Light and Environment: Regulation of Seasonal Reproduction in Wild Birds

Simple Summary

Birds have developed sophisticated ways to synchronize their reproduction with the best time of the year for raising chicks. In temperate regions, most species reproduce only when food is abundant, and weather conditions are favorable. The main environmental signal to start or stop breeding is the photoperiod, defined by the number of daylight hours relative to the 24 h cycle. Light is detected not only by the eyes, but also by special brain receptors, which trigger hormonal signals that activate or suppress reproduction. Other factors, such as temperature, rainfall, food availability, environmental stress, social interactions, and even artificial light, can advance, delay, or stop reproduction. This flexibility is crucial for survival, but it also makes birds vulnerable to rapid changes in climate and human-modified environments. Understanding how birds adjust their reproduction to the seasons helps to predict the effects of global change supporting the conservation of species.

Abstract

Reproductive seasonality in birds represents a key ecological adaptation that ensures synchronization between breeding activity and optimal environmental conditions for offspring survival and development. Photoperiod is the primary cue regulating the hypothalamic–pituitary–gonadal (HPG) axis, through brain photoreceptors and pineal melatonin secretion. Increasing day length induces thyroid hormone activation by hypothalamic type 2 deiodinase (DIO2), stimulates gonadotropin-releasing hormone (GnRH) secretion, and promotes gonadal growth, whereas prolonged exposure to long days triggers photorefractoriness, which has been linked to increased hypothalamic type 3 deiodinase (DIO3) expression in several studies, although the causal role of this enzyme remains under investigation. Secondary environmental modulators, such as temperature, food supply, precipitation, and social interactions, also play crucial roles in fine-tuning reproductive timing. Moreover, anthropogenic factors like artificial light at night can disrupt circadian and seasonal regulation, causing mismatches between breeding and food availability. Evidence from diverse species, including passerines, galliforms, waterfowl, and raptors, demonstrates both conserved mechanisms and ecological plasticity, with tropical and urban species showing more opportunistic breeding strategies. These findings highlight the multifactorial and flexible nature of avian reproductive cycles, underlining their vulnerability to climate change and habitat anthropization. Considering this, this review aimed to understand the neuroendocrine and environmental control of seasonality and to offer an integrative perspective on how light, hormones, and environmental factors interact to shape seasonal reproduction in wild birds.

1. Introduction

Reproductive seasonality in birds represents one of the most refined strategies of ecological adaptation. By synchronizing the sexual cycle with the most favorable seasons, these species maximize the survival of their offspring [1,2,3]. In regions with pronounced seasonality, most birds concentrate reproduction within a short window, usually between the end of winter and the beginning of summer, when there is greater availability of food and favorable climatic conditions for the development of chicks. This ability for temporal adjustment is the result of selective pressures that shaped the avian neuroendocrine system throughout evolution, making it sensitive to environmental markers. Among these, photoperiod stands out as the main regulator of the seasonal activation of the reproductive system [2,3,4].

The temporal control of the seasonal reproductive cycle generally involves three interdependent physiological states: photosensitive, photo-stimulatory, and photorefractory [2,5,6]. In the initial step of photoperception, light is detected not only by the eyes and pineal gland [7,8,9,10] but, by deep-brain photoreceptors located in the basal hypothalamus [11,12], which directly connect to neuroendocrine centers. This perception represents the entry point of photoperiodic information and establishes the foundation for subsequent responses [2,6,13].

In the photosensitive state, birds maintained under short photoperiod remain reproductively quiescent but in a responsive condition. Once increasing day length is detected by deep-brain photoreceptors, the transition to the photo-stimulatory state occurs, activating the hypothalamic–pituitary–gonadal (HPG) axis, resulting in gonadal growth, increased levels of sex hormones, and the onset of spermatogenesis in males, while in females it promotes follicular maturation and ovulation [2,3,14]. At the end of the reproductive season, many species enter the photorefractory state, a period of reduced responsiveness to long-day stimulation [5]. In birds that display absolute photorefractoriness, the testes regress even under long photoperiods [5], whereas in species with relative photorefractoriness, gonadal development can be maintained despite continuous long-day exposure [2], reflecting a partial and reversible loss of photosensitivity that allows reproduction to persist under favorable environmental conditions. Exit from this refractory state requires prolonged exposure to short days, a process mediated by local thyroid hormone conversion in the mediobasal hypothalamus, which provides the key timing signal that gates GnRH release and transitions between reproductive states [6,11,12,13].

Photoperiod therefore acts as the primary environmental marker of time, triggering a cascade of neuroendocrine events that regulate annual reproductive cycles with remarkable precision. Increasing day length is detected by deep-brain photoreceptors in the diencephalon, which transduce light signals into hormonal outputs through the hypothalamic–pituitary–gonadal (HPG) axis [11,15,16,17]. A central element of this pathway is the thyroidal switch mediated by type 2 and type 3 deiodinases (DIO2/DIO3), which control local availability of triiodothyronine (T3) in the mediobasal hypothalamus, thereby gating GnRH secretion and the transition between reproductive states [6,18]. Additionally, the pineal gland contributes primarily to circadian regulation through the rhythmic secretion of melatonin, which conveys information about daily light–dark cycles and indirectly modulates seasonal physiology. Pineal signals interact with hypothalamic pathways to fine-tune reproductive timing and synchronize it with environmental cycles [7,19,20].

Yet, these patterns are far from universal. Different species, and sometimes even different populations of the same species, display unique photoperiodic thresholds, variable speeds of gonadal activation, and distinct reliance on light-detection pathways [21,22,23]. On top of that, secondary factors, including temperature, rainfall, food supply, and social context, often play decisive roles, particularly in tropical or urban birds that rely on more flexible, opportunistic breeding strategies [24,25,26,27,28,29,30]. Human-driven influences add further complexity. Artificial light at night (ALAN), for instance, can sometimes accelerate reproductive activation at moderate levels, but at higher intensities it may disrupt circadian rhythms and reduce breeding success [31,32,33]. Its overall impact remains debated. For many groups, detailed studies are still scarce, leaving important gaps in knowledge.

In this review, the aim is to synthesizes what is currently known about the neuroendocrine and environmental regulation of avian reproductive seasonality, considering how these mechanisms may be reshaped by global challenges such as climate change and urbanization. Ultimately, the goal is also to provide an integrated perspective that can be understood across disciplines, while remaining rooted in the physiological and ecological details that define avian reproduction.

2. Neuroendocrine Axis and Molecular Mechanisms of Reproductive Seasonality

Photoperiod provides a reliable external signal for the initiation of the breeding season in birds, ensuring that reproductive activity begins under favorable environmental conditions. However, the mechanisms controlling the termination of breeding are not always governed directly by day length. In species that display absolute or relative photorefractoriness, the end of reproduction is instead regulated by endogenous timing processes that rely on internal oscillations fine-tuned by light cues throughout the annual cycle [2,5]. In this context, the neuroendocrine axes gain prominence, functioning as the bridge between the external perception of light and the physiological responses that mark each phase of the reproductive cycle. These systems integrate information between the brain, pituitary gland, thyroid, adenohypophysis and gonads, to coordinate seasonal changes in metabolism, gonadal growth, and reproductive behavior [34]. Thus, avian reproductive flexibility emerges from the interplay between environmental sensitivity and the complexity of hormonal feedback circuits [2,20,35].

