Birds: Did Evolution of Biological Novelties Compromise Their Capacity to Effectively Adapt to Extreme Environmental Conditions?

Simple Summary

Among extant air-breathing vertebrates, birds are the most species-rich animal group. Together with other traits, morphologically, physiologically and behaviourally, they are exceptionally well-adapted for life under diverse ecological habitats. To various extents, most species of birds are presently suffering the effects of extreme environmental conditions that are causing drastic biodiversity changes, population declines, contracting ecological ranges and extinctions. Here, critical appraisal of the unique adaptive specialisations of birds, the foremost adverse environmental conditions that birds are currently contending with and the biological consequences of their subsisting under severe surroundings are detailed and explicated. It is suggested that under existing ecological threats such as climate change, habitat devastation and pollution, among others, with the exception of a few exceptional species, the adaptive capacities of birds appear to have generally declined. It is suggested that due to these progressively worsening conditions, conservation of birds, especially the most adversely affected species, should be considered.

Abstract

Foremost, the structural, functional and behavioural traits of birds relate directly or indirectly to volancy, i.e., the capacity for powered flight, an elite mode of locomotion that decisively made them what they are today: ‘specialist and extreme animals’. Placing them at the pinnacle of the evolutionary hierarchy, birds possess exceptional biological specialisations which, dispersed across the globe, have provided them with profound survival advantages. The adaptive novelties of birds are above all indicated by the remarkable morphological refinements and physiological specialisations of their respiratory system, the lung-air sac system. To contribute to the ongoing discussions and debates on the impacts of existing and continuing extreme environmental conditions (ECs) on the biology of birds, here, a viewpoint is posed that the adaptive innovations that birds acquired in the past, ostensibly under different ECs, may have undermined their capacity to effectively adjust to different outcomes. To explain this perspective, the following aspects are considered: the specialist and extreme biology of birds; the prevailing brutal ECs that birds must presently endure; and the consequences of having to suffer extreme conditions that include global warming and habitat destruction and pollution. It is proposed that under these existential threats, in general, the adaptive capacities of birds appear to have weakened, rendering them more vulnerable to external pressures. It is suggested that urgent conservation measures, especially for the most threatened species of birds, should be considered.

1. Introduction

‘Evolutionary novelty, while often beneficial, frequently comes with associated costs. These costs can manifest as reduced fitness in certain environments, increased susceptibility to specific challenges, or trade-offs with other advantageous traits’.

[1]

From structural, functional and evo-devo (evolutionary developmental) perspectives, novelties are the derived, individualised body attributes and processes that are not homologous to hitherto existing ones; evolutionary novelties are the aspects that endow animals with exceptional traits, enabling them to appropriate new habitats. Fitness reduction is the waning of an organism’s capacity to exist in its environment and, in general, biological costs entail commitment of energy, time or resources into particular traits so as to maintain specialised adaptations [1,2,3,4]. Complex multicellular organisms comprise various structurally and functionally reciprocal interdependent constituents [5,6]. Synergy between the adaptive traits promotes outcomes that generate total performance that surpass the sum of the actions by the individual parts [7,8,9]. In biology, the concept of ‘symmorphosis’ [10] specifies that the structural designs of the various parts of the animals match the functional demands placed on them, meeting but not exceeding their needs to ensure economical utilisation of resources. While this consideration has not been heuristically embraced in every respect, particularly by evolutionary biologists [11,12,13,14], it remains fundamental to understanding life’s structural and functional states and processes [15,16]. For birds, due to factors such as their body sizes and the lifestyles they follow, indisputable pulmonary structural and functional correlations exist [14,17,18,19,20,21]. As of now, however, the mammalian lung is the only area where means and ways have been systematically investigated: a complete and thorough investigation has been conducted on the ‘O₂ flow pathway/cascade’, i.e., the route O₂ molecules follow from the gas exchanger (respiratory organ) to the so-called O₂-sink (mitochondria where energy is produced) [16,22]. Regarding the application of the concept of symmorphosis to the functional designs of avian (bird) and chiropteran (bat) lungs, Maina [15] observed that ‘the multidimensionality of such complex permutations make the state and process of optimisation and the particular factors behind such adjustments difficult to define precisely’. For animal life, integrated adaptive specialisations that scale from cellular- to organ-system levels are important for efficient utilisation of resources under the finite energy, nutrient and time constraints they live and operate under [23,24,25,26]. Invariably, allocation of resources to one trait results in reduction of what remains for the others [27,28]. Genetic, environmental, morphological, physiological and behavioural adaptations foremost determine the optimal functions for life [29,30,31]. Significantly driven by dietary requirements, types of habitat occupied, and the efficient management and utilisation of energy, birds have adaptively secured decisive ecological, morphological and physiological specialisations [32,33,34,35] that were mainly compelled by the high metabolic demands for powered (active) flight [36,37], a unique form of locomotion that was particularly supported by the most efficient respiratory system (the lung-air sac system) that evolved among air-breathing vertebrates [38,39,40,41,42,43,44,45,46,47].

