Fig. 2D). In T. elliotii, C increased significantly when Ta ​= ​30 ​℃, and it reached a maximum of 0.46 ​± ​0.02 ​mL O2/(g·h·℃) (n ​= ​8). C increased exponentially from 30 to 35 ​℃ as per the equation: log C ​= ​log 0.088 ​+ ​0.031 log Ta (R2 ​= ​0.365; P ​ < ​0.001; n ​= ​16). In C. sinica, C increased significantly when Ta ​= ​35 ​℃, and it reached a maximum of 1.60 ​± ​0.05 ​mL O2/(g·h·℃) (n ​= ​8). C increased exponentially from 32.5 to 40 ​℃ as per the equation: log C ​= ​log 0.077 ​+ ​0.041 log Ta (R2 ​= ​0.434; P ​ < ​0.001; n ​= ​24). The dry thermal conductance (Cdry) was stable when the Ta ​≤ ​25 ​℃ and increased linearly with elevated Ta when Ta ​ > ​30 ​℃ in P. dividi and C. sinica. Cdry was stable when Ta ​≤ ​30 ​℃ and increased linearly with elevated Ta when Ta ​ > ​30 ​℃ in P. sannio and T. elliotii (Fig. 2E).

    MWP/EWL decreased with Ta in all species (Fig. 2F). At any given Ta, MWP cannot offset the EWL in all species.

    Contrary to our predictions, the northwardly-colonized White-browed Laughingthrush exhibited different thermogenesis traits from its coexisting species in the new habitat, especially for the lower basal metabolic rate and thermal conductance. In the four studied species, the BMR of P. sannio is the lowest and is far below the predicted value for its body weight. It exhibited thermogenic features of tropical species, and these were much lower than those of its temperate congener P. davidi, which evolved in temperate zone. TNZ of P. sannio is broad, which is consistent with its broad geographical distribution, and lower limits of TNZ enhanced cold tolerance. Thermal conductance in P. sannio is the lowest of the four species, far lower than the predicted value based on its body weight, which is different from tropical passerines and similar to temperate species. These results suggest that the cheaper thermoregulatory strategy in the White-browed Laughingthrush favors its expanding distribution to higher latitudes.

    Differences in BMR between different bird species are correlated with traits such as body size, diet, phylogeny, and migratory or resident life style (McNab, 2009). Species from cold climates tend to have higher BMRs, while those from warm regions tend to have lower BMRs (Kendeigh and Blem, 1974). Increasing endogenous heat production favors cold tolerance (Swanson, 2010), and its reduction has adaptive value to tropical species (McNab, 2009). The BMR of P. sannio exhibits characteristics of tropical species, far lower than that of P. davidi, which evolved in temperate zone, and far lower than Hwamei (which is 181 ​mL O2/h), which is a laughingthrush inhabiting in South China that is adapted to a warm, mesic climate (Xia et al., 2013). P. sannio is widely distributed in tropical and subtropical regions of Southeast Asia and China, with northward expansion occurring in recent years. However, its endogenous heat production is still similar to tropical species, and it differs from its temperate congener P. davidi, the montane similar species T. elliotii, and the subtropical similar species Hwamei.

    Both P. sannio and P. davidi have broad TNZs with lower limits, which are similar to C. sinica but different from T. elliotii. A similar species in terms of historical habitat of the P. sannio, the Hwamei, has a narrow TNZ (Xia et al., 2013), which is different from P. sannio but similar to T. elliotii. Bozinovic et al. (2014) argued that species that evolved in cold climates exhibit a wider TNZ with lower Tlc. Compared to the Hwamei, whose TNZ is 31.8–35.3 ​℃ (Xia et al., 2013), the two Peterorhinus species had a wider and broader TNZ than T. elliotii, which might be related to their distinct distributions and living environments. Hwamei has adapted to warmer climates, and T. ellioti is a montane species, with a narrow thermal tolerance (Polato et al., 2018). While the two Pterorhinus species in our study sites adapted to temperate climates, they showed broader TNZs with lower Tlc to enhance their cold tolerance (Bozinovic et al., 2014). The upper critical temperature of the TNZ in P. sannio is higher than in P. davidi, indicating that P. sannio can tolerate a higher Ta than P. davidi and survive in tropical areas. This is consistent with findings in weavers, which found that the larger species within the taxon can tolerate a higher Ta during acute heat exposure (Whitfield et al., 2015).

