Disease-driven variation in body reserves links social rank, flock size, and overwinter survival in European greenfinches

Introduction

Winter represents one of the most critical periods in the annual cycle of small passerine birds, during which survival depends on a delicate balance between energy acquisition, predation risk, and pathogen exposure (Lima, 1998; Brodin, 2007). For resident granivorous species in temperate regions, low temperatures, short day length, and fluctuating food availability impose strong energetic constraints, while predators remain a constant threat (Parsons, 2005; White, 2008). Under these conditions, birds face trade-offs between maintaining sufficient energy reserves to avoid starvation and remaining lean enough to escape predators efficiently (Witter and Cuthill, 1993; Gosler et al., 1995).

Body mass and fat reserves are therefore key determinants of winter survival, but their optimal levels are context dependent. Numerous studies have shown that birds adjust their body reserves in response to perceived predation risk, often maintaining lower mass when predation pressure is high (Lima, 1986; Rogers, 1987; Krams, 2000). Conversely, increased energetic reserves can buffer individuals against periods of food scarcity, harsh weather, or physiological stress (Brodin, 2007). Importantly, energetic reserves may be stored not only as fat, but also as metabolically accessible lean tissue (Daan et al., 1990; Swanson et al., 2022), suggesting that both adiposity and overall body mass can contribute to survival under extreme conditions. These trade-offs become especially complex in social species, where access to food, exposure to predators, and information about environmental conditions are shaped by group living (Blem, 1990).

Many passerines, including greenfinches (Chloris chloris), spend the winter in flocks of varying size and stability. Flocking can reduce individual predation risk through dilution and increased vigilance, but it also intensifies competition for food and may facilitate the transmission of infectious diseases (Alexander, 1974; Cresswell, 2008). Within flocks, individuals differ in social dominance, which strongly affects access to food resources, feeding efficiency, and energetic state (Ekman and Askenmo, 1984; Krams et al., 2001). Dominant birds often monopolize profitable feeding sites, whereas subordinates experience frequent displacement and must compensate through alternative foraging strategies or higher fat reserves (Smith et al., 2001; Francis et al., 2018).

Flock size further modifies these dynamics. In small flocks, social hierarchies are often stable and easily enforced, allowing dominant individuals to secure priority access to food with relatively low competitive costs (Krams et al., 2001). In contrast, large flocks may reduce the effectiveness of dominance-based monopolization, increase encounter rates among individuals, and elevate the risk of pathogen transmission (Altizer et al., 2003; Cressler et al., 2016). As a consequence, the relationship between dominance, body condition, and fitness (quantified as adult survival) may shift across flock sizes, favoring different energetic strategies in small versus large social groups.

In recent years, infectious diseases have emerged as an increasingly important selective force shaping winter ecology in birds (Hosseini et al., 2004; Fuller et al., 2012). Trichomonosis, caused by the protozoan Trichomonas gallinae, has led to recurrent epidemics in finches across Europe, often resulting in high mortality (Robinson et al., 2010; Lawson et al., 2012). Infection typically impairs feeding and induces anorexia, dehydration, and rapid loss of body condition. Under such circumstances, individuals with greater energetic reserves may be better able to withstand prolonged periods of reduced food intake, either by mobilizing fat stores or by catabolizing lean tissue when fat reserves become depleted (Brodin, 2007). This suggests that energetic strategies that are costly under typical ecological conditions, in which predation risk generally outweighs infection risk in shaping survival strategies, may not be optimal under conditions of disease outbreak.

Despite growing interest in disease ecology, relatively little is known about how social structure and flock size interact with infection risk to shape individual energetic strategies and survival (Silk and Fefferman, 2021). Specifically, it remains unclear whether dominant and subordinate individuals adopt different body reserve strategies across flock sizes, and whether these strategies translate into differential survival during epidemic versus non-epidemic winters. Moreover, few studies have explicitly disentangled the relative contributions of adiposity and body mass corrected for structural body size (wing length), hereafter referred to as size-independent body mass (body condition) to survival under disease pressure. Understanding these interactions is essential for linking social behavior, physiological condition, and population-level consequences of emerging diseases.