During the photosensitivity phase, neuroendocrine responses are triggered once a population-specific critical photoperiod is reached. This threshold varies even within a species, as demonstrated in great tits (Parus major), where southern populations initiate gonadal growth at shorter day lengths than northern ones [36]. Beyond these differences, the circadian organization underlying photoperiodic responses in birds is more distributed than in mammals. Whereas the mammalian suprachiasmatic nucleus (SCN) functions as the main circadian pacemaker, birds possess multiple oscillators that include the eyes, pineal gland, and diencephalic nuclei, that cooperate to regulate daily and seasonal timing [8,37]. The avian SCN comprises a medial (mSCN) and a visual (vSCN) component, with the former expressing circadian clock genes and being essential for maintaining rhythmicity, while the latter receives retinal inputs but does not function as an independent oscillator [38,39]. The contribution of each center differs across species: in House sparrows (Passer domesticus), for example, the pineal gland is essential for the maintenance of circadian rhythm in the absence of light variations [40], whereas in Japanese quail (Coturnix japonica), the retina plays a predominant role in the capture of light [37]. In Rock dove (Columba livia), both the retina and pineal gland cooperate to synchronize rhythmic activity with environmental cycles [8].

In the seasonal context, light perception in birds extends beyond the eyes and pineal gland, occurring through deep-brain photoreceptors located in the basal hypothalamus, the pars tuberalis of the adenohypophysis, and the roof of the diencephalon [12,41]. Classic experiments in Japanese quail demonstrated that even after removal of both eyes and pineal gland, individuals retained normal gonadal responses to photoperiod, confirming that deep-brain receptors alone can drive seasonal reproduction [42]. Subsequent molecular studies in quail and chicken revealed that these photoreceptors activate a thyroidal switch within the mediobasal hypothalamus (MBH), where reciprocal regulation between activating and inactivating pathways of thyroid hormone metabolism links photoperiodic input to gonadal activation [6,13]. Opsins expressed in the avian brain, particularly Vertebrate Ancient Opsin (VA-opsin, OPNVA) and neuropsin (OPN5), mediate this pathway between light detection and thyroidal signaling [11]. More recent work in waterfowl has expanded this framework: in mountain ducks, OPN5 regulates follicular development via thyroidal signaling [16], while ontogeny studies in domestic ducks revealed that melanopsin (OPN4) is expressed at near-adult levels immediately after hatching, suggesting early neuroendocrine functions, whereas OPN5 expression increases later coinciding with puberty and GnRH activation [43]. Together, these findings show that deep-brain photoreceptors contribute in a temporally structured manner, from shaping early development to orchestrating full reproductive activation.

As time progresses, birds enter the photo-stimulatory state, in which light perception mediated by opsins such as OPN5 and OPNVA in the hypothalamus initiates a cascade of neuroendocrine events [11,12]. The pars tuberalis of the pituitary then secretes thyroid-stimulating hormone beta (TSHβ), which acts on tanycytes, specialized glial cells located on the floor of the third ventricle (3V) to modulate local thyroid hormone conversion [13]. Importantly, circadian timing refines this process. Almost all cells express clock genes, but only certain structures act as master clocks: in birds, the retina, pineal gland, and suprachiasmatic nucleus (SCN) form the core circadian pacemaker, while the mediobasal hypothalamus (MBH) functions as a seasonal timing center linking photoperiodic information to thyroidal and gonadotropic responses [39,44]. The MBH exhibits stable rhythmic expression of several clock genes, including Per1, Per2, Cry1, Cry2, Clock, Bmal1, and E4bp4, across photoperiodic conditions, supporting its key role in the integration of circadian and seasonal signals [44]. The pars tuberalis also expresses some of these genes, such as Per2 and E4bp4, as demonstrated in Japanese quail [44], but their rhythmic fluctuations appear unrelated to photoperiodic time measurement. Instead, the PT acts mainly downstream, aligning TSHβ secretion with melatonin-driven signals rather than serving as an independent pacemaker [44]. This hierarchical organization ensures that the switch in thyroidal activity and the resulting rise in hypothalamic T3 occur at the appropriate phase, providing the precise timing signal for GnRH release and seasonal reproductive activation [6].

Tanycytes then stimulate the expression of the enzyme deiodinase type II (DIO2), which is responsible for the conversion of thyroxine (T4) into triiodothyronine (T3), the active form of thyroid hormone, which increases its local levels in the hypothalamus. This increase in T3 activates neurons of the medial preoptic nucleus, stimulating the production of gonadotropin-releasing hormone type I (GnRH-I) (Figure 1) [11,13,16,45].

This sustained increase in GnRH-I secretion induces pituitary release of follicle-stimulating hormone (FSH) and luteinizing hormone (LH), which act in a coordinated manner on the gonads. In males, LH regulates the production of sex steroids, whereas FSH supports spermatogenesis through its action on Sertoli cells [35,46,47].

In females, luteinizing hormone (LH) acts on the theca cells, stimulating them to produce androgens such as androstenedione and testosterone. These androgens are then converted into estradiol by the granulosa cells under the direct influence of follicle-stimulating hormone (FSH). The coordinated action of LH and FSH is therefore fundamental for ovarian steroidogenesis and follicular growth in birds [48,49]. Classic studies in chickens revealed that this steroidogenic activity is spatially divided within the follicle: granulosa cells are the main source of progesterone; theca interna cells, under LH stimulation, convert this progesterone into androgens; and theca externa cells, influenced by FSH, contribute to estradiol synthesis through aromatization [50,51]. Taken together, these findings show a well-orchestrated system: estradiol prepares the female body by promoting vitellogenesis and oviduct development, but it is the sharp rise in progesterone secreted by the granulosa cells of the dominant follicle that ultimately triggers the preovulatory LH surge and ovulation [52,53,54,55,56].

As the preovulatory follicle (F1) matures, its granulosa cells undergo a functional shift: instead of producing primarily estrogens under FSH regulation, they progressively acquire luteinizing hormone receptors (LHCGR) and upregulate key steroidogenic enzymes such as 3β-hydroxysteroid dehydrogenase (3β-HSD). This molecular reprogramming, demonstrated by recent transcriptomic studies [54], enables the granulosa cells to switch from estrogen production to robust progesterone synthesis in response to LH. Early physiological studies had already shown that progesterone and LH interact in a positive feedback loop that culminates in the preovulatory LH surge [52,57]. In vitro studies confirmed that granulosa from the largest follicle responds directly to LH with a marked increase in progesterone secretion [53]. Plasma hormone profiles further reinforce this model: progesterone concentrations rise sharply 4–6 h before ovulation, coinciding with the LH surge, while estradiol levels decline as the F1 follicle becomes predominantly luteogenic [55,56]. Together, these findings clarify that while estradiol orchestrates the preparatory phase of reproduction, it is the progesterone surge from the dominant follicle that acts as the immediate trigger for the LH peak and ovulation.