To ensure survival under challenging ecological states and adverse ECs, naturally, organisms/animals employ a broad range of adaptive strategies that culminate in evolution of adaptive novelties [48,49]. The following are some of the models that have been developed and employed to gain a better understanding of the evolution of biological states and processes:

• The ‘evolutionary rescue models’ posit that adaptive evolutionary changes restore positive growth to declining populations and avert extinction [50,51].
• The ‘evaluation of adaptive capacity model’ gauges the capacity to adjust to climate change, threats or stressors, usually by determining indicator-based quantities that assess a species’ ability to cope with or adjust to changing climatic conditions [52,53].
• A ‘vulnerability assessment model’ evaluates the adaptive capacity of a species to climate change while identifying vulnerabilities and providing solutions [54,55,56,57].
• The ‘reaction norms model’ explains how a particular genotype generates various phenotypes through a spectrum of environments, and it considers how a range of phenotypic differences are produced when individuals of the same genotype are subjected to changing ECs [58,59].
• The ‘heritability estimates model’ statistically determines the proportion of variation in a specific trait within a population that is attributable to genetic variations instead of environmental factors [60,61].
• The ‘plasticity-first hypothesis’ purports that adaptive evolution often starts with environmentally induced phenotypic changes that are subsequently honed by natural selection, i.e., genetic alteration [62,63].
• The ‘buying time hypothesis’ suggests that when populations face different environments or harsher ECs, various phenotypes are rapidly produced (a plastic response), preventing extinction and providing time for the population to advance favourable genes that result in adaptive evolution [64].
• ‘Adaptive tracking models in rapidly shifting climates model’ assesses continuous adaptation in response to rapid change in ECs [65,66].
• The ‘bet-hedging hypothesis’ suggests that organisms in shifting environments evolve purposeful traits that lower continuing fitness variation, at times abandoning highly viable payoffs during good times to avoid extinction under exacting ones [67].
• ‘Phenotypic plasticity model’ specifies how a single genotype generates various phenotypes in response to changing ECs. It studies the capacity of a single genotype to produce discernible traits (phenotypes) in response to environmental signals [68,69].

These models address different aspects and provide various answers on how animal life responds to evolutionary and ecological conditions, as well as ECs. The data acquired should provide details that are important in the conservation of threatened species. Manifested physiologically, morphologically, biochemically and behaviourally, phenotypic plasticity is an overarching process for understanding life in general and fitness in particular: it explains how novelties evolve and ecological populations are established. For animals facing new, altered and especially extreme ECs, particular examples interestingly suggest that plasticity may accord no advantages and may even impair rather than enhance survival [70,71,72]. According to Chen and Khanna [73], for the birds of North America, when compared to generalist species, ongoing climate change is notably impacting specialist ones. Based on ongoing environmental changes, it is projected that by the end of this century, declines of 7–16% will have occurred for specialist animal species while the generalist ones will have suffered relatively lower losses of 1–3% [74]. Whilst specialist animals operate optimally under particular ECs, their adaptive specialisations may possibly constrain their capacity to adjust to different ECs [75,76,77]. To maintain balance while imparting optimality, in biology, adaptive processes entail transactions that involve trade-offs and compromises [78,79,80]: the best fitness levels are determined by traits that develop and work together [81,82,83,84]. Adaptively well-endowed animals survive and thrive to pass on their ‘good’ genes to new generations [7,80]. Under the extreme ECs which presently exist, for six classes of animals—including mammals, birds, amphibians, reptiles, fishes and insects—and based on extensive data published in the IUCN (International Union for Conservation of Nature) Red List, Finn et al. [85] showed that compared to other groups of animals, birds suffer a significantly higher extinction risk. Recently, Bickel and Bax [86] observed that with alarming consequences, the most specialised bird species are declining at a remarkable rate. Analysing data from ‘Living Planet Index’ (https://www.livingplanetindex.org) from 1950 to 2020, with the generally small passerine species particularly affected, Kotz et al. [87] observed that heatwaves, which were driven by climate change, had over time led to declines of between 25 and 38% of tropical bird populations. The adaptive capacities of birds appear to have weakened under existing extreme ECs such as global warming, habitat devastation and fragmentation and pollution [88]. From being particularly adaptable, certain species of birds are remarkably resilient to the ongoing ECs [89,90,91]. The rapid rate of increase of the severity of the ECs appears to have considerably reduced the adaptive capacities of many avian species [91]. Investigating change in community structure in response to climate warming (CW), Devictor et al. [92] determined that while birds are rapidly tracking CWM, the response is not enough to offset the injurious effects of particularly temperature increase: birds have lagged ~182 km behind the pace of CW. While ecological specialisation has been shown to be an important constraint to the response of species to ECs [93,94], here, it is argued that morphological and physiological novelties also contribute to susceptibilities of birds to extreme ECs. It is visibly becoming clear that highly specialised traits such as dietary requirements, nesting routines and morphological refinements, which once proffered significant evolutionary advantages, may have become evolutionary traps or liabilities that now severely hinder the ability of especially specialist animals to adapt to ongoing environmental pressures [93,94]. As the ECs shift, birds are struggling to adapt to rapid changes, with many species experiencing reduced reproductive success, constrained food availability and higher mortality rates from extreme weather events such as severe heatwaves and increased disease outbreaks that lead to direct mortality [95]. According to the classical model of biological trade-offs and traits [82], for the specialist animals, convex trade-offs support development of sympatry, i.e., coexistence between species, while concave ones lead to existence of intermediate species. Specialist animals, which are restricted to small ecological ranges and utilise special kinds of food, are at greater risk of extinction from changes in ECs [94,96,97,98]. While specialisation generally causes greater extinction risk, exploitation of various resources allows generalist animals to adapt and thrive under adverse conditions [93]. For birds, regarding their respiratory system, it has been shown that its structure predisposes them to infections, afflictions and diseases from pathogens and particulates, especially those acquired through inspired air [99,100,101,102].

To contribute to the ongoing studies, discussions and debates and to hopefully stimulate further research on the many unknown aspects on the effects of the environmental pressures on birds, the following question was posed:

• Do birds exhibit poorer rates of adaptive trait evolution compared to other vertebrates?
• Are physiological and morphological safety margins (reserve capacities) narrower in birds?
• For birds, is extinction risk associated with extent of respiratory specialisation?