In this study, we investigated how dominance rank, flock size, and trichomonosis epidemic context jointly influenced body condition and overwinter survival in free-living greenfinches. Using multi-year data collected during winters with and without trichomonosis outbreaks, we examined (1) how body mass and body mass index (BMI) varied with social rank across flocks of different sizes, (2) whether these relationships differed during epidemic versus non-epidemic winters, and (3) how body condition, dominance, and flock size predicted survival until spring. We further tested whether body mass contributed to survival independently of BMI, as expected if lean tissue provides an additional energetic buffer during infection-associated sickness behaviors, including reduced food intake. We hypothesized that dominant individuals would maintain lower body reserves in small flocks under non-epidemic conditions, reflecting selection for agility and predator avoidance, but higher reserves in large flocks during epidemic winters, where energetic buffering against infection becomes critical. By integrating social structure, energetic state, and survival, this study aimed to clarify how wintering birds adjust their strategies in response to shifting ecological and epidemiological pressures. Overwinter survival was assessed as apparent survival based on repeated resightings at feeding sites. While permanent emigration cannot be entirely excluded, greenfinches exhibit strong winter site fidelity, and sustained absence after repeated surveys is widely interpreted as mortality in feeder-based studies. We therefore treat disappearance as a proxy for death, while acknowledging this assumption explicitly.

Methods

Study species and winter flocks

Greenfinches form stable winter flocks that vary widely in size, from small groups in rural landscapes to large aggregations at concentrated feeding sites (e.g., farms, barns, and bird-feeding stations), where they primarily consume weed seeds, spilled grain, and livestock feed (including poultry and cattle food). In the study area, flock sizes at feeding sites typically range from 6 to 360 individuals (mean ± SD = 64.24 ± 82.71 individuals, N = 52 flocks), reflecting typical winter aggregation sizes in our focal population. Because flock size in greenfinches varies widely across regions, habitats, and resource conditions, we report locally observed values rather than relying on species-wide estimates from the literature. In our study region, greenfinches are largely year-round residents, although local movements occur. Their diet shifts seasonally, with insects forming an important component during the breeding season, while winter foraging is predominantly granivorous, centered on weed seeds, grain, and anthropogenic food sources at farms and feeding sites. This seasonal transition promotes flock formation and strong competition over concentrated resources during winter. During winter (late November–early March), individuals compete intensely for access to food, and dominance hierarchies strongly influence feeding opportunities, body condition, and survival. Dominance hierarchies strongly influence access to food resources, with higher-ranking individuals typically obtaining preferential feeding opportunities (Hake, 1996). Winter flocks are also epidemiologically relevant, as high host densities facilitate outbreaks of trichomonosis, which can impose substantial mortality and energetic costs (Robinson et al., 2010).

Study area and data collection

Data were collected during winters 2019–2021 in the countryside of Krāslava, southeastern Latvia (GPS coordinates of the central part of the study area: 55.8974° N, 27.1706° E). Birds were captured at feeding sites using mist nets and individually marked with unique color ring (2.3 mm) combinations. For each captured individual, we recorded bird identity, flock identity, sex, body mass, wing length, and winter of capture (December of the respective year). Body mass was measured to the nearest 0.1 g using a digital scale, and wing length was measured to the nearest 1 mm using a stopped wing ruler.

Birds were captured using standard small-passerine mist nets (mesh 16 mm; height 2.5 m), including nets recently obtained from Ecotone (Poland). Because captures were conducted in winter conditions, nets were normally kept closed and opened only briefly (typically 3–5 min per session) under continuous supervision to minimize cold exposure and handling stress. Birds were removed immediately upon capture (usually within seconds), weighed within 1–3 min, and released. Capture sessions typically ended after 5–7 birds were caught, at which point the nets were closed. Most individuals returned to feeding sites within minutes. This rapid-capture protocol was adopted to reduce disturbance and ensure animal welfare. All capture, handling, and marking procedures complied with Latvian wildlife regulations and were conducted under appropriate ringing and research permits (permit #87 issued by the Ethical Committee of the Food and Veterinary Service of the Republic of Latvia).

Body condition measurements

Body mass was converted from grams to kilograms, and wing length from millimeters to meters. Body mass index (BMI) was calculated as body mass divided by wing length cubed (kg·m^-³), following established practice for passerines and previous work on greenfinches (Krams et al., 2020). BMI was used as a size-corrected proxy of body reserves, whereas body mass was analyzed both with and without controlling for structural size.