    Animals that evolved in colder zones exhibit broader TNZs and with lower Tlc, especially in high latitudes and arctic zones (Manuel and Anna, 2018). Small birds usually have TNZs with a different range, which is related to the ambient temperatures they experience (Bozinovic et al., 2014). For example, the TNZ in the winter-acclimatized Daurian Redstart (Phoenicurus auroreus) is 25–35 ​℃ (Wang et al., 2020), in Pallas's Rosefinch (Carpodacus roseus) is 22.5–27.5 ​℃, in the Brambling (Fringilla montifringilla) is 25–30 ​℃, and in the Common Redpoll (Acanthis flammea) is 25–28 ​℃ (Liu et al., 2004). Tlc in the Yellow-billed Grosbeak (Eophona migratoria) is 23.5 ​℃, in the White-rumped Munia (Lonchura striata) is 34.5 ​℃, and in the Black-throated Bushtit (Aegithalos concinnus) is 28.8 ​℃ (Qiao et al., 2016). Compared to these birds, our three birds had significantly lower Tlc, allowing them to reduce their energy expenditure in thermoregulation during colder temperatures. Winter severity is a critical factor governing population trends of northern temperate species (Link and Sauer, 2007). Harsh winters with lower ambient temperatures and prolonged food shortages promoted high cold tolerances, especially for those resident species occupying open habitats, like P. davidi and C. sinica.

    The body temperature (Tb) depends on the balance between heat production and dissipation, and it determines the rate of energy supply as well as almost all other biological rates (Gillooly et al., 2002; Brown et al., 2004). Tb in P. sannio, T. elliotii, and C. sinica remained stable when the Ta ​was lower than ​30 ​℃, which is consistent with other reports in small birds (Tieleman et al., 2002; Burton and Weathers, 2003) and Hwamei (Xia et al., 2013). Tb in P. davidi was lower when Ta was below 20 ​℃ and increased with elevated Ta within this range, which differs from the other three species and from other reports, where Tb is constant within Ta range of 5–30 ​℃ (Tieleman et al., 2002; Burton and Weathers, 2003), and from Hwamei (Xia et al., 2013). We noticed that the T. elliotii maintained a higher Tb than the other three species in our study, and it was close to the Hwamei (42.4℃; Xia et al., 2013), which tends to live at higher elevations. Elevated Tb could help avoid biochemical damage caused by hypothermia (Tieleman and Williams, 1999). We suggest that the lower Tb in P. davidi is due to the cold winter at our study site and its northern distribution, as Ta is low and available food is limited in winter, so a lower Tb could reduce heat loss and energy expenditure for thermoregulation. When the Ta exceeded 30 ​℃, Tb in our birds increased, which is consistent with other studies (Tieleman et al., 2002; Burton and Weathers, 2003; Xia et al., 2013). Another possible explanation is that a high Tb has negative implications for the fitness of arid-zone birds, for instance, a tradeoff with heat dissipation behavior leading to reduced foraging efficiency (Plessis et al., 2012). Therefore, for the P. davidi, its lower Tb is advantageous for living in its arid environment.

    Compared with the Hwamei, which is a species adapted to a mesic climate, EWL in all of our four birds is higher, even under lower Ta (Xia et al., 2013). Generally, compared with their mesic counterparts, EWL is lower and reduced in the birds adapting to dry climate, which is related to rare water sources and higher Ta (Tieleman et al., 2002; Xia et al., 2013). We found that all our birds respond poorly to water restriction, especially when the Ta ​ > ​30 ​℃, as the EWL increased sharply. Our study site is located inland at the Loess Plateau, and it is rare for the daily air temperature to surpass 30 ​℃, and visible water sources are rare, so the water intake in P. davidi and P. sannio comes mainly from their food contents due to the lack of visible water sources in their habitats. T. elliotii could consume water regularly because their habitat is closer to water sources (Liu et al., 2021). EWL is the only avenue of evaporative cooling in birds under a high Ta (Noakes et al., 2016). Higher EWL dissipates most heat loads through cutaneous evaporation in birds (Smith et al., 2015). Higher EWL in P. davidi and T. elliotii indicate that these two species have weaker heat tolerance than P. sannio, resulting from acclimatization to temperate and montane environments, respectively. Of these, the temperate species P. davidi and the montane species T. elliotii seem most at risk from climate warming because of their lower threshold temperatures for increasing EWL. Similar trends were found in other cool-climate species (Jiguet et al., 2010), arid-zone birds (Albright et al., 2017), and in a high-altitude specialist from south hemisphere, the Cape Rockjumper (Chaetops frenatus; Milne et al., 2015).