However, this complex endocrine system does not remain active indefinitely. Near the end of the breeding season, many bird species enter a photorefractory state, during which reproductive responses to long days wane. In some models, this state has been linked to changes in thyroid hormone metabolism within the mediobasal hypothalamus (MBH): quail and sparrows, for example, exhibit sustained DIO2 expression and low DIO3 during refractoriness, indicating that suppression of GnRH secretion can occur independently of DIO3 induction [6,13,16,23,58]. Under short photoperiods, DIO3 expression increases markedly in the MBH, where it catalyzes the inner-ring deiodination of both T4 and T3, producing the inactive metabolites T3 (rT3) and T2 [6,58]. This enzymatic shift lowers local T3 availability and downregulates thyroid-dependent stimulation of GnRH neurons, thereby facilitating gonadal regression and the onset of photorefractoriness. Collectively, DIO3 serves as the inhibitory counterpart of DIO2 within the thyroidal switch of the MBH, and the reciprocal balance between both enzymes determines the local T3 signal that orchestrates the activation or cessation of seasonal reproduction [13,58]. This reciprocal regulation of DIO2 and DIO3 is driven by thyrotropin (TSHβ) released from the pars tuberalis, which acts on tanycytes in the MBH to modulate local thyroid hormone metabolism and thereby synchronize reproductive timing with photoperiodic input [13,16,58]. Thus, photorefractoriness is not a uniform phenomenon but reflects species-specific strategies to terminate reproduction. Consistent with a central thyroidal control point, the intracerebral administration of thyroid-stimulating hormone (TSH) to quail maintained under short photoperiods restored reproductive activity through enhanced local thyroid hormone activation in the hypothalamus [13,16].

In parallel to these mechanisms, melatonin, a hormone secreted by the pineal gland during darkness acts on the hypothalamic–pituitary–gonadal axis by modulating GnIH neurons. In Japanese quail, melatonin induces GnIH expression in the paraventricular nucleus of the hypothalamus through the direct activation of Mel1c receptors present on GnIH-producing neurons, stimulating the synthesis and release of this inhibitory neuropeptide [59]. This induction is further increased under short photoperiods, when nocturnal melatonin secretion is prolonged. Therefore, the increase in GnIH levels reduces the pituitary release of LH and FSH, resulting in suppression of the reproductive axis during unfavorable periods [60,61]. Corroborating these findings, studies in quail have shown that the administration of anti-melatonin antibodies during short photoperiods reactivates testicular growth [62].

The pineal gland of birds also actively contributes to intracranial light perception, expressing photoreceptors such as pinopsin, a light-sensitive opsin that directly regulates the circadian rhythm of melatonin synthesis [9,10]. In laying hens, different light regimes modulate the expression of the melanopsin gene (Opn4) in the pineal gland, in addition to altering the serum levels of melatonin [63]. In geese (Anser cygnoides), an elevated melatonin levels under a short photoperiod can suppress the expression of GnRH and gonadotropins, interrupting seasonal reproduction [64].

In addition to being modulated by melatonin, GnIH shifts in step with the seasonal rhythm of the neuroendocrine system. During short days, its expression in the paraventricular nucleus of the hypothalamus increases, while GnRH-I expression decreases, leading to lower plasma LH concentrations and regression of gonadal activity. This indicates that GnIH acts as a key inhibitory modulator that reinforces photoperiodic suppression of reproduction, acting in concert with thyroidal and melatonergic pathways [60,65]. In adult quails, the administration of GnIH reduced circulating levels of LH and testosterone in a dose-dependent manner, causing testicular atrophy and inhibition of spermatogenesis. In young birds, the administration of GnIH blocked testicular growth and delayed molt [65].

Another relevant aspect of GnIH is its direct action on the pituitary gland, where it reduces the responsiveness of gonadotropic cells to GnRH-I. In chickens, treatments with estradiol and progesterone decrease GnIH receptor expression in the pituitary gland, suggesting a feedback circuit between sex steroids and the GnIH–gonadotropin axis [66].

In addition to the direct effects of melatonin and gonadotropic hormones, recent studies have highlighted the role of vasoactive intestinal peptide (VIP) and prolactin (PRL) as mediators of reproductive seasonality in birds. VIP has been recognized for decades as a potent hypothalamic factor in the release of PRL in birds, as initially demonstrated in turkeys (Meleagris gallopavo) [67]. In Japanese quail, active immunization against OPN5 significantly reduces the expression of VIP and thyroid-stimulating hormone (TRH) in the basal hypothalamus under a short photoperiod, resulting in a subsequent decrease in the pituitary expression of PRL and in the ovarian prolactin receptor (PRLR) [68].

In agreement with these findings, exogenous administration of PRL in laying hens promotes ovarian follicular development and egg production [67,69]. On the other hand, situations of prolonged PRL excess show the opposite effect. In Yangzhou geese (Anser cygnoides domesticus), a peak in the ovarian expression of PRL and PRLR near the summer solstice coincides with the onset of photorefractoriness and gonadal regression [64]. These results suggest that high and prolonged levels of PRL, under extreme photoperiod, may inhibit ovarian function. This hypothesis is supported by studies in other geese that associate PRL increase with brooding behavior and suppression of laying [70]. Thus, prolactin exerts a dual function depending on the photoperiodic context: under moderate levels it supports reproduction by promoting follicular development and egg production, whereas when sustained at high levels it contributes to the onset of photorefractoriness. Importantly, this action is not isolated but occurs in integration with other regulatory signals, including GnIH, melatonin, and thyroidal pathways, forming a multifactorial network that governs the seasonal decline of reproductive activity [64,67,69,70].

In species from temperate zones, GnIH expression often rises during non-reproductive phases, particularly in autumn, suggesting a possible association with the transition to photorefractoriness. For example, House sparrows show a significant increase in GnIH-immunoreactive neurons in late summer and autumn, as well as in stressful situations during the breeding season [71]. These findings indicate that GnIH may function as a physiological integrator between environmental stress and the cessation of reproductive activity, although its precise role in photorefractoriness remains to be clarified.

Beyond the core GnRH–GnIH framework, additional modulatory neurohormones exert indirect but significant control over the hypothalamic–pituitary–gonadal axis in birds. Kisspeptin, for instance, has been identified immunohistochemically in the preoptic area and hypothalamus of the mallard drake (Anas platyrhynchos), where it likely contributes to the regulation of GnRH neurons [72]. Experimental studies have demonstrated that repeated administration of kisspeptin-10 in juvenile quail accelerates gonadal maturation and the onset of egg-laying, while in chicken granulosa cells it stimulates progesterone secretion, supporting a paracrine role in ovarian steroidogenesis [73,74]. Despite these functional indications, genomic analyses reveal that the Kiss1 gene and its receptor GPR54 are absent or highly degenerated in most avian lineages, with Kiss2-like sequences identified only in a few taxa such as ducks, pigeons, and zebra finches [75]. These findings suggest that, although the mammalian KISS–GPR54 signaling pathway is not conserved in birds, kisspeptin-like peptides may still act through alternative receptors or parallel pathways to influence reproductive activation.