To explain the viewpoint, the following aspects were considered: (a) birds as ‘specialist’ and ‘extreme’ animals; (b) the most important adverse ECs, i.e., climate change and habitat devastation, fragmentation and pollution, which birds are presently contending with; and (c) the consequences ensuing from birds facing challenging ECs.

2. Birds Are Specialist and Extreme Animals

Morphological, physiological and behavioural specialisations, among others, have enabled birds to disperse worldwide and inhabit different habitats. Exceptional biological traits made them ‘specialist- and extreme’ animals [103,104,105,106,107,108]. During the ~4.3 billion years (10⁹) that life has existed on Earth [63,64,65], only four animal taxa, namely insects, the now-extinct pterosaurs, birds and bats, chronologically in that order, have ever accomplished powered flight [109,110,111,112]. Volancy explains the remarkable speciation of birds. By applying a diagnostic evolutionary species concept to morphological- and global distributional data, Barrowclough et al. [113] estimated that there are 18,043 and possibly as many as 20,470 species of birds which surpass the probable 9010 amphibian (https://amphibiaweb.org/amphibian/speciesnums.html—accessed on 20 March 26), 11,050 reptilian [114] and 6640 mammalian species (https://www.mammaldiversity.org/—accessed on 20 March 26). After evolving to achieve powered flight, in order to overcome geographical obstacles such as mountains, rivers, seas, oceans and deserts, birds dispersed widely into diverse habitats and the adaptive radiation led to profound speciation [115,116,117]. On its own, speciation, i.e., species abundance or richness, does not meaningfully specify species’ adaptive superiority. Instead, modelling of ‘diversification’ or ‘tip’ rates [118,119,120,121], which shows species rates of changes over time, allows for the degree of lineage-specific divergence and identification of important novelties in the evolution of a heritage to be made.

The evolution of adaptive morphological, physiological, genetic, neurological, reproductive and behavioural traits, among others, which suited the habitats animals occupied and the lifestyles they followed, allowed birds to live and thrive [42,122,123,124,125]. Placing extreme demands, particularly on the respiratory, cardiovascular and muscular systems, active flight, for which power outputs per unit time is the highest compared to other types of locomotion, is energetically very demanding [126,127,128]. For migratory birds, particularly those that fly continuously over long distances, during a pursuit that occurs under metabolic rates that are ~10 times higher than those at rest [129], as much as ~20% of the flight muscle mass is lost due to protein catabolism [130]. The adaptive morphological specialisations for powered flight are so restrictive that while the number of species of birds far exceed those of mammals by a factor of about three, regarding their external morphologies, birds are reportedly more uniform than mammals [131,132,133,134]. Even those species that have for various reasons abandoned flight, i.e., have acquired secondary flightlessness [135,136,137], stem from volant progenitors [138,139].

The foremost distinctive biological traits that have placed birds high up on the vertebrate evolutionary ladder include the following:

• Their forelimbs were modified into wings which became totally committed to powered flight [140,141];
• The skeletal system was considerably modified mainly by loss and fusion of bones and significantly adapted for lightness and strength [142,143,144];
• Development of large and powerful hearts with strong muscles generated large cardiac outputs and short circulatory transit times that enhanced O₂ and nutrient procurement and delivery to the cells of the body [13,145,146];
• A lack of teeth (edentulism) [147,148], a feature which contributed to modification of the craniofacial skeleton, resulted in birds having to swallow food whole, a feature that was offset by development of a strong food-grinding gizzard [149];
• High and constant body temperatures (38–42 °C) raised metabolic rates [134,150,151,152,153,154] which together with powerful flight muscles [155,156] supported powered flight;
• An exceptionally efficient respiratory system [39,40,157,158] permitted acquisition of large amounts of O₂ which sustained the high metabolic rates that were vital to powered flight;
• Inclusive egg-laying (oviporosity) attribute and development of embryos outside of the body, reduced body mass which promoted powered flight [159,160,161,162];
• Methodical parental care, shrewd nest making, and the strategic placement of nests in hard-to-reach places ensured survival for adults and young ones [163,164];
• A highly developed nervous system with sharp senses permitted important highly specialised activities such as proper navigation during migration and effective communication [165,166,167];
• Superior brain-sanctioned problem-solving capacities—such as ‘tool use’, i.e., dropping of hard and difficult to break foods (i.e., nuts) from a height so as to break them open and access food [168,169,170] and food caching, i.e., strategically storing food for use during times of scarcity—allowed survival during difficult times [171,172,173,174];
• Sophisticated vocalisation that permitted complex sexual displays and ensured successful mating [175,176];
• The development of large eyes and excellent visual acuity, especially in the diurnal raptorial species, was important for navigation under subdued light and effective prey capture [119,176,177];
• Light and strong feathers served important needs such as thermal insulation, sexual displays, communication and flight [178].

