Seasonal changes in plumage density, plumage mass and feather morphology in the world’s northernmost land bird

doi:10.21203/rs.3.rs-2087743/v1

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Seasonal changes in plumage density, plumage mass and feather morphology in the world’s northernmost land bird

https://doi.org/10.21203/rs.3.rs-2087743/v1

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published 24 Mar, 2023

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The Svalbard ptarmigan is the year-round resident terrestrial bird in the high Arctic. While the physiological and morphological adaptations permitting its winter endurance are reasonably well understood, it remains unknown how the conspicuous moult from a greyish brown summer- to a white winter plumage, and any underlying changes in plumage structure and feather morphology, contributes to seasonal acclimatisation. Thus, using standard morphometric techniques, we, firstly, measured seasonal change in plumage and feather characteristics in six body regions. We then investigated if winter plumage traits differ between first-winter and older birds, because differential plumage acclimatisation has been suggested as an explanation for why young Svalbard ptarmigan lose more heat in winter. Plumage feather density (i.e., feathers × cm-2) and mass density (i.e., mg feathers × cm-2) was higher in winter, particularly on the head and feet where individual feathers were also heavier, longer, and downier. Seasonal changes in other regions (back, tarsi) indicated acclimatisation primarily to resist wear and wind. First-winter and older birds had similar feather density. However, mass density in the young birds was significantly lower in all but one body region (back) since individual feathers weighed less. This can explain previous observations of higher heat loss rates in first-winter birds. Our study suggests that plumage acclimatisation contributes to optimising winter phenotypes, both through higher insulative capacity and by improved resistance to harsh weather. The extent of these adaptations may be balanced by the time or energy available for feather growth, exemplified here by inferior insulation in first-winter birds.

Arctic

feather

moult

plumage

polar

thermoregulation

Animals that permanently reside in seasonal environments at high latitude must deal with pronounced variations in environmental conditions, including air temperature, photoperiod, and precipitation. This presents particularly large challenges in winter, when low temperatures mayincrease thermoregulatory energy costs, whilst short periods of daylight and food scarcity makes it more difficult to amass fuel. Hence, there is seasonal adaptation of physiology, morphology, and behaviour in high latitude residents (Blix 2016), such that winter-acclimatized animals are typically more efficient both in producing heat and in minimizing heat loss, than are the summer-acclimatized individuals (Blix 1989; Signer et al. 2011; Swanson and Vézina 2015; Haftorn 1992; Mortensen and Blix 1986; Nord and Folkow 2018).

