skip to main content

Title: The impacts of body mass on immune cell concentrations in birds
Body mass affects many biological traits, but its impacts on immune defences are fairly unknown. Recent research on mammals found that neutrophil concentrations disproportionately increased (scaled hypermetrically) with body mass, a result not predicted by any existing theory. Although the scaling relationship for mammals might predict how leucocyte concentrations scale with body mass in other vertebrates, vertebrate classes are distinct in many ways that might affect their current and historic interactions with parasites and hence the evolution of their immune systems. Subsequently, here, we asked which existing scaling hypothesis best-predicts relationships between body mass and lymphocyte, eosinophil and heterophil concentrations—the avian functional equivalent of neutrophils—among more than 100 species of birds. We then examined the predictive power of body mass relative to life-history variation, as extensive literature indicates that the timing of key life events has influenced immune system variation among species. Finally, we ask whether avian scaling patterns differ from the patterns we observed in mammals. We found that an intercept-only model best explained lymphocyte and eosinophil concentrations among birds, indicating that the concentrations of these cell types were both independent of body mass. For heterophils, however, body mass explained 31% of the variation in concentrations among species, much more » more than life-history variation (4%). As with mammalian neutrophils, avian heterophils scaled hypermetrically ( b = 0.19 ± 0.05), but more steeply than mammals (approx. 1.5 ×; 0.11 ± 0.03). As such, we discuss why birds might require more broadly protective cells compared to mammals of the same body size. Overall, body mass appears to have strong influences on the architecture of immune systems. « less
; ;
Award ID(s):
1656618 1656551
Publication Date:
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Page Range or eLocation-ID:
Sponsoring Org:
National Science Foundation
More Like this
  1. ABSTRACT Powered flight has evolved several times in vertebrates and constrains morphology and physiology in ways that likely have shaped how organisms cope with infections. Some of these constraints probably have impacts on aspects of immunology, such that larger fliers might prioritize risk reduction and safety. Addressing how the evolution of flight may have driven relationships between body size and immunity could be particularly informative for understanding the propensity of some taxa to harbor many virulent and sometimes zoonotic pathogens without showing clinical disease. Here, we used a comparative framework to quantify scaling relationships between body mass and the proportions of two types of white blood cells – lymphocytes and granulocytes (neutrophils/heterophils) – across 63 bat species, 400 bird species and 251 non-volant mammal species. By using phylogenetically informed statistical models on field-collected data from wild Neotropical bats and from captive bats, non-volant mammals and birds, we show that lymphocyte and neutrophil proportions do not vary systematically with body mass among bats. In contrast, larger birds and non-volant mammals have disproportionately higher granulocyte proportions than expected for their body size. Our inability to distinguish bat lymphocyte scaling from birds and bat granulocyte scaling from all other taxa suggests there maymore »be other ecological explanations (i.e. not flight related) for the cell proportion scaling patterns. Future comparative studies of wild bats, birds and non-volant mammals of similar body mass should aim to further differentiate evolutionary effects and other aspects of life history on immune defense and its role in the tolerance of (zoonotic) infections.« less
  2. Abstract

    Body size affects many traits, but often in allometric, or disproportionate ways. For example, large avian and mammalian species circulate far more of some immune cells than expected for their size based on simple geometric principles. To date, such hypermetric immune scaling has mostly been described in zoo‐dwelling individuals, so it remains obscure whether immune hyper‐allometries have any natural relevance. Here, we asked whether granulocyte and lymphocyte allometries in wild birds differ from those described in captive species. Our previous allometric studies of avian immune cell concentrations were performed on animals kept for their lifetimes in captivity where conditions are benign and fairly consistent. In natural conditions, infection, stress, nutrition, climate, and myriad other forces could alter immune traits and hence mask any interspecific scaling relationships between immune cells and body size. Counter to this expectation, we found no evidence that immune cell allometries differed between captive and wild species, although we had to rely on cell proportion data, as insufficient concentration data were available for wild species. Our results indicate that even in variable and challenging natural contexts, immune allometries endure and might affect disease ecology and evolution.