Another integrative signal is provided by neuropeptide Y (NPY), which connects energy homeostasis to the reproductive axis. NPY and its multiple receptor subtypes (Y1–Y7) are expressed in the avian hypothalamus, telencephalon, and anterior pituitary, where they modulate GnRH release and pituitary gonadotropin secretion in response to metabolic and photoperiodic cues [76,77,78]. Acting as both a metabolic and neuroendocrine integrator, NPY are suggested to be involved in the regulation feeding behavior, lipid mobilization, and hypothalamic activity, thereby coupling energetic state with the readiness for gonadal recrudescence [79,80,81,82].

In parallel, thyroid hormones, particularly thyroxine (T4) and its active form triiodothyronine (T3), play a multifaceted role in synchronizing metabolic state, growth, and reproductive timing. Beyond their conversion through DIO2 and DIO3, these hormones create a dynamic interface between the hypothalamic–pituitary–thyroid (HPT) and hypothalamic–pituitary–gonadal (HPG) axes [18,20,83]. Circulating T4 and T3 levels fluctuate across the annual cycle, coordinating metabolic rate, molt, and body condition with the energetic demands of reproduction [84,85,86]. Experimental suppression of thyroid activity inhibits pre-nuptial molt and gonadal recrudescence, whereas T4 replacement restores both processes, confirming its upstream regulatory role [84]. At the gonadal level, T3 enhances the responsiveness of Leydig and granulosa cells to gonadotropins, facilitating steroidogenesis and gametogenic activity [14,87]. In addition, thyroid hormones contribute to neural plasticity in seasonal species, supporting neuronal recruitment and glial within brain regions associated with reproductive and vocal behavior [88].

Although these modulatory pathways appear to play key integrative roles linking environmental and metabolic information to reproductive activation, their mechanisms remain poorly characterized across avian orders. Further comparative and functional studies are therefore needed to clarify the evolutionary conservation, tissue-specific signaling, and physiological significance of kisspeptin, NPY, and thyroidal pathways in the seasonal control of reproduction. Importantly, these endocrine mechanisms do not act in isolation but operate within an ecological framework in which environmental conditions continuously shape hormonal responsiveness and reproductive outcomes. Tropical and subtropical birds may display marked plasticity, adjusting reproduction not only to photoperiod but also to temperature, food supply and social stimuli [30,89,90,91].

3. Interaction with Secondary Environmental Factors

Beyond photoperiodic control, several environmental variables further shape the timing and intensity of avian reproduction. Temperature, food availability, social cues, and light pollution can modify gene expression, hormone secretion, and gonadal function through their action on the hypothalamus–pituitary–gonadal (HPG) axis, even under day lengths that normally promote breeding [2,3,21,23,31,32]. However, the magnitude and nature of these responses vary among orders, species and populations, reflecting phylogenetic differences, life history strategies and ecological adaptations [29,92].

Table 1. Positive and negative reproductive responses to the secondary environmental and anthropogenic factors studied for each species.