Heat loss rate can be altered immediately by increasing or decreasing local (skin) temperature in the body periphery, by way of adjustments in blood flow rate and/or circulatory pattern to these tissues (e.g. Irving and Krog 1955; Midtgård 1981; Johansen and Bech 1983). This allows animals to respond quickly to changes in their thermal environment or in their own thermal/energetic state (Winder et al. 2020; Tattersall et al. 2009; Ekimova 2005). However, the most decisive factor for heat balance in terrestrial taxa is the pelage (Scholander et al. 1950) In birds, this is provided by body feathers that cover most of the integument. The distal (‘pennaceous’) end of these feathers makes up the external layer of the plumage with the dual primary functions of protecting the inner plumage layers from the environment (including convective heat loss by wind, precipitation, and low temperature) and serving in communication (Prum and Brush 2002). The inner layer of the plumage contributes insulation and is composed of the proximal downy, or ‘plumulaceous’, parts of the body feathers (Fig. 1A) as well as specialised down feathers and semiplumes (Pap et al. 2020). Many species also have an auxiliary down-like feather attached to the base of the contour feathers (‘afterfeather’; Prum and Brush 2002), which is believed to function mostly in insulation (Williams et al. 2015). The plumage keeps birds warm by trapping air (and thereby body heat) in a matrix of interlocking barbs and barbules of the contour feathers (Fig. 1A). This probably explains why, across the bird phylogeny, species that occupy colder environments have more feathers per unit area and individual feather elements that are downier and loftier (i.e., have fewer barbs along the shaft), than do warmer-environment counterparts (Osváth et al. 2018; Pap et al. 2017). The same applies to the intraspecific level, where cold-hardier subpopulations have downier contour feathers (Koskenpato et al. 2016; Barve et al. 2021) While it is unsurprising that birds residing in colder areas are better insulated, less is known about the role of the plumage in seasonal acclimatisation to winter conditions. However, thermal conductivity of the plumage was nearly 30% higher in summer than in winter in rufous-collared sparrows (Zonotrichia capensis), a Central and South American sparrow (Novoa et al. 1994). Moreover, the dry mass of contour feathers was 31% higher in winter than in summer in the dark-eyed junco (Junco hyemalis), a temperate North American sparrow that may breed far into the Arctic, coincident with a seasonal increase in thermogenic capacity and cold tolerance (Swanson 1991). On the other hand, while the winter plumage in some cardueline finches from central North America was significantly heavier than summer plumage (Middleton 1985; Dawson and Carey 1976), the seasonal improvement in cold hardiness was not associated with the development of a thicker coat (Dawson and Carey 1976). While previous work points to mixed evidence for a role of the plumage in winter acclimatisation, it should be noted that these studies have been performed using small (< 50 g) species with low thermal mass and correspondingly high heat loss rates. As a result, small birds rely mostly on seasonal improvement in thermogenic capacity to stay warm in the winter (Swanson and Vézina 2015), whereas larger species can exploit improved insulation to a greater extent on account of their larger thermal mass (Blix 2016). Yet, to our knowledge there are no studies of seasonal changes in the micro- and macroscopic morphology of feathers and plumages in large birds.

To elucidate the role of body insulation in the winter energy balance of a large bird species, we studied the seasonal changes in plumage and feather traits in the Svalbard ptarmigan (Lagopus muta hyperborea Sundevall, 1845), the world’s most northerly distributed land bird. In winter, this bird experiences cold temperature and continuous darkness for four months, where foraging opportunities are scarce and unpredictable. To exist in this environment, the Svalbard ptarmigan exhibit a range of morphological and physiological adaptations, including a conspicuous autumnal fattening starting in late summer (Stokkan et al. 1986b) and downregulation of metabolically expensive processes such as immune function and locomotion in winter (Lindgård et al. 1995; Nord et al. 2020). There is also a post-nuptial moult from a greyish-brown, cryptic summer coat into a white winter coat, but it is not known if this entails structural changes to improve winter energy balance. Hence, we studied plumage thickness and density, as well as the macro- and microstructure of feathers, in key body regions for heat exchange, in summer- and winter-acclimated Svalbard ptarmigan. If winter acclimatisation also occurs on the level of the plumage, we predicted that winter birds would have a denser plumage with heavier feather elements, and individual feathers more conducive for heat retention, i.e., with a larger proportion of down and fewer feather elements along the shaft. There is a difference in the extent of the seasonal metabolic downregulation between first-winter and older Svalbard ptarmigan (Nord and Folkow 2018). It has been hypothesised that this reflects an age-related differential seasonal adaptation of the winter coat (Nord and Folkow 2018) because moulting into a more insulating plumage requires both nutritional resources, energy, and time (Nilsson and Svensson 1996; Broggi et al. 2011; Lindström et al. 1993; Pap et al. 2008). This can be difficult to reconcile in first winter birds that probably face a resource-based trade-off between physical maturation and feather growth that is not present to the same extent in mature birds (Butler et al. 2008). We tested this hypothesis by comparing winter plumage traits in Svalbard ptarmigan in their first winter with that in mature birds, under the prediction that first-winter birds would have a thinner, less dense plumage than older conspecifics. This study provides new information on causes and constraints on seasonal adaptation of body insulation and lays new pieces to the puzzle that explains the basis for winter existence in the world’s northernmost terrestrial bird.

