INTRODUCTION

Surviving at higher elevations poses significant challenges for organisms, primarily because of reduced oxygen availability. The partial pressure of oxygen (PO₂), a crucial factor influencing organismal physiology in such environments, steadily decreases with increasing elevation by approximately 1% per 100 m (Beall 2014). It is a known fact that the reduced PO₂ induces severe physiological stress as a result of hypoxia. At higher elevations, this is a recognized stressor that necessitates specific physiological adaptations, particularly in the context of blood oxygen transport. One of the primary challenges associated with hypoxia is its impact on aerobic metabolism, a critical process for energy production found in all organisms, including birds. As oxygen availability decreases, it reduces the diffusion of oxygen from the lungs into the bloodstream, posing a challenge to the essential homeostatic processes needed for mitochondrial metabolism.

When lowland organisms ascend to higher elevations, kidney cells increase the production of erythropoietin, leading to elevated levels of hemoglobin (Hb) and hematocrit (Hct), which represents the ratio of red blood cells in the total blood volume (Storz et al. 2010, Storz and Scott 2019). This leads to an increase in the oxygen-carrying capacity of blood, which is crucial for oxidative metabolism. However, these responses can become counterproductive in severe hypoxic conditions. For instance, heightened erythropoietic activity, while potentially beneficial, may lead to increased blood viscosity, resulting in reduced blood flow (Storz et al. 2010). This maladaptive plasticity involves a deviation of the mean phenotype from the new optimum, necessitating genetic changes to counteract environmentally induced alterations (Grether 2005). In this scenario, genetic compensation causes the phenotype to evolve to resemble that of an unstressed population (Storz et al. 2010, Beall 2014). A compelling example of potential genetic compensation is seen in Tibetan highlanders, exhibiting lower hemoglobin concentrations and a reduced erythropoietic response at higher elevations (Beall 2007, Beall et al. 2010), which is not the case in the Andean highlanders, who, because of their shorter high-altitude residence history, show increased hemoglobin concentrations (Moore et al. 2001, Beall 2006, Beall 2007). This is also observed to be the case in high-altitude mammals and birds exhibiting comparable hemoglobin and hematocrit levels to their low-altitude counterparts (reviewed in Ramirez et al. 2007, Tufts et al. 2013).

The phenomenon of a blunted erythropoietic response is well-documented in passerine birds, with closely related species (Clemens 1990, DuBay and Witt 2014) and even in the same species (Ruiz et al. 1995), showing similar hematocrit and hemoglobin levels across different elevations. On the contrary, there are also instances where other bird species have shown increased hemoglobin concentrations and hematocrit levels at higher elevations. In a study conducted in the Western Himalayan region, Barve et al. (2016) found that both elevational migrants and high-elevation residents showed an increase in hemoglobin concentrations with increasing elevation while high-elevation residents had higher mean cellular hemoglobin concentration (MCHC) than elevational migrants. However, in the case of high-elevation residents, hemoglobin levels and hematocrit were not correlated. Therefore, it is important to assess these parameters individually to determine whether the species shows an increase in both hemoglobin and hematocrit. Additionally, examining the correlation between these parameters may provide insights into their migratory behavior. Other studies have also demonstrated a consistent pattern of elevated hemoglobin and hematocrit levels in response to altitude (Yap et al. 2019, Minias 2020). Studies on Andean hummingbirds have likewise shown that hemoglobin concentration and hematocrit generally increase with elevation (Williamson et al. 2023, 2024). Another study on Andean birds highlighted that across 136 species, with increasing elevational range breadth, there was an increase in the plasticity of hemoglobin concentration and MCHC (Linck et al. 2023).