Among air-breathing vertebrates, the avian respiratory system (ARS)—the lung-air sac—is the most structurally complex and functionally efficient gas exchanger [39,42,43,133,157,179,180,181,182]. While its primary function is acquisition of O₂ and removal of CO₂, other important roles include sound production at the syrinx [42,133] and thermoregulation [82,135], especially because birds lack sweat glands [183,184,185]. In biology, research on the form and function of the ARS has been a long and frustrating process that was riddled with passionate debates and controversies [39,40,42,179,180,181,182]. Here, the differences between the structural properties of the ARS [42,45,46] and the mammalian one [186] are respectively shown in Figure 1(1–15) and Figure 1(16–30). The unique evolutionary, developmental, structural and functional specialisations of the ARS were recently detailed by Maina [42,43]. The distinctive features include the following:

• The ARS is structurally and functionally separated into a small compact lung that serves as the gas exchanger while the air sacs ventilate it (lung) (Figure 1(1–3)).
• Practically rigid, the avian lungs are firmly fixed to the ribs and the vertebrae, causing them to be uninflatable (Figure 1(1–7)).
• Structurally, the airway (bronchial) system of the avian lung comprises a three-tier, hoop-like arrangement (Figure 1(7)).
• The exchange tissue is intensely partitioned into extremely small terminal respiratory units, the air capillaries (Figure 1(8–15)).
• Notable morphometric specialisations, which include large respiratory surface area, thin blood–gas barrier (BGB) and large pulmonary capillary blood volume, exist in the avian lung [14,42,43,44,45,105] (Figure 1(14,15)).
• In the exchange tissue of the avian lung, the arrangement of the terminal structural parts, i.e., airway and vascular systems, form crosscurrent, countercurrent and multicapillary serial arterialisation gas exchange systems [42,43,105] (Figure 1(8–12)).
• Due to the existence of, in particular, cross-current and multicapillary serial arterialisation gas exchange systems [39,42], for the avian lung, the PO₂ in the expired air surpasses those of arterial and mixed venous bloods [39,40,161].
• Synchronised bellow-like actions of the caudal and the cranial groups of air sacs (Figure 1(1–3)) efficiently ventilate the avian lung continuously and unidirectionally in a caudocranial direction [39,40].

The above adaptive specialisations explain how and why the ARS is a remarkably efficient gas exchanger. Regarding the mass-specific maximum oxygen consumption (VO₂max.M⁻¹), birds are the most highly metabolically active vertebrate species. For the tiny (~3 g) hovering Anna Hummingbird (Calypte anna), its VO₂max.M⁻¹, which can be as high as (41.5 mlO₂.g⁻¹.h⁻¹) [187], surpasses that of the pronghorn antelope (Antilocapra americana), which among terrestrial animals achieves speeds that are only rivalled by the cheetah (Acionyx jubatus), and has a VO₂max.M⁻¹ of only 11.52–18.36 mlO₂ g^–1 h⁻¹ [188]. The hovering or flying nectar feeding bat, Glossophaga soricina, has a VO₂max.M⁻¹ of 15–21 mlO₂.g⁻¹.hr⁻¹ or higher [189]. In contrast to those of birds, mammalian lungs are lobulated and are freely contained in the thoracic cavity (Figure 1(16)), the airway (bronchial), arterial and venous systems branch dichotomously and closely pattern each other (Figure 1(17–20)). The airway system terminates with alveoli—the respiratory units (Figure 1(20–26))—and a thin BGB that separates air (in the alveoli) from the pulmonary capillary blood exists at the alveolar level (Figure 1(27–30)).

Comprising an epithelial basement membrane and endothelial parts, the design of the BGB is termed a ‘tripartite’ one [190,191,192,193,194]: in avian and the mammalian lungs, this structural feature is a shared one. Compared to those of mammalian lungs, for animals of equivalent body mass, the BGBs of the avian lungs are relatively thinner [14,42,45,46,105,191,192,193,194,195]. While a functionally thin BGB promotes gas exchange by diffusion [196,197], it renders the BGB more vulnerable to structural failure from excessive intracapillary (transmural) blood pressures [198,199,200,201,202,203]. When studying the lung of the Free-Range Chicken (Gallus gallus variant domesticus), after the birds were run (exercised) on a treadmill to a maximum speed of 2.95 m.sec⁻¹, an activity that increased the pulmonary capillary blood pressure beyond 3.39 kPa, Maina and Jimoh [202,203] observed that the raised intracapillary blood pressure caused stress failure of the BGB. Interestingly, it was found that BGB failure occurred to a lesser extent in the lungs of resting, i.e., unexercised, healthy birds [201,202]. It showed that BGB failures may be a prevalent and manageable occurrence in bird lungs. When studying the gas exchange tissue of the duck lung by respectively directly compressing the lung [204] and temporarily occluding one of the pulmonary arteries, an experimental procedure that about doubled the blood flow to one lung [205], i.e., after directing the entire cardiac output to the one functional lung, it was observed that the air and blood capillaries did not change in size, i.e., they were practically rigid. More recently, in the lungs of the white leghorn breed of chickens, Watson et al. [206] determined that when the pressure inside of the blood capillaries was increased from 0 to 2.5 kPa, their diameters increased by only 13% and that increasing the pressure outside of the blood capillaries to 3.5 kPa did not alter their diameters. Comparing the transmural pressures at which the BGBs of the lungs of the rabbit, the dog, the horse and the chicken structurally failed, values that were respectively ~5, ~10, ~14 and 3.39 kPa [200,202,203,207,208] and when considering that the respective harmonic mean thicknesses of the BGB are 0.65, 0.65, 0.60 and 0.314 µm [192,195,200], a cursory look at the data may suggest that compared with the mammals, the BGB of the chicken is relatively weaker. This, however, does not appear to be the case: when the blood pressures at which the BGBs failed are normalised with the thicknesses of the basement membranes, which are the specific load bearing parts of the BGB [209,210,211,212] and which contain the load bearing collagen type-IV fibres [193,194,198] and are respectively 0.045, 0.174, 0.319 and 0.386 μm thick [191,207], it is found that the avian (chicken) BGB is 2.8 times stronger than that of the rabbit and the dog and 2.4 times stronger than the lungs of the horse. Compared to those of mammals of equivalent body mass, the mean arterial blood pressures of resting birds are generally greater: they are higher than the 20 kPa (150 mmHg) pressure that is generally reported for mammals [213,214,215,216,217,218]. For reasons that were unclear, in a study where intravenous infusion of 2,4 Dinitrophenol (DNP)—a drug that affects oxidative phosphorylation, causing a significant increase in cardiac output, as occurs during intense exercise—was infused in a chicken, West et al. [219] found that the pulmonary arterial blood pressure increase was less than that of mammals. Unfortunately, the lungs of small and more energetic species of birds have so far not been investigated.