Data on plumage and feather characteristics were collected opportunistically from 38 Svalbard ptarmigan that had died of natural causes or been euthanized for tissue collection for other studies, between 2009 and 2017. The birds were either bred at UiT – the Arctic University of Norway, or were caught as young chicks near Longyearbyen, Svalbard (78 °N). They all completed their somatic growth and moult in captivity in Tromsø, either in indoor facilities in thermoneutrality (0 to + 5°C; Mortensen & Blix 1986, Nord & Folkow 2018) with simulated Svalbard photoperiod or outdoors subject to natural Tromsø photoperiod (69 °N) and temperature. Previous research has shown that the basic physiological and morphological characteristics do not differ in birds of wild and captive origin (e.g. Lindgård and Stokkan 1989; Stokkan et al. 1986a). Nine birds were in summer plumage (3 males, 6 females) and 29 in winter plumage (11 females, 17 males, 1 of unknown sex).

All birds were stored in -20°C prior to sampling, which occurred in 2016 and 2018. Plumage density characteristics were measured in six body regions with previously demonstrated significances for heat exchange (Nord and Folkow 2018, 2019; Mercer and Simon 1987), viz. in the periorbital area of the skull (“head”), between the scapulae (“back”), in the pectoralis area laterally to the sternal keel (“breast”), laterally on the outwards facing part of the tibiotarsus (“tarsus”), dorsally on the metatarsus (“foot”), and laterally on the innermost of the forward-pointing digits (“toe”) (Fig. 1B). Data were collected using protocols from our previous work (Osváth et al. 2018; Pap et al. 2020). Briefly, all feathers were plucked individually from the region of interest in completely thawed birds (to make sure no soft tissue adhered to the calamus), after which the bare skin area was photographed against a 1 × 1 mm grid, as scale reference. The feathers were then counted and put into a drying oven at 37°C for 48 h before being weighed to the nearest 0.1 mg. Pilot measurements confirmed that drying beyond 48 h was not associated with any further reduction in sample mass. The area of the plucked region of interest was measured in cm² using the freely available software ImageJ (Schneider et al. 2012), allowing us to derive metrics of plumage feather density (feathers × cm^− 2), plumage mass density (mg feathers × cm^− 2), and individual feather mass (i.e., total plumage mass / total feather count; in mg). Sample size varied between plumages, ages, and body parts depending on which tissues had been harvested for other projects before plumage measurements were made (cf. Tables 1, 2).

To measure feather macro- and microstructure, we collected feathers from the head, back, breast and leg in 14 birds in summer coat (2 females, 12 males), and again from the same birds, once they had completed moult into their winter. Data were also collected from three additional birds (all male) in winter plumage. We photographed one representative feather (as per our previous studies; e.g. Osváth et al. 2018; Pap et al. 2020; Pap et al. 2017) per bird, body region and season against a 1 × 1 mm grid and used these photographs to measure total feather length (i.e., fan + calamus), the proportion of downy (plumulaceous) barbs of total length, and density (i.e., no. per unit length) of plumulaceous and pennaceous barbs and barbules (cf. Pap et al. 2017). These morphological structures are illustrated in Fig. 1A. We were not able to measure the density of plumulaceous barbules on the head feathers because this structure was too small to meter accurately with our microscope. Leg feathers were downy in entity in both summer and winter, and so there are no data for pennaceous barbs and barbules for this feather type.

Statistical analyses

All statistical analyses were performed using R version 4.0.3 (R Core Team 2021). Seasonal changes in plumage feather density and plumage mass density, and feather weight, were compared in separate linear mixed effects models (lmer function in lme4) (Bates et al. 2015) with season (summer or winter) and body part, and their interaction, as fixed effects, and bird ID nested in plumage type as a random effect. The effect of age (first winter, 1 CY (calendar year) ; second winter or older, 2 CY+) was analysed using an identical model structure but using age in lieu of plumage as the explanatory factor. Age models were run using the same fixed structure, but with bird ID nested in age as the random factor. These models were fitted using the winter subset only, since we did not have access to any first summer birds (i.e., growing chicks). However, measurement on such birds would likely not have been meaningful, because Svalbard ptarmigan never attain a discrete post-juvenile summer plumage in their first year (A. Nord, pers. obs.). Nor would measurement on birds in their first summer plumage (i.e., when in their second calendar year) have been suitable to test the hypothesis on constraints on optimal moult in young birds, because all age-related differences in heat production and heat loss rates have disappeared by this time in Svalbard ptarmigan (Nord and Folkow 2018). We were not able to compare plumage traits on the breast between the age categories, because the pectoral muscles in all but two 1 CY birds had been excised for use in another study prior to feather sampling.