Flock size and social environment

Winter flock size for each individual was recorded as the number of conspecifics regularly observed at the feeding site. Flock size was estimated during repeated in-person observation periods at each feeding site. Multiple experienced observers independently counted birds and then agreed on a consensus value, using the maximum reliably observed number of individuals simultaneously present to avoid underestimation caused by transient movements. This value was used as the site-specific flock size metric in subsequent analyses.

Based on natural discontinuities in flock sizes and ecological considerations, flocks were grouped into four size categories: 10, 20–38, 55–88, and 125–330 individuals. These categories represent distinct social environments, ranging from small flocks in which all individuals could be captured and ranked to very large flocks in which only a subset of individuals could be marked.

Dominance rank assessment

Aggressive interactions were operationally defined as displacement events at feeding sites, where one bird supplanted another from access to food. Although minor agonistic behaviors (e.g., wing flicks or brief physical contact) were occasionally observed, only displacement interactions were used to quantify dominance relationships, as they provide a robust and repeatable measure of hierarchy rank in flocking passerines.

Aggressive interactions and flock composition were recorded through direct in-person observations by multiple trained observers rather than video recording. This approach was chosen because greenfinches are large and conspicuous, dominant individuals reliably occupy central feeding positions, and winter lighting conditions limited video quality. Observers jointly quantified flock size and aggressive displacement events, repeating counts several times and retaining the maximum reliably observed number. Behavioral observations were frequently dictated to a digital audio recorder for later verification.

Each flock was typically monitored for several hours per day across repeated visits, with observers focusing primarily on displacement interactions at feeding sites. Counts and behavioral classifications were agreed upon collectively to minimize observer bias.

In small flocks (size = 10), all individuals were captured and dominance hierarchies were determined directly from repeated aggressive interactions at feeders. In larger flocks, where complete sampling was not feasible, dominance rank of each marked individual was expressed as relative dominance rank on a percentage scale. Individuals occupying the top positions in observed interactions were assigned ranks of 90–100%, whereas the most subordinate individuals were assigned ranks of 0–10%. Intermediate ranks were scaled accordingly. For statistical analyses, dominance rank was treated as a continuous predictor and standardized so that coefficients represent effects per 10% change in rank. Thus, the most dominant individual was identified as the bird that consistently displaced conspecifics during feeding and maintained priority access to food; in large flocks, only this top-ranking individual was extracted because full hierarchy reconstruction was not always feasible.

Epidemic context

Trichomonosis outbreaks were documented in winter 2021, whereas winters 2019 and 2020 showed no evidence of epidemic infection and were therefore classified as non-epidemic. Winter 2021 was classified as an epidemic period based on the sudden appearance of multiple dead birds at feeding sites, followed by increasing mortality over subsequent days and weeks, together with repeated detection of motile T. gallinae trophozoites in oral–crop swabs and widespread clinical signs (e.g., dysphagia, lethargy). Because comprehensive prevalence screening is not feasible in free-ranging birds, epidemic status was determined by this characteristic pattern of escalating mortality combined with confirmed parasite presence rather than by a fixed infection threshold. In contrast, winters 2019 and 2020 showed no clinical cases and no evidence of population-level outbreaks.

Epidemic status was included as a categorical fixed effect in all models to test whether dominance-dependent body reserve strategies differed under disease pressure. Greenfinches were screened for infection using oral-cavity and crop swabs, which were examined immediately after collection for motile trophozoites. Swabs from the oropharyngeal region and esophagus were prepared as wet mounts in sterile saline and observed under a light microscope. T. gallinae was identified based on its characteristic rapid, non-directional motility and flagellated morphology, with confirmation at higher magnification by visualization of the undulating membrane (Krama et al., 2025).

Survival assessment

Overwinter survival was assessed by repeated resightings of color-ringed individuals at feeding sites from January through late February or early March. Survival status was coded as a binary variable (survived until spring: yes/no). The final dataset included N = 894 individually marked greenfinches with complete data on dominance rank, body condition, flock size, epidemic status, and overwinter survival.