Order and Family	Species and Common Name	Modulating Environmental Factor	Observed Response/Effect	Reference
Accipitriformes Accipitridae	Accipiter cooperii Cooper’s hawk	Food; Breeding density	High prey and nest density increased extra-pair mating and brood parasitism.	[93]
Accipitriformes Accipitridae	Aquila chrysaetos Golden eagle	Temperature; Food	High prey abundance and mild weather increased nesting success, while cold or hot springs reduced productivity.	[27]
Accipitriformes Accipitridae	Buteo buteo Common buzzard	Temperature; Precipitation	Cold, wet years reduced lifespan and reproductive success; warm, dry years increased fitness.	[94]
Accipitriformes Accipitridae	Gyps coprotheres Cape vulture	Social environment	High rates of extra-pair and same-sex mating linked to confined social structure and partner limitation.	[95]
Accipitriformes Accipitridae	Milvus migrans Black kite	Precipitation; Temperature	Cold and wet weather reduced foraging success, nestling growth, and fledging rates; mild, dry conditions enhanced hunting efficiency, chick condition, and reproductive output.	[26,96]
Accipitriformes Passeriformes Piciformes Strigiformes	B. jamaicensis; P. domesticus, C. brachyrhynchos, T. Migratorius; C. auratus; B. virginianus	ALAN	Eye shape and size changed over time and with human density across six urban bird species with different responses to night lighting, suggesting adaptation to artificial light.	[97]
Anseriformes Anatidae	Alopochen aegyptiaca Egyptian goose	Temperature	Heat caused tubular atrophy, germline necrosis and testosterone drop associated with oxidative stress and testicular inflammation	[98]
Columbiformes Columbidae	Streptopelia risorii Ring dove	Social environment	Distinct coo-call types linked to courtship, threat, and territorial contexts; vocal behavior varies with reproductive condition.	[99,100,101,102,103,104,105]
Falconiformes Falconidae	Falco berigora Brown falcon	Temperature; Precipitation	Heavy rain caused nest failure and adult mortality; dry, mild years improved breeding success and survival.	[106]
Falconiformes Falconidae	Falco mexicanus Prairie falcon	Food; Precipitation	Breeding success increased with abundant prey and dry weather; declined in wet years and food shortage.	[107]
Falconiformes Falconidae	Falco naumanni Lesser kestrel	Temperature; Precipitation	Moderate rain and mild temperatures improved breeding success; heavy rain during nesting reduced chick survival.	[24]
Falconiformes Falconidae	Falco sparverius American kestrel	Temperature; Precipitation; Food	Cold, wet weather reduced chick survival by limiting prey access; extra food helped females but not offspring outcomes.	[108]
Falconiformes Falconidae	Falco tinnunculus Eurasian kestrel	Food	High prey abundance increased polygyny and clutch size; food shortage reduced breeding success.	[109]
Falconiformes Falconidae	Polihierax semitorquatus African pygmy falcon	Social environment	Cooperative groups and helpers improved chick condition and survival in large broods; higher colony density increased copulation rate and mate guarding.	[110,111,112]
Galliformes Phasianidae	Coturnix japonica Japanese quail	Temperature; Food and water restriction	Heat or resource scarcity caused testicular degeneration, oxidative stress, reduced sex steroids, and lower sperm quality, associated with decreased ERα expression and antioxidant activity.	[113,114]
Galliformes Phasianidae	Gallus g. domesticus Chicken	Temperature; Water restriction	Heat or water restriction caused oxidative stress, apoptosis, lower sex steroids, and testicular degeneration.	[115,116]
Passeriformes Aegithalidae	Aegithalos concinnus Black-throated tit	Temperature	Warmer weather shortened incubation slightly; hatching success and chick growth unchanged.	[117]
Passeriformes Aegithalidae	Aegithalos glaucogularis Silver-throated tit	Temperature	Higher temperatures shortened incubation more strongly than in black-throated tits; no effect on hatching or chick growth.	[117]
Passeriformes Corvidae	Aphelocoma coerulescens Florida scrub-jay	Food	Extra or high-protein food advanced breeding, increased clutch size and fledgling success, and lowered stress hormones.	[118,119]
Passeriformes Corvidae	Corvus c. corone Carrion crow	Social environment	Larger groups with helpers bred more successfully.	[120,121]
Passeriformes Corvidae	Gymnorhinus cyanocephalus Pinyon jay	Food	Abundant piñon seeds allowed breeding in both winter and summer; food and day length worked together to speed gonadal growth.	[122]
Passeriformes Emberizidae	Emberiza melanocephala Black-headed bunting	Temperature	Warm conditions increased testosterone, fat and muscle buildup, and migratory and breeding readiness.	[123]
Passeriformes Emberizidae	Emberiza rutila Chestnut bunting	ALAN	ALAN delayed sleep onset, reduced sleep duration, and increased nocturnal awakenings; strongest effect under green and yellow light, intensity-dependent.	[124]
Passeriformes Emberizidae	Zonotrichia l. gambelii White-crowned sparrow	Social Environment	Social cues (male song and visual presence) accelerate ovarian growth only under suprathreshold photoperiods, without shifting the critical day length.	[125,126,127]
Passeriformes Emberizidae	Zonotrichia l. oriantha White-crowned Sparrow	Temperature; Climate	Cold and snow temporarily delay or suppress gonadal growth and lower LH and thyroid hormones; gonadal activity resumes rapidly with warming.	[23,29,128]
Passeriformes Emberizidae	Zonotrichia l. pugetensis White-crowned sparrow	Temperature	Low ambient temperatures delay gonadal development and reduce plasma LH even under long days, indicating thermal modulation of photoperiodic activation.	[129]
Passeriformes Estrildidae	Taeniopygia guttata Zebra finch	Temperature; ALAN	Broad thermal tolerance (−5 to 46 °C) but low incubation temperature (35.9 °C) delayed hatching, increased oxidative stress, and reduced adult survival; ALAN induced nocturnal feeding, fat gain, lower melatonin and thyroxine, and metabolic imbalance.	[130,131,132]
Passeriformes Fringillidae	Haemorhous mexicanus House finch	Food	Food restriction inhibited testis growth and GnRH release, suppressing HPG activation.	[28,133]
Passeriformes Fringillidae	Junco hyemalis Dark-eyed junco	ALAN; Latitude	Northern populations are more sensitive to ALAN; differences in photoperiod threshold; reproductive anticipation under artificial light	[22,31]
Passeriformes Fringillidae	Loxia curvirostra Red crossbill	Food	When food was abundant, birds developed active gonads even under short days, showing that food can replace long daylight as a breeding cue.	[134]
Passeriformes Fringillidae	Serinus canaria Canary	Social environment; Vegetation	Male song promoted nest-building, courtship, and earlier laying, especially in young females; females preferred complex or familiar songs linked to reproductive activation. Green vegetation under short days advanced breeding by several weeks.	[126]
Passeriformes Fringillidae	Spinus pinus Pine siskin	Social environment; Food	Preferred food triggered LH rise and gonadal growth in both sexes; presence of a potential mate further enhanced ovarian development and LH in females but had no effect on males.	[135,136]
Passeriformes Fringillidae Muscicapidae Turdidae	E. rubecula, T. merula, T. philomelos, P. major, C. caeruleus, F. coelebs European songbirds	ALAN	Earlier seasonal onset of dawn and dusk singing in illuminated sites.	[137]
Passeriformes Hirundinidae	Progne subis Purple martin	ALAN	White ALAN increased nestling mass but delayed fledging; pre-migration exposure advanced spring departure and arrival, risking phenological mismatch.	[138,139]
Passeriformes Melospizidae	Melospiza melodia Song sparrow	Social Environment; Temperature	Social and thermal cues modulated reproduction: territorial challenges rapidly increased brain androgens; female activity prolonged male reproductive state; warmer temperatures accelerated testicular growth and LH release.	[140,141]
Passeriformes Paridae	Cyanistes caeruleus Blue tit	ALAN	ALAN advanced morning activity, delayed rest, and increased nocturnal movement; in urban nestlings, elevated feather corticosterone.	[33,142]
Passeriformes Paridae	Parus major Great tit	ALAN	Earlier awakening and reduced sleep; lower melatonin and dose-dependent circadian shifts; higher corticosterone and lower fledging success under white/red light; earlier laying under ALAN, especially in cooler springs; altered incubation and lower energy expenditure under white/green light.	[33,143,144,145,146,147]
Passeriformes Paridae	Parus major Great tit	Temperature; Precipitation	Warmer or rapidly increasing spring temperatures advanced laying; heat and drought reduced clutch and fledging success; cold and rain caused nest failures and chick mortality.	[148,149,150,151,152]
Passeriformes Paridae	Parus major Great tit	Social environment	Preferred mates advanced laying; light advanced singing; noise raised stress and immune markers, especially in females and nestlings.	[153,154,155]
Passeriformes Passerellidae	Melozone aberti Abert’s towhee	Food	Restricted food reduced LH and testosterone levels and delayed reproductive activation.	[156]
Passeriformes Passeridae	Passer domesticus House sparrow	Social environment; ALAN	Social cues from breeding males increased female body mass, oviduct growth and egg-laying probability. White LED light made birds start activity earlier.	[157,158]
Passeriformes Passeridae	Passer montanus Tree sparrow	Temperature; ALAN	Reduction in TSHβ, DIO2 and GnRH-I expression under prolonged heat; early activation or reproductive inhibition depending on light intensity	[25,32]
Passeriformes Ploceidae	Plocepasser mahali White-browed sparrow-weaver	Social environment	Social rank influenced brain differentiation in song and reproductive areas, linking dominance to reproductive potential.	[159]
Passeriformes Ploceidae	Ploceus philippinus Indian weaver	Light intensity	Testicular growth and regression, molt, and plumage change occurred only under ≥ 500 lux; no reproductive activation under ≤ 50 lux.	[160]
Passeriformes Thamnophilidae	Hylophylax naevioides Spotted antbird	Food	Exposure to abundant prey and visual food signals accelerated testis growth and onset of reproductive activity.	[161]
Passeriformes Turdidae	Turdus merula Blackbird	ALAN; Urbanization	Artificial light advanced breeding and activity, suppressed melatonin, and accelerated gonadal growth and molt by up to one month. Chronic exposure disrupted gonadal cycles, while urban males showed earlier LH rise and reproductive activation; free-ranging birds experienced longer perceived daylength and earlier maturity.	[162,163,164,165,166,167,168,169,170]
Passeriformes Turdidae	Turdus rufiventris Rufous-bellied thrush	Urbanization; Human disturbance	Avoided people when activity was high but fed on human food after disturbance; built nests in disturbed areas, often in bromeliads, which reduced predation and maintained breeding success.	[171,172]
Passeriformes Sturnidae	Sturnus vulgaris European starling	Social environment; Light intensity	Brighter light accelerated testicular growth; presence of females further enhanced spermatogenesis and delayed regression, showing additive photic and social stimulation.	[173,174]
Psittaciformes Psittaculidae	Melopsittacus undulatus Budgerigar	ALAN; Social environment	ALAN increased body mass but reduced egg production and hatching success via melatonin suppression; male song enhanced female courtship and nesting behaviors independent of photoperiod.	[126,175]
Sphenisciformes Spheniscidae	Megadyptes antipodes Yellow-eyed penguin	Social environment	Artificial social stimuli advanced nesting activity and elevated plasma testosterone and estradiol.	[176]

provides a summary by order, family, and species, highlighting the environmental modulators and the corresponding positive or negative reproductive responses. In addition to the examples discussed in the text, the table also compiles complementary studies from other avian groups.