The Himalayas, the world’s highest mountain chain, remain relatively underexplored in terms of understanding species adaptation to their challenging conditions. Here, one notable species, the House Sparrow Passer domesticus occurs from the foothills to elevations as high as 4500 meters. The subspecies Passer domesticus indicus is common throughout India as well as in the lower Himalayas while P. d. parkini occupies the high Himalayan mountains, typically at elevations greater than 2000 m (Summer-Smith 1988). House Sparrows, being human-commensals, very likely moved into the Himalayas with people settling there and expanded their range with the expansion of habitations. Supporting this, preliminary analyses of citizen science occurrence records including museum records from the Global Biodiversity Information Facility (GBIF) indicate a lack of House Sparrow observations from high-elevation Himalayan sites such as Nelong valley and Kuti Yankti valley before 2014, followed by a slight increase in records in more recent years (GBIF 2025). Additionally, their upward range expansion may be influenced by shifting climate regimes, which have made higher elevations more suitable for their survival. This pattern is consistent with upward shifts observed in other bird species in response to rising temperatures (Chen et al. 2011, Freeman et al. 2018). Given that House Sparrows occur across the elevational gradient, it offers an ideal model to study physiological responses to hypoxia at higher altitudes. Our study, therefore investigated the effect of hypoxic environments on hemoglobin concentrations and hematocrit in House Sparrow populations occurring in the Himalaya.

MATERIALS AND METHODS

Study area

The study was carried out in the western Himalayan State of Uttarakhand in northern India, where the elevation ranges from 150 m to about 7800 m. Uttarakhand is predominantly a rural state, with its population primarily concentrated in the valleys and on mountain slopes particularly between 1000 and 2000 meters. A typical village consists of 30 to 40 families who share resources and generally, most households keep a few cattle in their backyard. In the rural areas, the socioeconomic conditions are mainly driven by horticulture, sheep rearing, and tourism, with agriculture serving as the primary means of livelihood. Paddy (Oryza sativa) is the major crop cultivated in irrigated regions, while kidney bean (Phaseolus vulgaris) is grown on higher, unirrigated slopes. Other locally grown cereals and millets include soybean (Glycine max), horsegram (Macrotyloma uniflorum), and finger millet (Eleusine coracana; Maikhuri et al. 2015).

Methods

We captured a total of 97 House Sparrows using mist nets during October–November 2023 at eight sites in the following elevations: 230 m, 620 m, 1400, 1620 m, 3240 m, 3530 m, 3845 m, and 3850 m (Fig. 1). The species has an elevational range that extends from the plains up to nearly 3900 m in Uttarakhand, so we sampled both the lowest and highest elevations of its distribution. To assess the status of blood parameters in the middle of its range, we also included sites at mid-elevations. The sites sampled were categorized into three elevational bands: low elevation (< 1000 m), mid-elevation (1000–2000 m), and high elevation (> 3000 m). This classification was used to categorize sites into ecologically meaningful zones that reflect major habitat and climatic transitions along the elevational gradient. Upon capture, individuals were sexed, weighed, and morphometrics were recorded. We banded each sparrow with a metal leg ring and extracted 10 to 20 µL of blood from the brachial vein. The blood samples were then analyzed on-site by taking a few drops of blood in a spectrophotometer cuvette for measuring hemoglobin concentration (g/dL) using Hemocue HB201+ without subtraction of 1.0 g/dL. For measuring hematocrit levels, we collected blood using a heparinized microcapillary tube and centrifuged the same in a hematocrit centrifuge Neuation iFuge HCT NXT at 12,000 rpm for 5 minutes to separate the RBCs from the blood plasma. All the hemoglobin and hematocrit measurements were taken by the same individual using the same equipment throughout the study to ensure consistency. The mean cellular hemoglobin concentration was then calculated using hemoglobin and hematocrit values (MCHC= ([Hb] X 100/Hct), following Chappell et al. (1995).

STATISTICAL ANALYSES

We conducted all analyses using the 'R' software (version 4.3.1; R Core Team 2023). To ensure the repeatability of our hemoglobin and hematocrit measurements, we recorded two successive measurements from the same individual birds in a subset of samples (Hb, n = 18 and Hct, n = 19). We checked repeatability using the intraclass correlation coefficient (ICC) with the ICC package and found it to be high (Hb, ICC = 0.97 and Hct, ICC = 0.94). To compare differences in Hb, Hct, and MCHC across the different elevation bands, an ANOVA was performed using the “aov” function, which was then followed by post hoc Pairwise Tukey’s HSD, using the “TukeyHSD” function from the “stats” package. We also compared these variables separately for the eastern and western elevational gradients to assess whether patterns of response differed, potentially due to local adaptations or genetic differences. We then conducted linear regression to test the relationship between Hb and Hct. Additionally, we examined whether hemoglobin concentration was influenced by body mass and wing length by conducting separate linear regressions between hemoglobin and body mass, as well as between hemoglobin and wing length of individuals.