    Small birds have a relatively larger heat dissipation surface area. In tropical species, thermal conductance rates should be higher than in their temperate counterparts to avoid hypothermia, as tropical small birds experience more challenging high temperatures (Liu et al., 2004; Xia et al., 2013). Our results show that thermal conductance in P. davidi reached its maximum when the Ta was over 30 ​℃, implying that this species has poor endurance in high temperatures and is adapted to temperate climates. More interestingly, thermal conductance in P. sannio is lower than in the other species in our study, the Hwamei (Xia et al., 2013) and other tropical species (McNab, 2009). It is also far lower than the predicted value based on its body weight, which might be attributed to its lower BMR, and the lower thermal conductance could reduce heat dissipation and facilitate stable Tb maintenance (Speakman and Król, 2010). Lower thermal conductance in northwardly-colonized P. sannio is crucial to survive in colder conditions.

    Our findings indicate that the MWP cannot offset EWL in any of the four species studied, implying that the four species should consume water regularly, and these species rely heavily on evaporative cooling to tolerate high temperatures. In the Hwamei, the MWP offsets EWL when the Ta is 14 ​℃, and it exceeds EWL when Ta ​was below ​14 ​℃, which is related to the mesic climate to which it is adapted (Xia et al., 2013). Water economy models assume that variations of MWP and EWL represent determinants of the state of water balance (MacMillen, 1990; MacMillen and Baudinette, 1993; MacMillen and Hinds, 1998). Our results indicate that MWP cannot equal EWL at any Ta we measured, which is attributed to arid climates and high evaporation on the Loess Plateau.

    Our studies found that the thermogenic traits in the northwardly-colonized White-browed Laughingthrush is different from the other three coexisting species in its new habitat. As residents in a temperate zone, the three native species raise energy metabolic rate to increase heat production to resist cold exposure. In addition, the P. davidi in particular maintains relatively lower body temperatures in colder Ta to reduce direct energy requirements. P. sannio has lower metabolic thermogenesis and has broad a thermal neutral zone with lower limits to enhance cold tolerance and lower thermal conductance to reduce heat loss, this is why P. sannio has been able to expand northward and persist in temperate zone in recent years. EWL in our species is high and increased with Ta. Water content in their food is important to their survival, especially for P. sannio and P. davidi, the species that use arid habitats. Tropical birds often have narrower temperature optima than their temperate counterparts (Stratford and Robinson, 2005), and birds heat dissipation ability declines in environments with higher humidity (Gerson et al., 2014). We suggest that the northward expansion of P. sannio might be attributed to global warming, which affects the thermal physiology and temperature optima of birds. Does the northwardly-colonized P. sannio adapt to temperate climates through plasticity of thermal physiology, or is it an ancestral trait? We should compare the present population with its historically southern populations to get the answer, though unfortunately the tropical population of P. sannio is missing from our sample. Given the similarities and differences among overlapping species in response to shared climates, it will be critical to understand their distribution and persistence. We suggest researchers further discuss the physiological response to climate change, particularly the physiological mechanisms of northward expansion in bird species.

    The capture of birds in this study was approved by the Bureau of Forestry and Grassland of Zhuanglang County (Permission code 2020-02). All animal procedures complied with the local and national rules concerning the care and use of animal subjects and were approved by the Animal Care and Use Committee of Longdong University (2020005LU).

    PL, RJ, MJ and SZ conceived the experiments; PL and YS designed the experiments, analyzed the data, wrote the manuscript, and reviewed the drafts. All authors read and approved the final manuscript.

    The authors declare that they have no competing interest.

    We are grateful for the help from two undergraduate students, Weidong Cheng and Bo Xu, with the fieldwork. We would like to thank Dr. Joseph Elliot at the University of Kansas for his assistance with English language and grammatical editing of the manuscript. Financial support for this study was provided by the National Natural Science Foundation of China (Grant No. 32070452, 32011530077).