Statistical analyses

All analyses were conducted using linear mixed‐effects models to account for repeated sampling of individuals within winter flocks. Analyses were restricted to individuals for which a relative dominance rank could be estimated. Birds without dominance rank estimates were excluded from statistical analyses, as rank was a focal predictor and central to the study hypotheses. Dominance rank was expressed as a continuous variable (relative dominance rank, %), ranging from low-ranking subordinate individuals (0–10%) to top dominants (90–100%). Treating dominance as a continuous predictor allowed us to test rank-dependent patterns across the full social gradient rather than imposing arbitrary rank categories. Flock size varied widely and was therefore grouped a priori into four biologically meaningful categories based on observed natural clustering and sampling constraints: 10, 20–38, 55–88, and 125–330 individuals. This categorical treatment reflects qualitative differences in social environment and competitive structure across flock sizes.

Two response variables were analyzed separately: Body mass (kg), and Body condition (BMI; kg·m^-³). For each response, we fitted a linear mixed-effects model with relative dominance rank, flock size category, and trichomonosis epidemic status (absent: 2019–2020; present: 2021) as fixed effects, including all two-way and the three-way interaction. These interaction terms were specified a priori to test whether dominance-related mass and condition strategies differ across flock sizes and epidemic contexts. Flock identity was included as a random intercept to account for non-independence of individuals within flocks. Model assumptions were evaluated by inspecting residual distributions and fitted–residual plots. Dominance rank was mean-centered to improve interpretability of interaction terms. Sex was included as a fixed effect in all BMI models.

Statistical significance was assessed at α = 0.05. Effect sizes and uncertainty are reported as model coefficients with standard errors and 95% confidence intervals. Estimated marginal means and predicted slopes were used for visualization.

To evaluate whether overwinter survival during epidemic conditions depended exclusively on relative adiposity (BMI) or also on somatic reserves independent of structural size (putatively including lean tissue), we fitted an additional set of models that jointly considered BMI and body mass. Because BMI is mathematically derived from body mass and wing length, including raw body mass and BMI in the same model would induce substantial collinearity; therefore, we quantified size-adjusted mass using a residual approach. Specifically, we first modelled log-transformed body mass as a function of log-transformed wing length (log(mass) ~ log(wing length)) and extracted individual residuals as an index of size-independent mass (hereafter “residual mass”). Positive residual mass indicates heavier-than-expected individuals for a given wing length, consistent with greater total somatic reserves.

We then analyzed survival (survived until spring: yes/no) using a binomial generalized linear mixed model with a logit link, including BMI, body mass, trichomonosis epidemic status (yes/no), social rank (continuous relative dominance rank, %), flock-size category (10, 20–38, 55–88, 125–330), and sex (m/f) as fixed effects. To maintain comparability with the main survival model and to test the key ecological predictions, the fixed-effects structure included the following interactions a priori: (i) BMI × epidemic and residual mass × epidemic, (ii) rank × flock-size category, and (iii) rank × flock-size category × epidemic. All continuous predictors (BMI, body mass, and rank) were standardized (z-scored) prior to modelling to facilitate interpretation of coefficients and to improve numerical stability. We included random intercepts for flock identity to account for non-independence of individuals wintering together; models including both flock- and individual-level random intercepts were preferred, but when convergence issues arose, models with flock-level random intercepts only were retained. Model fit was evaluated using likelihood-ratio tests for nested models and information criteria (AIC), and fixed effects were assessed using Wald z-tests. For visualization and inference, we derived estimated marginal means and predicted survival probabilities across the observed range of rank and reserve metrics, separately for epidemic and non-epidemic winters, within each flock-size category.

Results

Body mass as a function of dominance, flock size, and epidemic context

Total body mass showed weaker and inconsistent relationships with dominance rank and epidemic context (Table 1). Although body mass varied with flock size and was lower during the epidemic winter (epidemic main effect: χ²(1) = 19.95, p < 0.001; Table 1)), rank-related differences in body mass were less strongly modified by epidemic status than were differences in BMI. A significant rank × flock-size interaction (χ²(3) = 33.83, p < 0.001) indicated that dominant individuals in medium-sized and large flocks tended to be heavier than subordinates, whereas the absence of a significant three-way interaction with epidemic status (χ²(3) = 4.18, p = 0.243) suggests that total body mass was comparatively insensitive to disease-driven environmental change (Table 1). This pattern is consistent with body mass integrating both fat and lean tissue and therefore reflecting a more stable energetic state than BMI, which is more responsive to short-term fattening and depletion.

Table 1. Effects of dominance rank, flock size, sex, and epidemic context on body mass.