All feather structure data (apart from the proportion of plumulaceous barbs) were analysed using the same model structure, including bird ID as a random effect. The proportion of plumulaceous barbs was analysed using a generalised linear mixed effects model (glmer in lme4) with a binomial error structure and the fixed and random terms above. Significances were assessed using likelihood ratio tests in all cases. Non-significant (i.e., P > 0.05) interactions were removed from the models but main effects were always retained. When interactions were significant, we performed pairwise comparisons between plumage types within each level of body part, using the emmean function in the emmeans package (Lenth 2019).

All dependent variables (except for the proportion of plumulaceous barbs) were log-transformed before analyses to meet parametric assumptions (as inferred from diagnostic plots).

Descriptive data for all plumage and feather traits, arranged by body regions, seasons, and ages, are available together with the output from the statistical models in the Electronic Supplementary Materials (ESM 1). Effect sizes reported in the text refer to model-predicted values.

Plumage feather density and mass density differed between summer and winter on the head, breast, and toes (Table S1). The largest seasonal changes occurred on the toes, where there was a 2.5-fold increase in feather density, a 5.9-fold increase in mass density, and a 2.4-fold increase in mean feather mass, between summer and winter (Fig. 2). As a result, the proportion of bare skin in contact with the ground (i.e., on the underside of the feet) decreased from 44–0% (data not shown). Head feather density was 1.4-fold greater in winter, and mass density increased 2.9-fold (Fig. 2A, B). Mean head feather mass was also 2.1-fold higher in winter than in summer (Fig. 2C). In winter, the breast plumage was 30% denser than in summer (Fig. 2A), but individual feathers weighed 40% less (Fig. 2C). As a result, the plumage in the breast region weighed as much in winter as it did in summer (Fig. 2B).

There was no difference in plumage feather density in any body region between 1 CY and 2 CY + birds (Fig. 3, Table S2). However, mass density was higher in 2 CY + birds in all regions but the back. Specifically, on the head and tarsi, 2 CY + birds had plumage with 30% higher mass density compared to 1 CY birds. On the feet and toes, the mass density of the plumage in 2 CY + birds was 200% and 40% higher than in 1 CY ptarmigan, respectively (Fig. 3B, Table S2). As expected in view of similar plumage density, differences in mass density were driven by heavier feathers in all body regions in the 2 CY + birds (Fig. 3B, 2C, Table S2).

Seasonal changes in the macro- and microstructure of individual feathers were recorded mainly on the head, back and tarsus (Table S3). Head feathers were 1.5 times longer and 2.8 times downier in winter, whereas back feathers were 10% shorter, but 30% downier, in winter than in summer. Tarsus feathers were also 10% shorter in winter than in summer (Fig. 4A, B). Individual head feathers were loftier in winter. Specifically, on the head, there were 60% fewer pennaceous barbs and 10% fewer plumulaceous bars per mm feather, in winter than in summer (Fig. 4C, D). Thus, winter head feathers had fewer feather elements per unit length. By contrast, feathers on the tarsi (whose feathers were always plumulaceous in entity) showed 20% higher barb density in winter compared to summer (Fig. 4D). The interaction between season and body region was never significant in the barbule models. However, when averaging over body parts, the density of pennaceous barbules was lower in winter than in summer. Across seasons, pennaceous barbule density was higher, (which is suggestive of higher insulative capacity) on the back compared to the head which, in turn, had higher pennaceous barbule density than the breast (Fig. 4E). Plumulaceous barbule density did not differ between summer and winter, and was the highest on the back, followed by the breast and tarsus (Fig. 4F).