3. Environmental Conditions, Their Impacts on Birds and Aspects That Suggest Weakening of Their Adaptive Capacities

3.1. Susceptibility of Birds to Diseases and Injuries from Foreign Particulates

The ‘One Health Concept’ arose from appreciation that human health is closely associated with the well-being of other animals as well as with the states and conditions of shared environments and habitats [220,221]. Zoonotic diseases are illnesses that are naturally transmissible between animals and human beings or vice versa [222,223]. From the close association between people and animals, especially pet and companion relationships, zoonotic diseases are an important public health concern [223,224,225,226,227,228]. Migratory birds that travel over long distances during their seasonal sojourns are important transmitters of zoonotic diseases [226,229,230,231]: they interact with various species of animals and humans during their stopovers and at their final destinations. Rural birds generally visit polluted areas such as sprayed agricultural fields while the urban ones go to contaminated places such as factories, hospitals, dump sites and waste water- and refuse-treatment plants where they pick up pathogenic microorganisms and toxic chemical substances, which they then introduce into the food chain through their droppings, carcasses and direct interactions with other animals [232].

Avian migration is a highly rewarding undertaking because birds can relocate to sites where food is assured while escaping adverse weather conditions and boosting reproductive success, but it is also highly hazardous [233]. From the strenuous work of flapping flight, these travels entail a high energy cost, the birds are exposed to scarcity or lack of food and water and they have to cope with the extreme ECs of high altitudes such as extremely low ambient temperatures, low PO₂ (hypoxia) and dry air [234,235,236]. During migration, the continuous work of flying causes muscle damage, dehydration, weight loss, weakened immunity and diseases and deaths [91,94,237,238], with immunosuppressed birds being more susceptible to diseases [239,240,241]. Human incursion into habitats that were once exclusively occupied by birds, human pursuits such as the taming and domestication of wild birds as pets or for sport, as well as an increase in farming, consumption and utilisation of poultry products have all considerably increased the possibility of pathogens crossing biological (genetic) barriers and triggering zoonotic disease outbreaks [242]. For animals, the immune system (IS) has taken at least 1000 million years to evolve to its modern state [243]. From an evolutionary perspective, the avian IS separated from the mammalian one more than 200 million years ago [244]. Recently, immunogenomic studies of the major histocompatibility complex (MHC), which in birds is an important part of the adaptive immune system responsible for pathogen detection and setting off of immune responses, have been performed on the passeriform group of birds and the Mallard Duck (Anas platyrhynchos) [245,246,247,248]: passerine birds experienced a significant adaptive departure from the basic essential MHC organisation that is characteristic of other lineages of birds, possibly enabling them to contend with greater or more diversified pathogen burdens, while for the Mallard Duck, diverse immune genes that may assist the duck in fighting the influenza virus were observed.

The structural and functional novelties of the ARS have been well-described [39,40,42,132,179,180,182,190,193,249]. Under ECs that were ostensibly different from the present ones [250], the adaptive specialisations of the ARS developed in a transactional manner [251]. Birds are notably susceptible to attacks by pathogenic microorganisms, fungi and parasites and injury via particulate matter, especially those acquired by inhalation of air [42,252,253,254,255]. The physical and cellular defences of the ARS comprise intricate processes that include filtering of air and clearance, isolation, destruction of harmful pathogenic microorganisms and particulates as well as repair of the consequent injuries [256,257,258,259]. The notable structural features that appear to make the ARS susceptible to infections, afflictions and injuries include the following:

• Compared to mammals and animals of equivalent body mass, birds have a respiratory surface area that is 15% greater, and their BGB is 56–67% thinner and the pulmonary capillary blood volume is 22% more [42,45,46].
• The exchange tissue is lined by non-ciliated cuboidal or squamous epithelia that cannot efficiently remove or destroy pathogenic microorganisms and injurious particulates that settle there [190,259].
• Lacking a diaphragmatic partitioning, with some of them having pneumatized bones, the capacious air sacs (ASs) spread extensively in the coelomic cavity [259] for some species of birds such as the ostrich (Struthio camelus), and some of the ASs leave the coelomic cavity to lie subcutaneously [42,260,261,262,263,264,265] where they are highly vulnerable to injury from trauma and subsequent infection.
• Due to the dispersion of the ASs to most parts of the avian body, diseases and infections affect different parts of the body, ultimately spreading to the lung.
• The capacious ASs affords a large tidal volume that increases the measure of pathogens and particulates that are delivered to the lung.
• Because the walls of the ASs are very thin, delicate, poorly vascularized and scantly lined by an epithelium [182,265], the ASs are highly vulnerable to attack and injury from pathogens and particulates, and because of their fragility they provide little protection to the parts/organs of the body with which they interface.