Joint tests (body mass):.

rank × flock_category: χ²(3) = 33.83, p = <0.0001.

epidemic main: χ²(1) = 19.95, p = <0.0001.

rank × flock_category × epidemic: χ²(3) = 4.18, p = 0.243.

Results from a Gaussian linear mixed-effects model testing how body mass varies with relative dominance rank, flock-size category, and trichomonosis epidemic status in wintering greenfinches. Fixed effects included relative dominance rank (expressed per 10% increase and mean-centered), flock-size category (reference level: 10 individuals), epidemic status (reference level: no epidemic), sex (reference level: male), and all two-way and three-way interactions among rank, flock size, and epidemic status. Flock identity was included as a random intercept to account for non-independence of individuals wintering together. Estimates are shown with standard errors, test statistics, and p-values. Joint χ² tests summarize the overall significance of interaction terms.

Body condition (BMI) as a function of dominance, flock size, and epidemic context

Body condition (BMI) was shaped by a context-dependent interaction between dominance rank and flock size, rather than by a uniform effect of rank across all social environments. In the linear mixed-effects model, the main effect of dominance rank on BMI was not statistically significant (Table 2), indicating that rank alone did not predict body reserves when averaged across flock sizes (Figure 1).

Table 2. Effects of dominance rank, flock size, and epidemic context on body condition (BMI).

Joint tests (BMI):.

rank × flock_category: χ²(3) = 16.16, p = 0.00105.

epidemic main: χ²(1) = 9.24, p = 0.00243.

rank × flock_category × epidemic: χ²(3) = 9.84, p = 0.02.

Results from a Gaussian linear mixed-effects model testing how body condition, expressed as body mass index (BMI; kg m^-³), varies with relative dominance rank, flock-size category, and trichomonosis epidemic status in wintering greenfinches. Fixed effects included relative dominance rank (per 10% increase and mean-centered), flock-size category (reference level: 10 individuals), epidemic status (reference level: no epidemic), sex (reference level: male), and all two-way and three-way interactions among rank, flock size, and epidemic status. Flock identity was included as a random intercept to account for shared social environment. Estimates are shown with standard errors, test statistics, and p-values. Joint χ² tests evaluate the overall significance of interaction terms and indicate that rank-related variation in BMI is contingent on flock size and epidemic context rather than reflecting a uniform main effect of dominance.

Instead, the relationship between dominance rank and BMI differed among flock-size categories, as evidenced by a significant rank × flock-size interaction (χ²(3) = 16.16, p = 0.0011; Table 2). In medium-sized (55–88 individuals) and very large flocks (125–330 individuals), higher-ranking individuals maintained significantly higher BMI than subordinates, whereas no such rank-related differences were detected in small flocks (10 or 20–38 individuals).

Trichomonosis epidemic status had an overall negative effect on BMI (epidemic main effect: p = 0.0024), indicating reduced body reserves during the epidemic winter. Epidemic context further modified rank-dependent patterns in a flock-size–specific manner, as shown by a significant three-way interaction between dominance rank, flock size, and epidemic status (χ²(3) = 9.84, p = 0.020; Figure 1, Table 2). Figure 1 illustrates predicted BMI across dominance ranks and flock sizes separately for epidemic and non-epidemic contexts, highlighting how disease conditions reshape social gradients in body condition.

This three-way interaction was driven primarily by medium-sized flocks (55–88 individuals), where the positive association between dominance rank and BMI observed in non-epidemic winters was significantly reduced during the epidemic winter (Table 2). In the largest flock category (125–330 individuals), a similar attenuation was suggested but did not reach conventional levels of statistical significance. In contrast, rank–BMI relationships in small flocks remained weak and statistically indistinguishable from zero regardless of epidemic status.

Sex did not have a significant main effect on BMI and did not interact with dominance rank, flock size, or epidemic context (all p ≥ 0.1; Table 2).

Overwinter survival

Overwinter survival (survived until spring: yes/no) was strongly influenced by epidemic context and individual body condition, with additional contributions from dominance rank and flock size. The mixed-effects logistic regression model explained a substantial proportion of variation in survival (likelihood-ratio test comparing full and null models: χ² = 482.2, df = 27, p < 0.001; marginal R² = 0.40).

