Discussion
We predicted that phenotype-by-environment interactions between color morph and snow would drive differences in survival within and among winter seasons. We further predicted that phenotypic mismatches would vary across winter with gray morphs exhibiting higher survival during period of persistent snow cover and red morphs having higher survival during times with little or no snow cover. We found that phenotypic mismatch with snow explained differences in survival between ruffed grouse color morphs throughout the winter season, but the magnitude of the mismatch effect was variable across years. Specifically, phenotypic mismatch had the highest impact during the winter with lower overall survival. During this winter, weekly survival flip-flopped across morphs with red morphs having higher weekly survival during snow-off periods (the beginning and end of the winter season) and gray morphs having higher weekly survival during snow-on periods (the core of the winter season).
For many species, cryptic coloration is a critical adaption for evading predation and depends on both the visual ability of the predator and the prey matching a background environment characterized by a suite of factors such as light conditions, ground substrate, and land cover (Cott 1940, Endler 1990, 1992, Stevens and Merilaita 2009). In high-latitude ecosystems, seasonal snow cover transforms the physical environment and can have strong implications for the survival of cryptically colored species through increased predation risk during times of phenotypic mismatch. We found evidence in some years of our study that phenotypic mismatch with snow cover reduced survival throughout the winter season for ruffed grouse, potentially through the same mechanisms found in other species of reduced background matching leading to higher predation for phenotypically mismatched individuals (Zimova et al. 2018, Wilson et al. 2019, Koskenpato et al. 2020). Although grouse are subject to high predation rates from a diverse suite of avian and mammalian predators, grouse populations across the Upper Midwest appear to be most vulnerable to raptors in winter (Small et al. 1991, Shipley et al. 2020), which have higher visual sensitivity compared to mammalian predators such as coyotes and humans (Endler 1993, Stevens and Merilaita 2009). We observed this in our study where the majority (76%) of mortality events were attributed to predation and more than half (69%) of those predation events were attributed to raptors. Previous research into the dynamics of northern forest prey communities suggests increased abundances of one species may alleviate predation pressure on other prey species, as was seen for North American porcupines Erethizon dorsatum through an experimental revival of a snowshoe hare Lepus americanus population (Wilson et al. 2022). Interestingly, the predominantly avian predator guild for ruffed grouse may decouple grouse from this system, despite grouse and hare mortality both being dictated by mismatch-mediated predation pressure. Regardless of color morph, the mottled and disruptive coloration patterns of ruffed grouse plumage, which may provide increased camouflage in forest habitats with variable light conditions, indicates that selection for camouflage is an important driver of ruffed grouse coloration (Endler 1993, Rusch et al. 2020). Our results suggest that the persistence of red and gray color morphs reflects a further adaption of increased crypsis to match with seasonal snow cover. Consequently, the presence of multiple morphs within a species could be an adaptation strategy of “bet hedging” that favors the survival of one morph over another during certain environmental conditions (Xue et al. 2019).
In addition to cryptic coloration, thermoregulatory properties associated with coloration have been proposed as an alternative or complementary function for polymorphic and seasonally color changing species in winter environments. For example, winter white pelages in seasonally color changing mammals are more insulative than brown summer coats and further, the winter coats of more northerly snowshoe hare are longer and denser than those of hares in lower latitudes (Gigliotti et al. 2017, Zimova et al. 2018, Kennah et al. 2023). Similarly for a polymorphic raptor, denser contour feather structure has been found in the gray morph of the tawny owl Strix aluco , providing increased plumage insulative capacity over red morph individuals (Koskenpato et al. 2016). While we included minimum temperature as a covariate in our weekly survival analyses, we found no strong effect of temperature on survival. Thermoregulatory ability is a function of many different processes related to intrinsic properties such as coloration, behavior, body size, and metabolism, but also many extrinsic properties such as land cover, solar radiation, and weather (Stuart-Fox et al. 2017). Often, color polymorphic traits in birds and mammals are correlated with a suite of other behavioral, sexual, and ecological traits through pleiotropic effects at the loci or other associated genes (Mundy 2005, Roulin and Ducrest 2011). To test whether morphs exhibit different thermoregulatory abilities, more research is needed into the genetics and potential morphological, behavioral, or metabolic differences between ruffed grouse color morphs.
Our findings support our general hypothesis that phenotypic mismatch would predict overwinter survival, but we found that the negative effect of mismatch was not constant throughout the years of our study. The effect of mismatch was strongest in years when overall winter survival was lowest, suggesting that mismatch is important, but the strength of its effect may be conditional on other factors. We did not find any support for general climate conditions mediating survival, and as such, the variability of the mismatch effect may be due to other extrinsic factors such as fluctuations in local predator abundances or availability of quality food resources (e.g., mast or aspen buds). Higher abundances of predators may increase predation pressures on grouse and subsequently increase the importance of phenotypic matching with background to avoid predation. Low food resources or high abundance of chemically guarded aspen buds, an important winter food source for grouse, may in turn lower overall body condition and make individuals more vulnerable to predation (Jakubas and Gullion 1991). Alternatively, snow presence or absence alone did not predict differences in overwinter survival, but differences in snow cover characteristics such as depth and density or fine-scale spatial or temporal variation in these properties may also mediate the effects of mismatch on survival. For example, snow-roosting in deep, low-density snow has been shown to lower stress and increase survival for ruffed grouse potentially by providing concealment from predators and protection from cold ambient temperatures through the insulative properties of deep snow (Shipley et al. 2019, 2020). Limited availability and use of deep, low-density snow for snow roosting during years of low or variable snowfall may increase the effect of phenotypic mismatch on survival. Timing of snow season may also amplify the effect mismatch as the winter season we saw the strongest effect of mismatch was also the year with earliest onset of persistent snow cover (Fig. S1). Alternatively, mismatch may always have a negative impact on survival, but the effect was only detectible in our study sample in years with a high enough number of observed mortalities. Further research into the drivers of morph-specific survival should be explored in areas of their range with different snow regimes and predator assemblages to further disentangle the effects of phenotypic mismatch and winter conditions on survival.
In addition to exploring effects of phenotypic mismatch and weather, we also explored effects of habitat type on overwinter survival for grouse. We predicted that individuals occupying areas of dense cover such as young aspen forest, would have higher survival. Dense cover associated with high stem density such as young aspen forest is thought to provide refuge from predators (Whitaker and Stauffer 2003, Zimmerman et al. 2009). Additionally, we predicted that dense cover may be able to offset negative impacts of phenotypic mismatch on survival, as was found for phenotypically mismatched snowshoe hare (Wilson et al. 2019). Instead, we found increased proportion of open habitat had a negative effect on survival, regardless of morph. Although ruffed grouse tend to occupy a range of different forest types and ages, they are very closely associated with young successional forests and reach highest populations densities in young aspen habitat (Zimmerman et al. 2009, Tirpak et al. 2010). Much of the literature documenting the importance of young forest and dense cover for grouse concerns habitat requirements during breeding and brood rearing seasons. Winter habitat requirements may differ from other seasons in that dense cover habitat is not as important for survival, and instead, survival is lower in landscapes with more open habitats. We suggest that this is driven by low concealment from predators in more open habitat types. Additionally, mature forest cover had a positive effect on survival, potentially because buds of mature aspen trees have been identified as a high-quality winter food source for ruffed grouse (Gullion and Marshall 1968, Doerr et al. 1974).