Our study clearly suggests that the post-nuptial moult into a white winter plumage in Svalbard ptarmigan is associated with morphological adaptation to counter low temperature, increased snow depth, and inclement weather during the cold season. On average, the winter plumage had more feathers and feather mass per unit area (i.e., density and mass density were higher), and was composed of heavier and loftier feathers (i.e., with fewer feather elements per unit length) with more insulating down. These traits will improve coat insulation by increasing air space within the plumage and correspond well to plumage and feather adaptation to low temperature in interspecific studies (Pap et al. 2017; Osváth et al. 2018; Pap et al. 2020).

Seasonal acclimatisation varied in both type and magnitude between body regions, which probably reflects the multiple simultaneous roles of the plumage as a physical barrier between the body and the environment (Prum and Brush 2002). We found pronounced seasonal changes on the head, where the winter plumage was denser, and individual feather elements were heavier, longer, downier, and loftier than in summer. It is not surprising that morphological adaptation of head plumage and feather traits were more pronounced than in other body regions. Specifically, the proximal location and high surface-area-to-volume ratio of the ptarmigan head, with its highly metabolically active brain, makes it particularly poorly insulated (Nord and Folkow 2018, 2019) to the point where a significant proportion of the metabolic heat produced in winter might have to be allocated just to keeping the head warm (Nord and Folkow 2018). Because peripheral cooling (local heterothermy) in the head region could impair cognitive ability (Carr and Lima 2013; Rashotte et al. 1998), and consequently increase predation risk (Carr and Lima 2013; Brodin et al. 2017), investment in head insulation seems a prudent fitness consideration.

While area-specific heat loss from the head is likely the highest across the ptarmigan integument (Nord and Folkow 2018), total heat loss will probably be the largest from the body trunk on account of the considerably larger surface area (cf. McCafferty et al. 2013). In view of this, it is somewhat surprising that there were few seasonal changes to plumage- and feather traits across the back and breast. For example, breast feather density increased between summer and winter (Fig. 2A) but because individual feathers were lighter (Fig. 2C), there was no seasonal improvement in plumage mass density (Fig. 1B), which is propably more instrumental for insulation. It is possible that a denser (i.e., more feathers per unit area) coat is more resitant to wear, which could be an important consideration since ptarmigan sport the same winter plumage for 9 months of the year (Stokkan et al. 1986a; Steen and Unander 1985). Alternatively, or additionally, it is possible that strcuture of the plumage covering the pectoral muscles (the most thermogenic tissue in birds; Hohtola 2004) represents a trade-off between the need to minimise heat loss at rest but to allow sufficient heat dissipation during strenous activity, for which a sparesely feathered ventral surface is important (Nord and Nilsson 2019). Back feathers were some 10% shorter, but 30% downier, in winter. These feathers were by far the longest and heaviest year-round, so it is possible that a seasonal increase in either length or density on the back might not be compatible with other plumage functions, such as keeping drag minimal during flight. However, the back plumage is key to sheltering thoracic/abdominal internal organs by keeping heat loss minimal, since even at rest and in inclement weather Svalbard ptarmigan will often have the entire dorsal surface exposed (AN, pers. obs.). It is possible that the added insulation from an increased amount of down countered any negative effect on insulation from feather length reduction bewteen summer and winter (Pap et al. 2020). Moreover, shorter feathers might be less susceptible to disruption by strong winds, helping to keep the feather layer intact during spells of inclement weather in winter. This protective role of the back plumage can also explain why plumulaceous barbule density was the highest in back feathers (Fig. 4F), facilitating adhesion between feather elements in the insulative layer (Prum and Brush 2002).