Apparent survival was markedly lower during the trichomonosis epidemic winter, indicating a strong negative effect of epidemic conditions on overwinter persistence. Because epidemic status entered the model in interaction with body condition and social variables, the main-effect coefficient for epidemic status reflects survival at reference and mean-centered values of covariates and is therefore not directly biologically interpretable on its own. Consequently, inference focuses on interaction terms and predicted survival probabilities.

Body condition (BMI) played a central role in modulating survival, and its effect depended strongly on epidemic context. During the epidemic winter, higher BMI was associated with a substantially increased probability of survival, as indicated by a strong positive BMI × epidemic interaction (β = 1.56 ± 0.19, z = 8.22, p < 0.001). Individuals with low BMI exhibited lower survival probabilities during the epidemic, whereas individuals with higher BMI retained a markedly greater likelihood of surviving until spring.

In contrast, during non-epidemic winters, BMI showed a weak but statistically significant negative association with survival (β = −0.14 ± 0.07, z = −2.07, p = 0.039). This pattern suggests potential costs of maintaining elevated body reserves under benign conditions, consistent with mass-dependent trade-offs such as reduced escape performance or increased predation risk.

Dominance rank independently predicted overwinter survival across contexts, with higher-ranking individuals showing higher survival probabilities on average (β = 0.023 ± 0.003, z = 6.90, p < 0.001). However, the survival advantage of dominance was reduced during the epidemic once individual body condition was accounted for, indicating that energetic reserves, rather than social rank per se, were the primary determinant of survival under disease pressure.

Flock size category also influenced survival, with several medium and large flock categories exhibiting lower baseline survival probabilities relative to small flocks (multiple contrasts, all p < 0.01). These effects were modest compared with the strong influence of epidemic status and body condition but indicate that social environment contributes to variation in overwinter survival. Random intercepts for flock identity (and individual identity where model convergence permitted) were retained to account for non-independence of individuals within winter flocks and repeated measures across years.

To evaluate whether somatic reserves independent of relative adiposity contributed to survival, we fitted an extended model including body mass (residual mass) in addition to BMI. This model provided a significantly improved fit relative to the BMI-only model (likelihood-ratio test: χ² = 21.07, df = 2, p > 0.001; ΔAIC = −17.1). Body mass had a positive main effect on survival (β = 8.37 ± 2.35, z = 3.56, p < 0.001), indicating that individuals heavier than expected had higher survival probabilities. However, the interaction between body mass and epidemic status was not statistically significant (β = −7.14 ± 4.89, z = −1.46, p = 0.144), suggesting that body mass did not confer an additional epidemic-specific survival advantage beyond that associated with BMI.

Predicted survival probabilities derived from the fitted models illustrate a pronounced context-dependent shift in the fitness consequences of body condition. This pattern is supported by a significant three-way interaction between BMI, dominance rank, and epidemic status (χ²(3) = 9.84, p = 0.020; Table 2), indicating that the relationship between body condition and survival differed across social and disease contexts. During non-epidemic winters, survival was highest at relatively low BMI, particularly for dominant individuals in small flocks. In contrast, during the epidemic winter, survival increased steeply with BMI across flock sizes, with the strongest gains observed among higher-ranking individuals in larger flocks. Across all contexts, subordinate individuals exhibited lower survival probabilities and weaker condition-dependent benefits, consistent with the significant rank × flock-size interaction (χ²(3) = 16.16, p = 0.00105; Table 2).

Discussion

Our study demonstrates that overwinter energetic strategies and survival in greenfinches are shaped by context-dependent interactions between social dominance, flock size, and epidemic context, rather than by uniform effects of rank or body condition across all social settings. By integrating body condition, social structure, and survival outcomes, we show that dominance-related variation in energetic reserves emerges only under specific social conditions and is further modified during disease outbreaks. In particular, body mass index (BMI) was a strong predictor of overwinter survival during a trichomonosis epidemic, whereas its relationship with survival was weak and slightly negative during non-epidemic winters. These results indicate that the adaptive value of body reserves is highly conditional on ecological and epidemiological context.

Dominance, flock size, and energetic strategies

In winters without trichomonosis outbreaks, we did not detect a general association between dominance rank and BMI across all flock sizes. Instead, rank-related differences in body condition were restricted to medium-sized and very large flocks, where higher-ranking individuals maintained higher BMI than subordinates. In small flocks, dominance rank was not associated with BMI, suggesting that social rank alone does not universally predict energetic strategy.