  • BirdLife International. 2012. Grus japonensis and G. vipio. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1. . Accessed on 09 July 2012.
    Bradter U, Gombobaatar S, Uuganbayar C, Grazia TE, Exo KM. 2005. Reproductive performance and nest-site selection of White-naped Cranes Grus vipio in the Ulz river valley, north-eastern Mongolia. Bird Conserv Int, 15: 313-326.
    Cheng L, Li XM. 2006. The status and conservation of Cranes in Heilongjiang Province. Territ Nat Resour Study, 1: 90-91. (in Chinese with English abstract)
    Feng KM, Li JL. 1985. Aerial surveys of the Red-crowned Cranes and other waterflowls in China. J Northeast Forest Univ, 13(1): 80-87. (in Chinese with English abstract)
    Feng SZ, Liu HJ, Yu WT, Jiang ZD. 2005. The survey on bird diversity in Xingkai Lake, China. Wetland Sci, 3(2): 149-153. (in Chinese with English abstract)
    Frederick PC, Towles T, Sawicki RJ, Bancroft TG. 1996. Comparison of aerial and ground techniques for discovery and census of wading bird (Ciconiiformes) nesting colonies. Condor, 98: 837-841.
    Fujita G, Harris J, Bold A, Tseveenmayadag N, Chuluunbatar S. 1994. Habitat preference of Demoiselle and White-napped Cranes, Anthropoides virgo and Grus vipio, breeding in Mongolia. In: Higuchi H, Minton J (eds) The Future of Cranes and Wetlands. Wild Bird Society of Japan, Tokyo, Japan, pp 93-96.
    Han YL, Ge DN, Zhang YX. 2003. The research about birds resource and conservation in Sanjiang Plain. Territ Nat Resour Study, 1: 76. (in Chinese with English abstract)
    Hanski I. 1998. Metapopulation dynamics. Nature, 396: 41-49.
    Harris J. 1994. Cranes, people and nature: preserving the balance. In: Higuchi H, Minton J (eds) The Future of Cranes and Wetlands. Wild Bird Society of Japan, Tokyo, Japan, pp 1-14.
    Hilton-Taylor C. 2000. IUCN Red List of Threatened Species. Gland, Switzerland and Cambridge, UK: IUCN.
    Hua Y, Li XM, Liu XC, Sun ZY. 2006. Comparison of bird diversity during spring and autumn in Honghe Nature Reserve. J Northeast Forest Univ, 34(3): 23-28. (in Chinese with English abstract)
    Jiang HX, Liu CY, Qian FW, Li CY, Qiu FC. 2009. A model of nest-site selection of Red-crowned crane based on RS, GIS and GPS techniques at Zhalong wetland, China. Sci Silv Sin, 45(7): 76-83. (in Chinese with English abstract)
    Lee SD, Jablonski PD, Higuchi H. 2007. Winter foraging of threatened cranes in the Demilitarized Zone of Korea: behavioral evidence for the conservation importance of unplowed rice fields. Biol Conserv, 139(1-2): 286-289.
    Li FM, Li PX. 1998. A comparative study on territories of White-napped Crane and Red-crowned Crane. Acta Zool Sin, 44(1): 109-111. (in Chinese with English abstract)
    Li FM, Li PX. 1999. A comparative study on territories of White-napped Crane and Red-crowned Crane. China J Ecol, 18(6): 33-37. (in Chinese with English abstract)
    Li XM, Hu YM, Ma YJ, Jia JL. 2003. Status and conservation of cranes in Sanjiang Plain. Territ Nat Resour Study, 1: 74-75. (in Chinese with English abstract)
    Liu HY, Li ZF. 2008. Effects of landscape change of wetlands on habitats of waterfowls within Honghe Nature Reserve by its surrounding area. Acta Ecol Sin, 28(10): 5011-5019. (in Chinese with English abstract)
    Liu HY, Zhang SK, Li ZF, Lv XG, Yang Q. 2004. Impacts on wetlands of large-scale land-use changes by agricultural development: The small Sanjiang Plain, China. Ambio, 33(6): 284-288. (in Chinese with English abstract)
    Liu XT. 1997. Marsh resource and its sustainable utility in the Songnen-Sanjiang Plain. Sci Geogr Sin, 16(Suppl. ): 451-460. (in Chinese with English abstract)
    Liu XT. 2000. Influence of large-scale reclamation on natural environment and regional environmental protection in the Sanjiang Plain. Sci Geogr Sin, 20: 14-19. (in Chinese with English abstract)
    Liu XT, Ma XH. 2002. Natural Environmental Changes and Ecological Protection in the Sanjiang Plain. Science Press, Beijing. (in Chinese)
    Ma YQ, Jin LR. 1987. The numerical distribution of the Red-crowned Crane in Sanjiang Plain area of Heilongjiang Province. Acta Zool Sin, 33(1): 82-87. (in Chinese with English abstract)
    Masatomi H, Ogawa S, Miyama K. 1990. The relations between land cover monitored by satellite remote sensing and distribution of the Tancho's nests in Kushiro Marsh, Hokkaido. J Hokkaido Coll, Sensu Univ, 23: 209-223.