The evolution of the adaptive specialisations of the ARS evidently entailed trade-offs and compromises, with two examples described as follows:

• While paucity and lack of free avian respiratory macrophages (FARMs) on the respiratory surface of the avian lung [99,101,102] promoted gas exchange efficiency by reducing the thickness of the BGB [46,47,105], it concurrently caused the tissue barrier to become highly susceptible to structural failure [201,203] and injury from pathogens and particulates.
• While the rigidity of the avian lung supported intense subdivision of the gas exchange tissue, a process that created a large respiratory surface area, the air capillaries were apparently rendered highly vulnerable to infections and afflictions, particularly from dearth or absence of the FARMs from the respiratory surface [42,99,105,266].

Physiologically, the most important processes that make birds particularly vulnerable to respiratory infections and afflictions are the following:

• During each respiratory cycle, the large tidal volume, that stems from the large ASs leads to complete turnover of the volume of air in the lung [267], which delivers large quantities of pathogens and particulates to the lung.
• From synchronised actions of the cranial and caudal ASs, the exchange tissue of the avian lung is continuously and unidirectionally ventilated with air in a caudocranial direction, a process that increases the delivery and deposition of pathogens and injurious particulates in the exchange tissue [39,40,42,105,190].
• For diseases such as aspergillosis [239,268,269], rapid fungal growth has been attributed to the high body temperatures of birds ranging from 38 to 42 °C.
• Because inhaled air containing large quantities of pathogens and particulates is shunted to the back of the lung via the intrapulmonary primary bronchus to the caudal ASs [40,41,42,43,190], compared to the other parts of the ARS, the caudal parts of the avian body are more vulnerable to injuries from inhaled pathogens and particulates [190].

Respiratory diseases are particularly common in pet and poultry birds [269,270,271], and mortalities can cause considerable financial losses [254,272,273]. The notable susceptibility of poultry to diseases, especially respiratory ones, may also largely derive from the conditions under which the birds are kept or raised [42,273,274,275,276,277,278,279,280,281,282,283,284,285,286]. States and conditions such as overcrowding, poor ventilation, high environmental temperatures and humidities, hypoxia and high concentrations of toxic gases such as ammonia (mainly from putrefaction of faecal waste matter) and possible harsh routine procedures such as poor handling during times such as feeding, examination and medication inflict stress on birds, especially poultry [241,276,277,278,279,280,281]. Stress from adverse ECs weakens the immune system of birds, making them more susceptible to infections and afflictions [276,282,283,284,285]. The prevailing high environmental temperatures and those predicted for the future [286,287], mainly in the tropics, will exacerbate the susceptibility of birds to diseases.

3.2. Effects of Climate and Anthropogenic Habitat Devastation on Bird Life

Ongoing climate and habitat changes are some of the leading drivers of losses of biodiversity, population declines and extinctions [236,286,287,288]. Among vertebrates, birds and amphibians are the most vulnerable animal taxa [289,290,291,292,293]. Regarding the impacts of current changes in ECs on animal life, birds are the best-studied group [294,295,296]. The many enthusiastic bird watchers and bird lovers who observe, identify, enumerate and track birds across the world, contribute meaningfully to understanding their biology in various ecotopes [297,298,299,300]. Due to their involvement in activities such as eradication of pests and disease vectors, pollination of plants and dispersal of seeds, birds play vital roles in maintaining ecosystem integrity [301,302,303]. Because of their global distribution, and with some of them migrating over long distances, birds are highly vulnerable to the effects of climate and habitat change [55,290,302]; these factors adversely affect their distribution, diversity and numerical abundance [304,305,306,307,308,309].

Prediction of global warming and ensuing changes in biodiversity and extinctions of species entail complex mathematical and computational models dependent on various assumptions and are generally categorised into climate (physical) and ecological (biological) models [310,311]. The multiplicity of the methods and the differences in the assumptions lead to various scenarios [312]. To achieve more meaningful predictions, over the years, the approaches have changed from simple correlative ones to complex, process-based simulations that integrate mechanistic, demographic and evolutionary processes. The pros and cons of using different models were underscored by Bellard et al. [309]. While Species Distribution Models (SDMs) continue to be used, modern approaches address and integrate the inadequacies inherent in the SDMs by considering aspects such as niche conservatism, dispersal constraints and lack of evolutionary adaptation [313,314]. With the average global temperature predicted to rise considerably in the time to come [73], extinction rates will increase markedly [314,315,316,317,318,319,320]. By the year 2100, the expected 3.5 °C increase in the Earth’s surface temperature will cause extinctions of 600 to 900 species of birds of which 89% of them will be in the tropics [317]. In future, climate change is expected to accelerate at a rate 20 times faster than it has at any time during the last 2 million years [319]. The process will lead to severe ecological range contractions [318]. Birds with poor capacity to vacate stressful habitats, e.g., flightless birds, will face greater danger of extinction [290]. Certain species of birds are more vulnerable to the effects of climate change than others [298]. Generally, depending on the nature and the degree of susceptibility, species with extreme traits such as small body size are, compared to the larger ones, at greater risk of population decline and extinction from changes in ECs [320,321,322]. For evolutionary ‘older’ (‘ancestral’ or ‘basal’) species, phylogeny affects the social organisation of bird populations by increasing the size and the range of their habitats, while for ‘recent’ (derived) species, phylogeny determines species abundance [323,324]. Because extreme ECs decimate occasional species (https://www.iucnredlist.org/—accessed on 1 April 2026), regarding aspects such as body size and shape, in future, it is anticipated that birds will become more uniform [323,324,325].