3.1. Temperature and Precipitation

Among secondary factors, ambient temperature and precipitation are particularly influential, acting directly on physiological processes such as steroidogenesis and gametogenesis, and indirectly by altering food availability and foraging success [25,29,31,108].

Experimental evidence in migratory Redheaded buntings (Emberiza bruniceps) demonstrated that exposure to higher ambient temperatures under long-day conditions significantly altered hypothalamic transcription of key photoperiod-responsive genes, including TSHΒ, EYA3, DIO2, GNRH and GNIH, with upregulation of TSHΒ, DIO2 and GNRH at 38 °C compared with 22 °C [177]. These findings indicate that temperature not only accelerates photoperiodic responses but can directly reshape neuroendocrine regulation of seasonal reproduction by modulating thyroidal and gonadotropic pathways.

Studies with tree sparrows (Passer montanus) revealed that prolonged exposure to heat during the photorefractory phase compromises the reactivation of the neuroendocrine system controlling reproduction, with effects detected at both the hypothalamic–pituitary–thyroid (HPT) and hypothalamic–pituitary–gonadal (HPG) axes. This suppression was evidenced by lower expression of central genes such as TSHβ, DIO2 and GnRH, and by delays in testicular development, as demonstrated by histological, hormonal and molecular analyses [25]. Beyond its impact on axis reactivation, heat stress also acts directly on the gonads, impairing gamete quality through oxidative stress and protein instability. Testis-enriched proteins such as HSPA2 are particularly sensitive to thermal stress, and their dysfunction leads to impaired spermatogenesis [178]. In roosters, the accumulation of reactive oxygen species (ROS) causes testicular damage and a decline in sperm quality, effects that can be alleviated by antioxidant supplementation [179]. Similar outcomes have been observed under toxicant exposure, where excessive ROS and altered expression of heat shock proteins (HSPs) disrupted both germ cell and Leydig cell function [180]. Together, these findings highlight oxidative imbalance and protein instability as central pathways through which heat stress undermines avian fertility [181].

In Japanese quail, continuous heat stress causes degenerative changes in the testes, increased oxidative stress and decreased sex steroid production, affecting different levels of reproductive function [113]. In Egyptian geese (Alopochen aegyptiaca), extreme heat causes severe testicular damage, including tubular atrophy, germinal necrosis and a decrease in plasma testosterone levels. These effects are attributed to processes of oxidative stress, testicular inflammation and mitochondrial dysfunction [98].

Among raptors, the brown falcon (Falco berigora) is highly sensitive to annual variations in temperature and precipitation. In hot and dry years, lower water availability reduces the supply of prey, compromising the energy balance of adults and leading to the absence of eggs or early loss of broods. In milder years, with moderate temperatures and greater rainfall, the increase in food resources and the reduction in heat stress favor the maintenance of gonadal function and stimulate reproductive behaviors, resulting in greater success of hatching and offspring survival [106]. This phenomenon may be related to an indirect mechanism in which a reduction in water availability leads to a decrease in the abundance and accessibility of prey, thus compromising the energy balance of adults. With lower caloric intake, birds can delay or suspend the activation of the reproductive axis, avoiding the high physiological costs of reproduction in a scenario of scarcity [118].

The same occurs with the American kestrel (Falco sparverius) and the prairie falcon (Falco mexicanus). The reproductive success of these species depends on the interaction between climate and food availability. Adverse conditions, such as severe winters, intense rains or extremely dry summers, can reduce the supply of prey, compromising the survival of offspring [107,108].

In the golden eagle (Aquila chrysaetos), the study by Steenhof [27], conducted with populations in western North America, revealed that severe winters with very low temperatures and greater snow cover were associated with significant decreases in hatching rates and the survival of offspring. This effect was even more evident in prey scarcity years, indicating that the climate acts not only directly, compromising the metabolism and thermoregulation of offspring but also indirectly, by making it difficult for adults to obtain food. Under these conditions, the extra foraging effort, added to the lower capture efficiency, can lead to an energy deficit that affects the initial growth of chicks.

Similarly, in the common buzzard (Buteo buteo), winter severity has a substantial impact on both annual productivity and reproductive success throughout life. Colder and longer winters reduce not only the survival of the offspring in the first year but also the probability of the adults reproducing in the following season, suggesting a residual effect that extends between seasons. Furthermore, the availability of prey affects this relationship, acting as a buffer or an amplifier of climate impact. In years of food abundance, even severe winters had attenuated effects; on the other hand, the combination of intense cold and low food supply resulted in frequent reproductive failure and lower lifetime success of the individuals [94].

The link between food scarcity, harsh winters, and reduced reproduction in birds can be further understood through the physiological consequences of negative energy balance. Under conditions of limited resources, circulating levels of glucose, insulin, and insulin-like growth factor 1 (IGF-1) decrease, weakening the stimulatory signals required for gonadal growth and pituitary LH synthesis [57,182]. Simultaneously, the reduction in circulating lipids limits cholesterol availability, the essential substrate for steroid hormone biosynthesis in the ovary and testis [57,183].

In birds, however, the classical mammalian model linking adiposity, leptin, and reproductive activation does not apply straightforwardly. Although leptin is the key lipostatic hormone in mammals, its role in avian metabolism and reproduction remains controversial [184,185,186,187,188,189]. The authentic avian leptin gene shows predominant expression in the brain and pituitary, rather than in adipose tissue suggesting a non-classical signaling role [183,188,189]. This expression pattern indicates that avian leptin may act mainly through autocrine/paracrine rather than endocrine pathways [187,189]. Experimental studies have shown that exogenous leptin administration in Japanese quail can advance puberty and modulate plasma sex-steroid concentrations under controlled conditions, supporting a permissive role in reproductive regulation [183,190]. However, there is still no direct evidence that leptin acts on the hypothalamus to regulate GnRH or GnIH activity in birds.

The experimental results in Mountain white-crowned sparrow (Zonotrichia l. oriantha) confirm the effects of low temperatures on reproduction. Under stimulating photoperiods (15 h light: 9 h dark), individuals subjected to 5 °C exhibited slower gonadal development and delayed regression, whereas higher temperatures (30 °C) accelerated these processes. Interestingly, the study showed that plasma LH levels remained stable, suggesting that temperature acts on downstream targets, such as testes and steroidogenic pathways. In addition, T4 levels were lower in cold environments, indicating metabolic deceleration. Subspecies such as White-crowned Sparrow (Zonotrichia l. pugetensis) show greater reproductive sensitivity to temperature elevation, indicating that intraspecific differences adapt to climate [29].

3.2. Availability of Food Resources

As previously mentioned, food availability is a critical modulator of reproductive seasonality. In Blackbird (Turdus merula), a continuous food supply in urban populations was associated with early activation of the HPG axis and increased LH and FSH levels, in contrast to individuals from forest populations [170]. On the other hand, food shortage induces an increase in the expression of corticosterone, a glucocorticoid that suppresses the expression of GnRH-I and reduces the secretion of gonadotropins, causing testicular regression in males and follicular atresia in females, as observed in different populations of white-crowned sparrows [23,128].