RESULTS

The blood parameters of the House Sparrow populations sampled in our study had a mean hemoglobin concentration of 19.5 ± 1.7 S.D g/dL (range: 15.6–24.0 g/dL), a mean percentage hematocrit level of 54.6 ± 6.8 S.D % (range: 42.0–71.0 %), and a mean MCHC of 35 g/dL ± 2.8 S.D (range: 27.0–44.0 g/dL). The site-specific hemoglobin and hematocrit values are given in Appendix 1. Further, the hemoglobin concentration and hematocrit level varied significantly across the three elevational bands (Hb: F = 59.84, df = 2, 94, p < 0.05; Hct: F = 35.74, df = 2, 94, p < 0.05) while MCHC was not different (F = 1.19, df = 2, 94, p < 0.31; Fig. 2). At higher elevations, the hemoglobin concentration and hematocrit percentage of House Sparrows were found to be significantly higher compared with mid and low elevations while these parameters were similar between the mid and low elevations (Table 1), and we found similar patterns when analyzing eastern and western gradients separately (Appendix 2).

The linear regression analysis revealed a positive linear relationship between hemoglobin concentration and hematocrit levels, indicating individuals with higher hemoglobin concentrations also had higher hematocrit levels (R² = 0.48, p <0.001, Fig. 3a). Additionally, hemoglobin concentration showed a positive relationship with body mass (R² = 0.05, p < 0.05, Fig. 3b) and wing length (R² = 0.16, p <0.001, Fig. 3c), though with a weak explanatory power, as evidenced by the low R² values.

DISCUSSION

The blood parameters recorded for House Sparrow populations in this study were distinctly higher compared to those documented elsewhere. In a study from central Spain, adult House Sparrows sampled in September (n = 8) had relatively lower mean hemoglobin concentrations of 13.7 g/dL, hematocrit level of 45.3%, and MCHC of 30.3 g/dL (Puerta et al. 1995). Likewise, Goldstein and Zahedi (1990) reported a mean hematocrit level of 48% for House Sparrow populations in Ohio, midwestern USA, which is far lower than that recorded in our study. The differences observed are likely a result of elevational influence, with the studies mentioned above representing lowland populations, while ours is a highland population. Further, in support of the elevational influence, we also observed lower mean hemoglobin concentrations and hematocrit levels in a small sample of lowland population from the northern Indian plains (data not included in this study; n = 7) being 16.4 ± 0.8 g/dL and 47.7 ± 2.7%, respectively. Passerines are known to exhibit higher average hemoglobin concentrations (~16.3 g/dL) and hematocrit levels (50.6%) than non-passerines (Minias 2020), with typical ranges between 15 and 21 g/dL for hemoglobin and 45 and 55% for hematocrit (Campbell and Ellis 2013); our high-elevation values fall at the upper end of this expected range. This variation in blood parameters across elevation zones has also been observed in other bird species, where highland populations consistently had higher values compared to their lowland counterparts of the same species (Minias 2020, Williamson et al. 2024).

The higher hemoglobin and hematocrit levels observed in House Sparrow populations above 3000 m in our study is very likely a case of physiological response, particularly given that partial pressure of oxygen (PO₂) decreases by nearly 30% at 3000 m compared to sea level. The similar hemoglobin and hematocrit levels at mid and low elevations observed in House Sparrows in our study, on the other hand, suggest that the populations at these elevations likely do not require enhanced oxygen-carrying capacity, as oxygen availability at these elevations may not be low enough to trigger a significant polycythemic response as also noted in some mammalian species (Mortola and Wilfong 2017). This further relates to the increased erythropoietic activity facilitating oxygen transport in House Sparrow populations inhabiting hypoxic environments.

Although these results provide meaningful insights into the complex interaction between hypoxic stressors and adaptive mechanisms, there exists a dichotomy in the response of avian species to hypoxic challenges, with few studies demonstrating no increase in hemoglobin concentrations and hematocrit levels at higher elevations (Clemens 1990, Ruiz et al. 1995, Ramirez et al. 2007, DuBay and Witt 2014), while others report an elevation-dependent increase in hemoglobin concentrations (Barve et al. 2016, Minias 2020, Linck et al. 2023). Our observation of elevation-dependent increases in hemoglobin levels in House Sparrows aligns with Barve et al. (2016), who reported rising hemoglobin concentrations with elevation in both elevational migrants and high-elevation residents, and with Linck et al. (2023) emphasizing the role of expanding elevational range in enhancing hemoglobin plasticity.