These findings are consistent with theoretical expectations that the benefits of dominance depend on social environment (Tibbetts et al., 2022; Leighton et al., 2023). In small flocks, dominance hierarchies are stable and food access is predictable, allowing dominant individuals to meet energetic demands without accumulating large reserves (Lendvai et al., 2006). Under such conditions, selection for agility and predator avoidance may favor relatively lean phenotypes even among high-ranking individuals. In contrast, in larger flocks—where competition is more intense, feeding opportunities are less predictable, and dominance hierarchies may be harder to enforce—dominant individuals may need to accrue greater energetic reserves, resulting in the positive rank–BMI associations observed in these flock categories. Importantly, these patterns should not be interpreted as fixed dominance strategies, but rather as flexible outcomes arising from interactions between social structure and energetic constraints.

Disease context alters the fitness consequences of body reserves

The most striking result of this study is the strong context dependence of the relationship between body condition and survival. During the trichomonosis epidemic winter, higher BMI was associated with substantially increased survival probability, whereas during non-epidemic winters BMI showed a weak negative association with survival. This contrast suggests a reversal in the fitness consequences of elevated energetic reserves under disease pressure.

Trichomonosis impairs feeding and induces anorexia, dehydration, and rapid loss of body condition. Under these circumstances, individuals entering winter with greater energetic reserves are likely better able to tolerate prolonged periods of reduced intake, either through mobilization of fat or catabolism of somatic tissues once fat reserves are depleted (Lawson et al., 2012; Cressler et al., 2016). Our results are consistent with this interpretation, as survival during the epidemic increased steeply with BMI across flock sizes. By contrast, outside epidemic conditions, elevated body reserves may carry costs, potentially through reduced maneuverability or increased predation risk, as predicted by mass-dependent predation models. The weak negative association between BMI and survival during non-epidemic winters supports this interpretation, although the effect size was small. Notably, corresponding patterns in total body mass were comparatively weak and less responsive to epidemic context, consistent with body mass integrating both fat and lean tissue and therefore reflecting a more stable energetic state than BMI.

Dominance does not uniformly translate into survival advantages

Although dominance rank was positively associated with overwinter survival on average, this effect was substantially reduced once body condition was taken into account during the epidemic winter. Dominance per se did not guarantee survival under disease pressure, indicating that social advantages are insufficient when physiological tolerance becomes the primary constraint. This finding contrasts with studies conducted under benign winter conditions, where dominant individuals often show higher survival due to superior access to food resources (Lahti, 1998; Francis et al., 2018). Our results suggest that disease can weaken or partially override the survival benefits typically associated with high social rank, shifting the selective landscape toward traits related to energetic buffering rather than competitive ability. In this sense, infectious disease may act as a conditional equalizer within social groups, reducing the fitness disparity between dominant and subordinate individuals when survival depends primarily on physiological resilience.

Social dominance has also been linked to variation in immune function across taxa, with dominant individuals often exhibiting altered inflammatory profiles, pathogen resistance, or immune investment compared with subordinates (Habig and Archie, 2015; Smyth et al., 2018). Such dominance-associated immune differences may interact with body condition to influence survival under epidemic stress. Although we did not directly measure immune parameters, these findings suggest that social rank may shape disease outcomes through both energetic and immunological pathways. Future studies combining physiological, immunological, and behavioral data will be necessary to disentangle these mechanisms.

Flock size as a mediator of trade-offs

Our results further indicate that flock size mediates the balance between competition, predation risk, and pathogen exposure, shaping both energetic strategies and survival outcomes. Rank-related differences in BMI emerged primarily in larger flocks, and the survival benefits of elevated BMI during the epidemic were most pronounced in these social environments (Näther et al., 2009).

Large flocks are likely characterized by increased contact rates, elevated pathogen transmission risk, and greater uncertainty in food access. Under such conditions, maintaining higher energetic reserves may be particularly advantageous during disease outbreaks, even for dominant individuals that might otherwise favor leaner phenotypes (Gustafsson et al., 1994). Conversely, in small flocks, where dominance hierarchies are stable and predation risk may be more salient, lean strategies appear sufficient outside epidemic contexts. These findings emphasize that flock size is not merely a background variable but a key ecological factor that conditions the fitness consequences of dominance and body condition.