In the House finch (Haemorhous mexicanus), food restriction causes a broad physiological response, capable of affecting all levels of the HPG axis in an integrated manner. In the face of food limitation, there is a decrease in the plasma concentrations of testosterone and LH, accompanied by decreased expression of GnRH in the hypothalamus. This suppression of both central regulation and the response of the gonads reflects an adaptive strategy: the organism, upon recognizing the scarcity scenario, reduces investment in reproductive processes and avoids the high metabolic and behavioral costs of reproduction, directing energy and resources to ensure survival [28].

In contrast, feed supplementation can reverse the effects of natural scarcity and promote the onset of the breeding season and increase the success of offspring development, as demonstrated in the Florida scrub-jay (Aphelocoma coerulescens), where birds that received a supplement in their diet started reproduction earlier, produced larger broods and had greater survival of the chicks, especially in years of low natural food availability [118].

Similar patterns are observed in the common kestrel (Falco tinnunculus), where there is a seasonal decline in clutch size associated with a reduction in prey availability, an effect that can be reversed with feed supplementation [109]. Without supplementation, this effect was not observed in the lesser kestrel (Falco naumanni), where heavy rains during the rearing of the offspring reduced the availability of insects, compromising the growth and survival of the young [24]. In black kites (Milvus migrans), predation pressure, strong winds and frequent rains can affect the foraging of adults and reduce the food supply to the nests, lowering chick survival. In contrast, chicks that hatch early in the season exhibit greater growth and survival, favored by better weather conditions and greater prey abundance [26,96].

3.3. Social Interactions

Social interactions act as powerful environmental signals in the regulation of the HPG axis and may precede, intensify, or prolong reproductive activity. In many species, courtship behavior stimulates ovarian development and ovulation in females. Pioneering studies with house sparrows and European starlings (Sturnus vulgaris) have already shown that the presence of sexually active males and courtship is associated with greater growth of the oviduct and a greater probability of laying [158,174]. Experiments with Ring dove (Streptopelia risoria) reinforced these findings, demonstrating that castrated males, incapable of performing complete courtships, significantly reduced the reproductive response of females [100].

This response, however, is not based solely on the physical presence of the male. The degree and direction of courtship influence the intensity of hormonal activation in females [100]. In species such as canaries (Serinus canaria) and Gambel’s white-crowned sparrows (Zonotrichia l. gambelii), male song, particularly that of conspecific males, can precede spawning and raise LH levels in females, with the effect being potentiated when combined with visual stimuli such as movements and physical approaches [125,126,127]. Nevertheless, activation of the HPG axis is primarily triggered by photoperiodic cues, while social signals such as male song act synergistically to enhance or fine-tune gonadotropin release and ovarian development [125,126,127,157]. This adaptive refinement ensures that reproductive activation reaches its full expression only when environmental and social conditions jointly indicate favorable circumstances for breeding.

The opposite can also occur: sexually receptive females can modulate the reproductive physiology of males. In starlings (Sturnus vulgaris), Burger reported that the mere presence of females accelerates the resumption of gonadal activity in males [173]. Experiments with Gambel’s white-crowned sparrows have shown that females treated with estradiol prolong the manifestation of sexual behaviors and maintain high LH and testosterone levels in their partners, delaying entry into the photorefractory phase [191,192]. In Ring dove, simple visual and auditory contact with a receptive female can cause a rapid increase in male testosterone, followed by a decrease when the females move to the incubation phase [102,103].

In addition to direct reproductive interactions, social conflicts influence the HPG axis. In Song sparrow (Melospiza melodia) outside the mating season, territorial disputes and aggressive interactions rapidly increase brain levels of androgens, such as 5α-dihydrotestosterone (5α-DHT) and androstenedione (AE), without a concomitant increase in circulating testosterone [140]. These results, in addition to those of previous seasonal studies, indicate that the brain acts as an autonomous endocrine microenvironment, regulating the local production of neurosteroids regardless of gonadal activity [141].

3.4. Artificial Light Pollution at Night (ALAN)

Finally, artificial light at night (ALAN) has been shown to be a human-induced factor capable of profoundly disrupting the physiological rhythms of birds, affecting everything from sleep to reproduction. In great tits, experiments revealed that the constant presence of night light alters natural activity patterns and modifies the expression of genes linked to the biological clock and the stress axis, suggesting that the organism may become desynchronized from environmental cycles even without direct activation of the reproductive axis [33]. In tree sparrows, the reproductive response to ALAN depends on light intensity: exposure to moderate light during the dark phase (night) (≈85 lux) accelerates the activation of the hypothalamus–pituitary–gonadal axis, prematurely increasing the expression of genes such as TSHβ, DIO2, and GnRH-I in the brain, in addition to advancing the hormonal peaks of LH and estradiol. In contrast, higher intensities (150–300 lux) ultimately suppress this endocrine cascade, inhibiting the seasonal function of the reproductive system [32].

In highly urbanized environments, other studies with great tits have shown that the combination of night lighting and high spring temperatures advances both the onset of laying and the elevation of testosterone in males. This reproductive advancement, although initially seemingly advantageous, results in a mismatch between the timing of breeding and the actual availability of food for the young, reducing reproductive success. ALAN also affects the expression of genes that regulate the reproductive axis, such as GnRH-I, and alters circulating LH levels, especially in urban contexts where light intensity is constant and intense [143]. These results are supported by broader evidence that the neuroendocrine system of birds can be confused by artificial light signals, leading to advances, delays, or failures in reproductive timing. Although ALAN acts through the same photoperiodic pathways as natural light, it represents an anthropogenic distortion of photoperiodic information, producing desynchronization between internal biological rhythms and external environmental cues [193]. This highlights the importance of considering both natural and artificial light signals, together with climatic variability, in conservation strategies for seasonally breeding species.

However, the way birds respond to ALAN may also depend on their geographical origin. In the dark-eyed junco (Junco hyemalis), for example, populations living at higher latitudes initiate reproduction only when days become much longer, while those from lower latitudes activate the reproductive axis with shorter days. This difference is linked to internal mechanisms that regulate hormones such as TSH, DIO2 and GnRH, allowing each population to adjust to its natural environment [31]. When exposed to light at night, all birds tend to anticipate reproduction, but those in the north react more intensely. This finding illustrates that artificial light at night does not affect all populations equally. Birds breeding at higher latitudes, which naturally require longer days to initiate reproduction and terminate breeding sooner, show a stronger and more accelerated response when exposed to night lighting, while lower-latitude populations remain comparatively less sensitive [31]. In other words, ALAN can shift the reproductive calendar forward but cannot override intrinsic latitudinal differences in photoperiodic thresholds [22]. This means that species with naturally narrow breeding windows are particularly vulnerable, as artificial light may desynchronize their reproductive preparation from optimal environmental conditions.

Thus, reproductive seasonality in birds should be understood as a multifactorial and plastically modifiable phenomenon resulting from the dynamic interaction between photoperiod and secondary environmental stimuli. In view of the intensification of climate change and the anthropogenic modification of natural habitats, it is urgent to adopt integrative approaches that consider both natural and anthropogenic drivers to understand avian reproductive physiology and to design more effective conservation strategies.