There is a notable divergence in the MCHC results, as Barve et al. (2016) found higher mean cellular hemoglobin concentrations in high-elevation residents than migrants. Similarly, Linck et al. (2023) also found that species with broad elevational ranges showed increased MCHC plasticity. Additionally, Barve et al. (2016) reported that elevational migrants showed an increase in hematocrit levels with elevation, whereas high-elevation residents had no clear relationship between hemoglobin and hematocrit, reflecting a strategic avoidance of elevated hematocrit to minimize blood viscosity costs. A similar pattern is observed in giant hummingbirds: southern elevational migrants show higher hematocrit levels than northern high-elevation residents, which tend to avoid increased hematocrit (Williamson et al. 2024). On the contrary, our study found a significant increase in hematocrit without changes in MCHC at higher elevations. This highlights the divergent response of high-elevation House Sparrows to hypoxic stressors compared to other species studied by Barve et al. (2016), Linck et al. (2023), and Williamson et al. (2024), and is likely shaped by the species’ colonization history to the higher elevations of the Himalayas.

The temporal dynamics of habitat colonization and species adaptation are likely key factors governing a species’ physiological response to hypoxic environments. One possible explanation is that species exhibiting increased hemoglobin and hematocrit levels at higher elevations have recently colonized these environments, undergoing rapid physiological adjustments to cope with hypoxic conditions. Conversely, species displaying similar hemoglobin and hematocrit levels as their lowland counterparts may have inhabited high-altitude environments for a longer time scale, possibly undergoing genetic adaptations that mitigate the need for pronounced physiological responses to hypoxia. Although our findings suggest a possible recent expansion into these environments, this interpretation is, however provisional and needs to be supported by genetic data.

The observed hematological plasticity in House Sparrows may be attributed to their recent population expansion into higher elevations of the Uttarakhand Himalayas. Field observations, supported by the data from eBird (downloaded on 26 May 2025), indicate an absence of House Sparrow occurrence records from high-elevation study sites during winter months, suggesting a seasonal downslope migration. Such seasonal movements may explain the elevation-dependent increases in hemoglobin and hematocrit levels observed in our study, suggesting that these populations may not yet be fully adapted to high-altitude environments. This type of behavior has been linked to higher hemoglobin and hematocrit levels in other species too, such as the Citril Finch (Carduelis citrinella), which displays elevated Hct levels at altitudes above 2000 m (Borras et al. 2010). Carey and Morton (1976) also reported similar trends in White-crowned Sparrow (Zonotrichia leucophrys) and Pine Siskin (Spinus pinus), where highland birds exhibit increased Hct levels. Williamson and Witt (2021) also explained that species exhibiting elevational niche-shift migration (ENSM) tend to have greater phenotypic flexibility, including plasticity in blood characteristics, which enables them to occupy different elevations across seasons. Recent studies (e.g., Ivy and Williamson 2024, Williamson et al. 2024) highlight how flexible blood traits can be, often shifting in response to seasonal changes and elevation. This suggests that the patterns we observed in House Sparrows are likely more about short-term physiological adjustments to seasonal movements across elevations, rather than evidence of permanent adaptation to life at high altitudes.

Our investigation into the physiological responses of House Sparrows to high-altitude environments prompts a close examination of the temporal and adaptive dynamics shaping avian responses to hypoxic stressors. It is clear from multiple examples that the species acclimated to high elevations often exhibit little or no hematological response, suggesting a biochemical adaptation characterized by genetic modifications and the evolution of phenotypes mirroring those of low-altitude populations (Storz et al. 2010, Beall 2014). Several studies have shown that evolved enhancements in Hb-O₂ affinity play a significant role in the adaptation to hypoxia across a wide array of birds (Black and Tenney 1980, Projecto-Garcia et al. 2013, Galen et al. 2015, Natarajan et al. 2015, 2016, 2018, Zhu et al. 2018). Taken together, these findings suggest that molecular structural modifications, underlie the successful adaptation of these species to hypoxic environments; however, they do not act in isolation. Complementing these avian examples, recent work on high-altitude deer mice has shown that evolved genetic changes suppress maladaptive traits, specifically right-ventricle hypertrophy under hypoxia, by reducing ancestral plasticity through shifts in gene regulation (Velotta et al. 2018). These findings highlight that adaptation is not just about gaining beneficial plasticity, but also about losing a harmful form of it. This shows how closely genetic evolution and phenotypic plasticity can work together in helping species navigate the challenges of high-altitude environments.