Contributions of size-independent mass

By jointly considering BMI and size-adjusted body mass, we found that individuals heavier than expected for their structural size exhibited higher overwinter survival, independent of relative adiposity (Speakman, 2018). This result suggests that total somatic reserves, potentially including lean tissue, contribute to survival during winter. However, we found no evidence that size-independent mass conferred an additional survival advantage specifically during epidemic conditions beyond that provided by BMI. This indicates that while somatic reserves are generally beneficial, relative adiposity appears to be the dominant energetic buffer under disease-induced anorexia (Speakman, 2018). These findings underscore the importance of distinguishing between different components of body condition when assessing survival mechanisms.

From a physiological perspective, these results are consistent with a sequential use of endogenous energy reserves during periods of food deprivation or illness (Brodin, 2007; Houston et al., 2007). Relative adiposity, captured by BMI, likely represents a first-line energetic buffer that supports short-term tolerance to reduced intake and disease-induced anorexia. Conversely, size-independent body mass may reflect additional somatic reserves, including metabolically accessible muscle protein, that can be mobilized once fat stores become depleted. The strong epidemic-specific effect of BMI on survival suggests that, under trichomonosis outbreaks, survival hinges primarily on avoiding early energetic collapse during acute phases of anorexia rather than on sustaining prolonged fasting (Blem, 1990; Daan et al., 1990). In contrast, the positive main effect of size-adjusted body mass across winters indicates that greater overall somatic reserves contribute to survival more generally, potentially by extending endurance once fat reserves are exhausted. Because our data do not allow us to track the temporal sequence of fat versus lean tissue depletion, the contribution of muscle catabolism to late-stage survival remains inferential; nevertheless, the divergent effects of BMI and residual mass are consistent with distinct, temporally structured roles of fat and lean tissue in overwinter energy management.

Predator role in disease dynamics

Predation pressure may also interact with disease dynamics to shape overwinter survival. Raptors such as Eurasian sparrowhawks (Accipiter nisus) can acquire T. gallinae through infected prey, and infections have been documented in nestling sparrowhawks during songbird trichomonosis outbreaks (Kunca et al., 2015). Although infection does not necessarily imply clinical disease or reduced hunting efficiency, these findings raise the possibility that predator condition or activity may change during epidemic periods. If predator pressure were reduced, this could inflate the apparent survival benefits of elevated body condition. Conversely, weakened prey individuals may also become more vulnerable to predation. Because predator abundance and hunting activity were not quantified in our system, we cannot evaluate these possibilities directly. We therefore interpret our results primarily in terms of disease-mediated energetic constraints while acknowledging that predator–pathogen interactions may represent an additional ecological layer influencing survival during epidemics.

Implications and limitations

This study provides evidence that wintering birds flexibly adjust energetic strategies in response to interacting social and epidemiological conditions, with direct consequences for survival. By explicitly modeling interactions between dominance rank, flock size, and disease context, we demonstrate that the fitness value of body reserves cannot be inferred from main effects alone.

Several limitations should be acknowledged. Because survival was inferred from resightings, our estimates reflect apparent rather than true survival. Although undetected dispersal is theoretically possible, strong winter site fidelity in greenfinches makes emigration unlikely, and disappearance after repeated surveys is widely accepted as a proxy for mortality in this system. We also did not directly measure infection status or pathogen load at the individual level; consequently, disease effects are inferred indirectly from the epidemic context rather than confirmed infection. Additionally, BMI is an imperfect proxy for energetic reserves and does not capture variation in immune function or muscle composition. Future studies combining physiological measurements with pathogen diagnostics would help clarify the mechanisms underlying disease tolerance.

Broader implications and conclusions

Our findings show that the adaptive value of body reserves in greenfinches is highly context dependent, shaped jointly by social structure, group size, and trichomonosis epidemic. Dominance-related differences in energetic strategies emerge only in particular social settings and are reshaped during disease outbreaks, while elevated body reserves confer strong survival benefits only under epidemic conditions. These results highlight the need to integrate disease ecology into traditional frameworks of winter survival and social behavior. As emerging pathogens become increasingly prevalent in wildlife populations, understanding how individuals flexibly balance energetic trade-offs in social environments will be critical for predicting survival and population dynamics.

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Footnotes

Edited by: W. Douglas Robinson, Oregon State University, United States

Reviewed by: Geoffrey E. Hill, Auburn University, United States

Francis Tillman, Memphis Zoo, United States