4. Opportunistic Reproduction and Alternative Modes of Seasonality

Although the classical photoperiod model satisfactorily explains reproductive seasonality in most high- and mid-latitude birds, an increasing number of studies have revealed alternative strategies in tropical, subtropical, and urban species whose reproductive responses are less dependent on light and more sensitive to immediate environmental triggers such as rainfall, food abundance, temperature, and social interactions [2,90,128,194].

A striking example of this reproductive flexibility is the Eared Dove (Zenaida auriculata), which reproduces throughout the year in tropical and urban environments. Unlike the classical photoperiodic model, its reproduction seems to respond mainly to food availability, rainfall, and local social stimuli [90]. In addition, this species expresses three seasonally regulated opsins in the diencephalon, OPN4, OPN5 and VA-opsin, which provide a multichannel capacity to detect variations in light spectrum, intensity, and timing, and possibly to integrate correlated environmental information such as daily temperature cycles. This sensory plasticity likely contributes to the functional maintenance of the HPG axis even under constant photoperiods [195]. While further studies are required to confirm its phylogenetic distribution, this combination of endocrine flexibility and neural photoreception seems to reflect an adaptive mechanism of opportunistic breeders such as Eared Dove, rather than a universal avian trait.

A comparable pattern of reproductive flexibility is observed for tropical Columbidae of the genus Columbina. Prolonged gonadal activity was observed in Common ground-dove and Plain-breasted ground-dove (C. passerina and C. minuta), with reproduction associated with the rainy season and seed availability and not with the photoperiod [196]. Even in more arid and unpredictable environments, as observed in Common ground-dove, the species maintained reproduction throughout the year whenever the rains became sufficient to sustain the feeding and rearing of the young [197].

The reproductive seasonality of the Rufous-bellied Thrush (Turdus rufiventris) is equally flexible, especially in urban environments. Although the reproduction of the species is concentrated in spring in natural areas, records from urban centers indicate an advancement of song, territorial defense, and nest construction in late winter, induced by artificial light, food abundance, and reduced predation pressure [172]. This flexibility is supported by seasonal changes in the song control nuclei HVC (proper name) and RA (robust nucleus of the arcopallium), whose activity and volume increase during the reproductive season under the influence of sex hormones [198]. A similar phenomenon occurs in the Pale-breasted Thrush (Turdus leucomelas), which shows prolonged breeding activity and multiple broods under favorable tropical conditions [199], reinforcing the ability of the genus Turdus to modulate its reproductive phenology according to the environment.

Similar neuroendocrine flexibility is also evident in boreal finches. A comparative study analyzed GnRH expression in the hypothalamus of three species, Common redpoll (Carduelis flammea), Pine siskin (Spinus pinus) (Carduelis pinus) and White-winged crossbill (Loxia leucoptera), after prolonged exposure to long days. The first two showed a strong reduction in GnRH-immunoreactive neurons, accompanied by testicular regression and onset of molting, indicating a classic pattern of absolute photorefractory. On the other hand, White-winged crossbill maintained relatively stable GnRH expression and incomplete gonadal regression, suggesting that photorefractoriness in this species develops more slowly or manifests in a milder form, resembling relative photorefractoriness, where sensitivity to photostimulation is only partially lost and reproductive activity may persist under favorable conditions [200].

Even finer differences have been described within the same species. Subspecies of the white-crowned sparrow (Zonotrichia leucophrys) exhibited contrasting endocrine profiles. Resident populations such as Nuttall’s white-crowned sparrows (Zonotrichia leucophrys nuttalli) present a relatively low photoperiod threshold, short refractoriness and tolerance to prolonged exposure to light, allowing wide reproductive windows and multiple broods at mid-latitudes. In contrast, Gambel’s white-crowned sparrows (Zonotrichia leucophrys gambelii), which is migratory and nesting in arctic regions, exhibits extremely rapid acti-vation and regression of the HPG axis, favoring a single litter within a very restricted range [201].

Tropical and subtropical birds further illustrate the plasticity of reproductive timing. In such environments, the HPG axis can be regulated largely independent of photoperiod, with reproduction responding instead to short-term ecological signals such as rainfall, food abundance, or social stimuli [92]. Experimental work in a neotropical antbird (Hylophylax naevioides) showed that both visual and nutritional food cues can accelerate gonadal development and courtship behavior, fine-tuning reproductive readiness to local conditions [161]. Similarly, studies in the Rufous-collared sparrow (Zonotrichia capensis) revealed marked seasonal changes in hypothalamic immunoreactive GnRH-I content despite constant day length, underscoring a high degree of neuroendocrine flexibility under tropical photic regimes [202].

This ability to integrate multiple environmental signals and fine-tune the timing of reproduction represents a highly advantageous evolutionary strategy, especially in unpredictable environments. By not relying exclusively on photoperiodic information, which serves as an external environmental cue used by the internal biological clock to synchronize physiology with seasonal changes, birds gain greater flexibility to take advantage of favorable ecological windows. This capacity enhances reproductive success even under unstable climates or rapidly changing habitats.

5. Conclusions

Seasonal reproduction in birds arises from a dynamic interplay between endogenous mechanisms and environmental cues. Photoperiod remains the most reliable signal, anchoring the hypothalamic–pituitary–gonadal axis to the annual cycle. Yet, the plasticity of this system becomes evident when secondary modulators are considered: temperature, rainfall, food availability, social interactions, and, increasingly, artificial light at night. Each of these factors introduces additional layers of complexity to neuroendocrine regulation, with the potential to either reinforce or disrupt photoperiodic control.

The diversity of reproductive responses observed among species and populations demonstrates that avian seasonality is not a rigid, predetermined program but a flexible and adaptive strategy shaped by evolutionary history and ecological context. In raptors, for instance, although research remains limited, existing evidence suggests that fluctuations in prey availability and climatic conditions can decisively influence breeding outcomes. Such findings emphasize the importance of adopting an integrative view of avian reproduction—one that incorporates both physiological mechanisms and ecological driver.

In the context of global environmental change, marked by climate warming, urban expansion, and light pollution, there is an urgent need to advance research that bridges fundamental and applied perspectives. Future studies should move beyond traditional temperate-zone models to encompass tropical, subtropical, and polar regions, where photoperiod interacts with distinct environmental pressures. Expanding the taxonomic scope is equally important: many species of high conservation concern, including raptors, seabirds, and long-distance migrants, remain underrepresented in reproductive research despite their vulnerability to environmental perturbations.

Specific priorities for future work include: (1) comparative analyses across latitudinal gradients to clarify how photoperiodic sensitivity and endocrine plasticity evolve under different ecological regimes; (2) long-term field studies integrating behavioral, hormonal, and genomic data to link environmental variability with reproductive performance; and (3) targeted research on threatened or data-deficient taxa to identify both the flexibility and the physiological limits of seasonal adjustment. While most current insights derive from passerine models, expanding this framework to include more non-passerine groups will be essential for capturing a larger range of reproductive strategies across avian lineages. Together, these research directions will clarify how environmental and evolutionary forces interact to shape reproductive strategies, guiding both theoretical advances and conservation efforts aimed at sustaining avian diversity in a changing world.