The positive correlation between the levels of hemoglobin and body size in our House Sparrows suggests that larger birds tend to have higher concentrations of hemoglobin and hematocrit. Minias (2015), had similarly reported positive correlations between hemoglobin levels and body mass across 12 avian species. Our results though diverged from other studies conducted at interspecific levels (Yap et al. 2019, Minias 2020), where hemoglobin and hematocrit levels were found to be negatively correlated with body mass. Our study highlights that House Sparrows at higher elevations exhibit larger body sizes, along with elevated hemoglobin and hematocrit levels. This observation is consistent with our previous findings (Bala et al. 2024), which also reported larger body sizes in high-elevation populations. However, it remains unclear whether these differences reflect distinct genetic adaptations or are simply phenotypic responses to environmental conditions.

In the higher elevations of the Uttarakhand region, it is still unknown whether the observed differences in blood parameters reflect subspecies-level variations or represent distinct populations and requires further investigation. According to literature, the subspecies Passer domesticus parkini is reported to occur in the trans-Himalayan regions (Summers-Smith 1988) and it is possible that this subspecies was an early colonizer of these regions, potentially linked to the upward movement of pastoral communities. P. d. parkini is characterized by its larger body size, as noted by Ali and Ripley (1998), and our previous study (Bala et al. 2024) similarly observed larger body sizes at higher elevations. However, it is currently unknown whether the House Sparrow populations at higher elevations in our study represent the parkini subspecies.

The role of shifting climate regimes in range expansion of House Sparrows can not be overlooked. With the rise of global temperature, species are increasingly forced to shift their ranges toward higher elevations (Thomas et al. 2004, Freeman et al. 2018), at a median rate of 1.1 m per year in mountainous regions, underlining the widespread nature of climate-induced range changes (Chen et al. 2011). In the Himalayas, areas that were once persistently covered with snow are now experiencing reduced snowfall, enabling human settlements to expand into previously inhospitable regions. House Sparrows, being human-commensals, may have moved upward with the expansion of permanent human settlements, either by directly following humans in higher altitudes or by responding to climate changes that have made these elevations more suitable for their survival. Our field observations (Bala et al. unpublished data) suggest that House Sparrows are scarce in lower urban parts of the Uttarakhand Himalayas, whereas their numbers appear higher in villages and border checkpost camps at higher elevations. This may be due to the availability of leftover food, insect availability from agriculture in villages, and the plantation of trees and hedges in camps. However, the absence of House Sparrows at the 4500 m checkpost suggests that they have not yet colonized this altitude, possibly because the settlement is relatively recent and the species has yet to establish itself. Understanding the factors influencing their upper distribution limits will be crucial in assessing the long-term impact of climate and human-induced landscape changes on their range expansion.

As climate change reshapes both natural and human-dominated ecosystems, species like House Sparrows must navigate multiple environmental challenges, including shifting temperatures, habitat modifications, and the physiological demands of high-altitude hypoxia. Understanding how these factors interact is crucial for predicting species’ adaptive responses and developing conservation strategies. Future research in other high-altitude regions, such as the Tibetan Plateau, where House Sparrows are year-round residents, could provide valuable insights into adaptations to hypoxic conditions. Additionally, considering that House Sparrows are a human-commensal species with a long history of association with human settlements, populations living close to these settlements in the trans-Himalayas may exhibit distinct physiological responses compared to those observed in this study, necessitating further investigation. Further research is needed to understand the underlying genetic mechanisms governing these responses and their implications for species survival and adaptation in high-altitude environments. Also, understanding the possible influence of climate change on the range expansion of House Sparrows to higher elevations is necessary for developing effective conservation strategies. This study demonstrates the pivotal role of physiological responses in understanding a species’ range expansion and its colonization history in hypoxic environments.

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