    Mcgarigal K, Cushman SA, Neel MC, Ene E. 2002. FRAGSTATS v3: Spatial Pattern Analysis Programme for Categorical Maps. Computer software programme produced by the authors at the University of Massachusetts, Amherst. . Accessed on 10 October 2008.
    Noss RF, Murphy DD. 1995. Endangered species left homeless in sweat home. Conserv Biol, 9: 229-231.
    Pang SL. 2000. The report on the aerial survey of Red-crowned Crane in the Zhalong Nature Reserve. J Sci Teach Coll Univ, 20(2): 59-60. (in Chinese)
    Piao RZ, Han AH, Zhang MH. 2000. Remote sensing and geographic information system to estimate habitat selection of red-crowned crane in Sanjiang Plain of Northeastern China. In: China Ornithology Association, Wild Bird Society of Taipei and China Wildlife Conservation Association (eds) Studies on Chinese Ornithology — Proceedings of the 4th Ornithological Symposium of Mainland and Taiwan, China. China Forestry Publishing House, Beijing, pp 170-197. (in Chinese with English abstract)
    Prugh LR, Hodges KE, Sinclair ARE, Brashares JS. 2008. Effect of habitat area and isolation on fragmented animal populations. PNAS, 105(52): 20770-20775.
    Rodgers JA, Kubilis PS, Nesbitt SA. 2005. Accuracy of aerial surveys of waterbird colonies. Waterbirds, 28(2): 230-237.
    Schmidt BD, Roland J. 2006. Moth diversity in a fragmented habitat: importance of functional groups and landscape scale in the boreal forest. Ecol Popul Biol, 99: 1110-1120.
    Smirenski SM. 1988. Chick relationships and brood sizes in Red-crowned (Grus japonensis) and White-napped (Grus vipio) Cranes. In: Litvinenko NM, Neufeldt IA (eds). The Palearctic Cranes. Amur-Ussuri Branch of the USSE Ornithological Society, Vladivostok. USSR, pp 49-53.
    Smirenski SM, Harris J, Gray C, Strom K, Ichida N. 1995. Report of the Amur program of the Socio-Ecological Union. In: Halvorson CH, Harris JT, Smirenski SM (eds) Cranes and storks of the Amur River: the Proceedings of the International Workshop. Arts Literature Publishers, Moscow, Russia, pp 205-212.
    Song KS, Liu DW, Wang ZM, Zhang B, Jin C, Li F, Liu HJ. 2008. Land use change in Sanjiang Plain and its driving forces analysis since 1954. Acta Geogr Sin, 63(1): 94-104. (in Chinese with English abstract)
    Su LY, Xu J, Zhou DS. 1991. Breeding habitats of White-napped Cranes at Zhalong Nature Reserve. In: Harris J (eds) Prodeedings of 1987 International Crane Workshop. International Crane Foundation, Baraboo, Wisconsin, USA, pp 51-57. (in Chinese)
    Su LY, Wang QS. 2010. The mainland population of the red-crowned crane faces growing threat. China Crane News, 14(1): 3-8.
    Swift TL, Hannon SJ. 2010. Critical thresholds associated with habitat loss: a review of the concepts, evidence, and applications. Biol Rev, 85: 35-53.
    Temple SA. 1986. The problem of avian extinctions. Curr Ornithol, 3: 453-485.
    Wang QS. 2008. Threats for Red-crowned Crane. China Crane News, 12(2): 7-12.
    Yang XJ, Zhang SM, Zhang XX, Feng WY. 2005. The composing and analysis of large waterbirds diversity in the Sanjiang Plain. J Northeast For Univ, 33(3): 56-58. (in Chinese with English abstract)
    Zhang GC, Deng W, Lu XG, Song KS, Li HD, Zhang HY. 2007. The dynamic change of wetland landscape patterns in Xinkai River Basin. J Nat Resour, 22(2): 204-210. (in Chinese with English abstract)
    Zhang SQ, Na XD, Kong B, Wang ZM, Jiang HX, Yu H, Zhao ZC, Li XF, Liu CY, Patricia D. 2009. Identifying wetland change in China's Sanjiang Plain Using Remote Sensing. Wetlands, 29(1): 302-313.
    Zhao KY (ed). 1999. Chinese Mire Records. Science Press, Beijing. (in Chinese)
    Zhou DS, Su LY. 1990. Preliminary study on the territory behavior of Red-crowned Crane. In: Heilongjiang Forestry Department (ed) Conservation and Research of International Cranes. China Forestry Publishing House, Beijing, pp 54-58. (in Chinese)
    Zou HF, Wu QM, Ma JZ. 2003. The nest-site selection of Red-crowned crane in Zhalong Nature Reserve after burning and irrigating. J Northeast Norm Univ, 35(1): 54-59. (in Chinese with English abstract)
  • Related Articles

Catalog

    Figures(4)  /  Tables(6)

    Article Metrics

    Article views (2508) PDF downloads (2099) Cited by()

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return