For birds, climate change has considerably impacted migration and breeding timing [55,277,325,326,327]. With catastrophic consequences, loss of stopover habitats has made birds fail to reach their breeding sites on time or not at all [286,289,328,329,330]. Late starting and arrival times are a common cause of the decline in migratory bird populations [325,327,331,332,333]. Disorganised food webs, altered breeding seasons, reduced survival and reproduction rates, increased disease incidents, changes in ecological ranges and population declines are indicators of the adverse effects that altered ECs are having on animal life [55,289,334,335,336,337]. Haile [337] and Radchuk et al. [338] observed that presently, certain species of birds are indicating signs of inadequacies in adjusting to the pressures they are facing from prevailing ECs, or such species may not be responding fast or adequately enough to the challenges ECs are presenting. The possible causes and explanations for the perceptible flagging of resistance of some species of birds to external stressors and invading pathogens have been investigated through the application of some of the following models:

• A ‘habitat fragmentation limiting dispersal model’ illustrates how fragmentation of a continuous habitat into smaller, isolated areas constrains the dispersal of organisms/animals and gene flow between groups, greatly increasing the likelihood of localised extinctions [334,335].
• A ‘phenological mismatch model’ is a contextual framework that used to investigate, simulate, and envisage the outcomes of out-of-phase timing between interrelating species caused by climate change [336,337]: it commonly reduces species fitness and population abundance [336,337].
• In conservation biology and evolutionary ecology, an ‘anthropogenic mortality surpassing evolutionary response rates model’ is a conjectural and mathematical schema that sculpts conditions where human-inflicted deaths happen too fast for natural selection to let the impacted population to adapt [338,339]: it causes precipitous population declines, degraded genetic diversity from inbreeding and likely local extinctions.
• In most species of animals, especially for small populations, instabilities that meaningfully increase risk of extinction can be investigated by a ‘demographic and environmental stochasticities model’ that combines randomness in individual births/deaths with environmental stochasticity, i.e., random changes in factors like weather, to determine likelihoods of species survival or extinction risk [340].
• The ‘evolutionary rescue model’ details how a population initially facing extinction due to severe environmental stress can rebound through rapid and adequate adaptation, i.e., genetic changes [341,342,343].
• A ‘species-focused, broad-based conservation strategies model’ applies an integrated approach designed to save particular endangered species while simultaneously protecting their broader ecosystems [344,345,346]: its goal is to address both immediate extinction risks and long-term ecological health.

Whilst in the past the prevailing view was that adaptation was too slow to keep pace with changes in ECs, recent models such as ‘adaptive tracking’ [65,66], ‘environmental stochastic change’ [347], ‘evolutionary rescue’ [341,342,343] and empirical investigations show that under particular states and conditions, evolution can match changes in ECs and prevent extinction. For some species of birds, the adaptive novelties that may have served them well in the past, under ostensibly different ECs, may now have rendered them unresponsive under the very different (current) extreme conditions [348,349].

3.3. Effects of Environmental Pollution on Birds

The increasing global level of environmental pollution is critically impacting the survival of animal life, including birds [55,294,295]. By causing suppression of the immune system and other factors, pollution is making birds more vulnerable to diseases, injuries and poisoning [55,295,350,351,352]. From their numerical abundance and global distribution, at various places, birds are exposed to various ECs and consequently to diverse pathogenic microorganisms and contaminants [224,353,354,355]. Birds are well-known ‘biosensors’, ‘bioindicators’ or ‘sentinels’ of environmental pollution [353,354,355,356,357,358,359,360,361,362,363,364,365,366]. Their sensitivity to changes in the ECs makes them important early-warning detectors of ecosystem threats [357]. Smith et al. [367] determined that for birds, air quality correlates with species diversity, numerical abundance and breeding success while Fry [365], Abbasi et al. [366], Sanderfoot and Holloway [356], Shore and Taggart [367], Maznikova et al. [368], Castagna et al. [369] and Vetere et al. [370] noted that in accordance with other apex predators, birds are highly susceptible to toxins and pollutants which they largely acquire from the air they breathe, foods they eat, water they drink and from physical contact with their surroundings.

Depending on the nature and the level of pollution in a habitat and the state of the suppression of the immune system, which usually occurs under various stressful conditions, birds are particularly susceptible to diseases and injuries [279,358,360,371,372,373,374]. Birds exposed to PM2.5-sized particulates have high macrophage infiltration and small lung volumes [375]. Feral pigeons exposed to inhalation of nitrogen oxides (NOx) have lower erythrocyte counts and high oxidative stress markers [373]. Liang et al. [374] reported that the decrease in the numbers of migratory warblers across North America was attributable to ozone pollution. Jat and Gurjar et al. [375] observed that air pollution seriously affects the migratory behaviours of birds.

Because of the high energetic cost of flight, which is aggravated by the effect of pollution, Hedenström [376] noted that long-distance migratory birds suffer severe metabolic stress and have relatively shorter longevities. High mortality rates of birds, low species diversity and respiratory distresses occur under altered environmental condition [377,378,379,380]. After birds were exposed to smoke from wildfire, for a time afterwards, song complexity and performance were reduced by a factor of 15% [381]. Together with deteriorating lung function, birds exposed to highly toxic gases and injurious particulates presented histopathological injuries of the respiratory tissues [359]. In different ways, compared to the mammalian respiratory system (Figure 1(16–30)), certain aspects of the morphological and physiological specialisations of the ARS (Figure 1(1–15)) [39,42,45,46,105,181] make birds susceptible to attack from pathogenic microorganisms and injury by particulates.