Feathering on the ventral and lateral aspects of the foot (“toes”) increased profoundly between summer and winter (Fig. 2), such that the proportion of ventral skin in contact with the ground surface decreased from some 44% in summer to 0% in winter. This could provide energetic benefits by reducing conductive heat loss through the feet, and, not the least, reduce risk of foot freeze injuries, in winter (Gates 1980). However, conductance through foot tissue will probably be low even without seasonal adaptation of plumage thickness and density since counter-current vascular arrangements together with control of motor state in the blood vessels in ptarmigan legs (Midtgård 1981) presumably allow regulation of foot pad temperature near ambient (Mercer and Simon 1987). It is plausible, therefore, that, aside from keeping foot tissue from freezing, the main energetic benefit of the seasonal growth of ventral and lateral plumage of the digits is a “snowshoe effect” whereby the load when walking on soft snow is greatly reduced (Höhn 1977). Staying on top of ground substrate will reduce the cost of transport (Mármol-Guijarro et al. 2021) which, when coupled to a seasonal improvement in the energetic efficiency of locomotion (Lees et al. 2010), might be more influential for the energy budget than the reduction in heat transfer rate from the foot pad. Efficient physiological (cardiovascular) control of leg and feet heat loss could also explain why there were no seasonal differences in plumage traits on the legs and dorsal aspects of the foot. In line with this idea, leg feathers were shorter and had increased barb density in winter (Fig. 4A, D). These changes should reduce insulative value but will probably make the feathers more resistant to physical wear and increase feather-to-feather adhesion when the bird is in the wind.

Plumage density (i.e., the number of feathers per unit area) was relatively similar between the winter plumages of young (first winter) and older (second winter, or older) birds, but plumage mass density (i.e., the mass of feathers per unit area) was significantly higher in nearly all body regions in the older birds (Fig. 3). This observation is in keeping with the notion of temporal and energetic constraints on moult in juvenile birds (Butler et al. 2008) that might carry over to plumage insulation (Broggi et al. 2011; Nilsson and Svensson 1996). Our study therefore supports the hypothesis that time- or energy allocation-based constraints on investment in plumage growth, together with lower fat deposits, can explain the elevated heat loss rates in first winter compared to older Svalbard ptarmigan (Nord and Folkow 2018). Here, this trade-off between completing somatic growth and investing in a high-quality plumage was evident not by the number of feather elements but instead by their lower mass (Fig. 3). Because our birds were captive and so had unlimited resources to invest in feather growth, it is plausible that the main constraint on feather development was time. Svalbard ptarmigan chicks hatch in mid- to late July and even though they double their body mass every week, they still weigh only about two thirds of adult weight when moult commences (Steen and Unander 1985). On the other hand, being raised under sheltered captive conditions may have caused acclimation-related effects on first-winter plumage mass and quality. Future studies should critically test these aspects by studying wild birds and by measuring the thermal conductivity of plumaged skin samples (e.g. Ward et al. 2007) or, preferably, whole plumaged skins (e.g. Bakken et al. 1983; Bakken et al. 1981) in young and old birds over a range of relevant environmental conditions.

Our study suggests that seasonal changes in plumage and feather traits optimise the winter phenotype in Svalbard ptarmigan. These seasonal adaptations differ between body regions and feather types in line with the multiple functional roles of the plumage, entailing providing insulation, aiding locomotion, and shielding from wind and precipitation. However, the extent of these adaptations is balanced by the time and/or energy available for feather growth, much like what is found in other bird species.

ACKNOWLEDGEMENTS

Hans Lian, Hans Arne Solvang, and Renate Thorvaldsen excellently cared for the experimental birds. Daniel Appenroth and Gabriela Wagner kindly provided additional material for the plumage characteristics study.

FUNDING

AN was supported by the Swedish Research Council (grants no. 637-2013-7442, 2020-04686) and the Carl Trygger Foundation for Scientific Research (grant no. 14-347). PLP was financed by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences (HAS).

ETHICS

Ethical permission for the upkeep of birds that were used in the feather trait study was granted by the Norwegian Food Safety Authority (FOTS-6639).

AUTHORS’ CONTRIBUTIONS

AN and PLP conceived the idea and designed the protocol with input from LPF. AN collected the data and measured feather and plumage traits together with BJ and VH. AN, PLP and LPF interpreted the results. AN analysed the data, produced the graphical material and wrote the first draft, which was edited by all authors. All authors approved submission and agreed to be accountable for all contents.

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No competing interests reported.

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Seasonal changes in plumage density, plumage mass and feather morphology in the world’s northernmost land bird

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