  3. A central theme in the field of ecology is understanding how environmental variables influence a species’ distribution. In the last 20 years, there has been particular attention given to understanding adaptive physiological traits that allow some species to persist in urban environments. However, there is no clear consensus on how urbanization influences physiology, and it is unclear whether physiological differences in urban birds are directly linked to adverse outcomes or are representative of urban birds adaptively responding to novel environmental variables. Moreover, though low-density suburban development is the fastest advancing form of urbanization, most studies have focused on animals inhabiting high intensity urban habitats. In this study, we measured a suite of physiological variables that reflect condition and immune function in male song sparrows ( Melospiza melodia ) from rural and suburban habitats. Specifically, we measured hematological indices [packed cell volume (PCV), hemoglobin concentration, mean corpuscular hemoglobin concentration (MCHC)], circulating glutathione (total, reduced, and oxidized), oxidative damage (d-ROM concentration), antioxidant capacity, and components of the innate immune system [bacteria killing ability (BKA), white blood cell counts]. We also measured whole-animal indices of health, including body condition (scaled mass index length) and furcular fat. Song sparrows inhabiting suburban environments exhibited lowermore »hemoglobin and MCHC, but higher body condition and furcular fat scores. Additionally, suburban birds had higher heterophil counts and lower lymphocyte counts, but there were no differences in heterophil:lymphocyte ratio or BKA between suburban and rural birds. PCV, glutathione concentrations, and oxidative damage did not differ between suburban and rural sparrows. Overall, suburban birds did not exhibit physiological responses suggestive of adverse outcomes. Rather, there is some evidence that sparrows from rural and suburban habitats exhibit phenotypic differences in energy storage and metabolic demand, which may be related to behavioral differences previously observed in sparrows from these populations. Furthermore, this study highlights the need for measuring multiple markers of physiology across different types of urban development to accurately assess the effects of urbanization on wildlife.« less
  4. null (Ed.)
    ABSTRACT Miniature insects must overcome significant viscous resistance in order to fly. They typically possess wings with long bristles on the fringes and use a clap-and-fling mechanism to augment lift. These unique solutions to the extreme conditions of flight at tiny sizes (<2 mm body length) suggest that natural selection has optimized wing design for better aerodynamic performance. However, species vary in wingspan, number of bristles (n) and bristle gap (G) to diameter (D) ratio (G/D). How this variation relates to body length (BL) and its effects on aerodynamics remain unknown. We measured forewing images of 38 species of thrips and 21 species of fairyflies. Our phylogenetic comparative analyses showed that n and wingspan scaled positively and similarly with BL across both groups, whereas G/D decreased with BL, with a sharper decline in thrips. We next measured aerodynamic forces and visualized flow on physical models of bristled wings performing clap-and-fling kinematics at a chord-based Reynolds number of 10 using a dynamically scaled robotic platform. We examined the effects of dimensional (G, D, wingspan) and non-dimensional (n, G/D) geometric variables on dimensionless lift and drag. We found that: (1) increasing G reduced drag more than decreasing D; (2) changing n had minimalmore »impact on lift generation; and (3) varying G/D minimally affected aerodynamic forces. These aerodynamic results suggest little pressure to functionally optimize n and G/D. Combined with the scaling relationships between wing variables and BL, much wing variation in tiny flying insects might be best explained by underlying shared growth factors.« less
  5. Synopsis

    Reproduction and self-maintenance are energetically costly activities involved in classic life history trade-offs. However, few studies have measured the responses of wild organisms to simultaneous changes in reproductive and self-maintenance costs, which may have interactive effects. In free-living female Barn Swallows (Hirundo rustica), we simultaneously manipulated reproductive costs (by adding or removing two nestlings) and self-maintenance costs (by attaching a ∼1 g weight in the form of a GPS tag to half of our study birds) and measured mass, immune status, blood glucose, feather growth, and reproductive output (likelihood of a second clutch, number of eggs, and time between clutches). GPS tags allowed us to analyze how movement range size affected response to brood size manipulation. Tagging altered females’ immune function as evidenced by an elevated heterophil to lymphocyte (H:L) ratio, but all females were equally likely to lay more eggs. There was no evidence of interactive effects of the tagging and brood size treatment. Range size was highly variable, and birds with large ranges grew feathers more slowly, but analyzing the effect of brood size manipulation while accounting for variation in range size did not result in any physiological response. Our results support the theoretical prediction that short-lived vertebratesmore »do face a trade-off between reproduction and self-maintenance and, when faced with increased costs, tend to preserve investment in reproduction at the expense of parental condition. This experiment also helps us to understand how movement patterns may be relevant to life history trade-offs in wild birds.

    « less