4. Conclusions

The evolutionary progress of birds is well-reflected in their global dispersion, remarkable speciosity, numerical abundance and the diverse lifestyles they pursue. Presently, the marked reduction in avian biodiversity and the increase in the rates of extinction are largely driven by ongoing harsh ECs that include global warming, environmental pollution and habitat devastation. Some of the results inflicted by the ECs on birds include high susceptibility to diseases, especially those acquired through the respiratory system, and the inability to sufficiently respond to physiological challenges such as heat loading. Caged birds are particularly vulnerable to conditions like hyperthermia, which may arise from poor physiological thermoregulatory capacity [277,382,383]. Extreme environmental temperatures negatively affect bird health [384,385,386]. This is particularly worrisome because modelling studies have predicted that temperature will continue to rise for the rest of this (21st) century [387,388,389]. In particular, migratory birds will face multiple challenges such as devastation of their stopover habitats, deaths from extreme weather conditions and food and water scarcity. Seabirds are presently among the most threatened group of birds [390,391].

By prevailing over onerous population chokepoints and adapting to new habitats [392,393], naturally, by behavioural and phenotypic changes, certain species of birds have shown remarkable rebounds after teetering on the verge of extinction, largely from brutal habitat loss, hunting and pesticide poisoning. For example, in the Pacific Flyway of North America, between the years 1970 and 2022, the estimated spring population of the Lesser Snow Geese (Anser caerulescens caerulescens) increased from ~300,000 to ~2,300,000 [394]: the increase was attributed mainly to high per-capita productivity in the Western Arctic and immigration to Wrangel Island. Various species of birds are, however, facing rates of EC-related changes that they may not be able to adequately adjust to, and they may consequently be suffering a perilous mismatch between adaptive traits (phenotypic) and climatic changes [353,354,394,395]. Some of the models, indices or metrics that have been used to assess and rate the adaptive changes and endurance capacities of birds’ relative changes in response to ECs include the following:

• ‘Estimated evolutionary rates’, when applied to Galápagos finches [396,397] and the Great Tit (Parus major) [398], showed that phenotypic evolution can occur very fast in response to ECs.
• In ecosystems facing rapid disruption, the ‘climate velocity’ or ‘velocity of climate change’ model determines the rapidity and the trajectory that climatic conditions change over the surface of the Earth, expressed in km.year⁻¹ [399]. This value speaks to the rate at which species must travel, i.e., migrate, to preserve their existing climate niche.
• Representing the mean age of parents of a new cohort and in every respect driving how species react to ecological, demographic and ECs over time, ‘the generation time and temporal scaling in birds model’ is an important rating factor for population dynamics, where longer generation times correlate to robust total density reliance and greater scale of environmental unpredictability [400].

Bird populations are increasing or decreasing from both their capacity to adapt to anthropogenic driven effects and ecological and life-history specialisations. Generalist species that can adapt to various ECs are thriving while specialist ones, which require intact habitats, are declining [73,74,93,96,97]. Generally, species that are prospering usually have traits that permit them to exploit new or distressed environments [401]. The factors and reasons that explain why and how some species of bird and populations prosper while others decline or wane include the following, among others.

Prospering:

• Rapid reproduction rate;
• Dietary and habitat flexibility;
• Effective adaptation to ECs;
• Exploiting (adjusting to), rather than resisting, anthropogenetic effects.

Declining:

• Living in specialist niches;
• Developing habitat loss and fragmentation;
• Migratory hazards;
• Increasing nest predation, especially for ground-nesting species;
• Invasion of exotic species that outcompete the native ones for resources;
• Climate-driven phenological mismatch which moves resource (food) availability out of phase with aspects such as breeding season;
• Intensification of agricultural activities through the use of new methods and toxic agents such as pesticide spraying [402,403,404,405,406].

In birds, life-history traits are robust predictors of resilience in response to changing ECs [407,408]: species with fast reproduction rates cope better from sudden disruptions while those with slow rates are usually more at risk, despite possessing greater resistance to certain stressors. Because of its broad predictive power, especially of a species’ capacity to endure, disperse and adapt, compared to specialised, single-trait considerations such as respiratory specialisations, the generalist–specialist continuum is commonly deemed an outstanding backdrop for explicating inclusive ecological patterns such as distribution, abundance and responses of a species to ECs [409]. Because of extreme pressures emanating from the prevailing extreme ECs, conservation of birds, especially threatened and endangered species, is warranted. Recognising the vital biological and ecosystem parameters that herald environmental stresses may allow timely conservation interventions [395]. In birds, biomarkers of early stress, which are generally classified into endocrine, oxidative and haematological markers, are important indicators of environmental pressures that physiologically threaten long-term fitness and survival [410,411,412,413]. For birds, feather corticosterone (fCORT or FCORT), reactive oxygen species (ROS) and antioxidants, blood heterophils-to-lymphocytes ratio, haematocrit, telomere shortening, immune cell counts and morphological changes are commonly used to assess stress [408,409]. A good understanding of the levels of production affecting molecular stress biomarkers and the states and conditions the birds are at when they are produced would be important in determining the tension(s) birds are under and their state of health in general, and they may be useful in anticipating future outcomes [414,415,416]. Regrettably, for many species of birds, current data on biological and ecological ‘tipping points’—i.e., the critical thresholds where extra (even modest) pressures trigger significant sudden, self-perpetuating ecosystem changes (often irreversible) from a stable state to a different (chaotic or worse) condition—are lacking [411,412]. Such details can be meaningfully leveraged to enhance conservation efforts. It is interesting to note that while climate is generally disdained as harmful to biodiversity [309], interestingly, it benefits certain bird populations by, e.g., increasing food availability, affording milder winters and extending habitats, especially at higher altitudes and latitudes and by driving phenological adaptation [416]. However, such changes are likely to benefit generalist species over specialist ones, resulting in a complex reorganisation of bird communities instead of causing a net increase in biodiversity [417].