Animal populations occurring at high elevations are often assumed to be in peril of extinctions or local extirpations due to elevational-dispersal limitations and thermoregulatory constraints as habitats change and warm. However, long-term monitoring of high-elevation populations is uncommon relative to those occurring at lower elevations, and evidence supporting this assumption is limited. We analyzed 45 years of reproductive data for two Colorado populations of white-tailed ptarmigan (Lagopus leucura), an alpine-endemic species with restricted distribution in western North America. Seasonal temperatures measured by the number of growing degree days warmed significantly at our study sites for pre-nesting, nesting, and brood-rearing seasonal periods (mean advance of 8 growing degree days per decade), and both populations advanced their reproductive phenology over the study period based on median hatch dates (median advance of 3.7 and 1.9 days per decade for the northern and southern sites, respectively). Reproductive performance measured by the number of chicks per hen declined significantly at one study site but not the other, and differences between sites may have been due to habitat degradation at one study area. Annual variability in chicks per hen was large at both sites but only weakly related to seasonal weather. An index of precipitation and temperature during the brood-rearing period was the best predictor for reproductive success with warm and dry conditions relating positively to number of chicks per hen. Our results provide evidence for two alpine ptarmigan populations that are remarkably invariant to fluctuations in seasonal weather with respect to reproductive success as measured by number of chicks per hen in the breeding population. These results are surprising given the general perception of alpine animal populations as being highly sensitive to warming temperatures.

Funding: This work was supported by the National Science Foundation (1966–1969; www.nsf.gov ) through graduate support to CB through a NSF Traineeship, and also in the 1970s through the Tundra Biome Program. This work was also supported by the Colorado Division of Wildlife (1970–1999; http://cpw.state.co.us/ ) through Federal Aid in Wildlife Restoration Project W-37-R, Grouse Inc. (2000–2008), the United States Geological Survey (2007–2012; http://www.usgs.gov/ ), and Colorado State University (2008–2012; www.colostate.edu ). GW was partially supported by the Rocky Mountain Conservancy through the Leslie Bailey Charitable Trust Fellowship. The U.S. Geological Survey and Colorado State University provided support in the form of salaries for authors GW and CA, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.

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We predicted an advance in timing of breeding in our populations as the relationship between warm springs and timing of nesting is well documented in many avian species (e.g., [ 24 ]). Wang et al. [ 23 ] also found advancing hatch dates of ptarmigan for a subset of years in one of our populations (1975–1999). Ptarmigan fecundity is known to be adversely affected by spring snow depth [ 25 ] and we predicted that precipitation during spring and the pre-laying period would negatively correlate with reproductive success. We also predicted weather would not correlate with reproductive success during the nesting period because hens protect eggs from the abiotic environment during incubation. Precocial willow ptarmigan (L. lagopus) chicks are also known to be adversely affected by cold and wet conditions during brood rearing [ 26 ] which led us to predict that warm and dry conditions would positively correlate with reproductive success during this period. We discuss our results in the context of other alpine and avian studies, as well as implications for future viability of the species.

We analyzed two long-term population data sets for ptarmigan to test the effects of seasonal weather on annual breeding phenology and number of chicks per hen produced in the population (as a measure of reproductive success). Phenology data were obtained in the form of median hatch dates from captured chicks and represents data from successful nests, and reproductive data were based on numbers of chicks observed in the summer per hen in the breeding population. Our aims were to: 1) examine how recent spring warming (temperatures in April through June) has affected breeding phenology, 2) present annual rates of reproductive success based on observed counts of chicks and hens in the breeding population and test for trends in those rates, and 3) test for relationships between annual rates of reproductive success and seasonal weather.

The white-tailed ptarmigan (Lagopus leucura) is an alpine-endemic species with a restricted distribution in western North America that spends its entire life cycle in the alpine and subalpine [ 17 ]. White-tailed ptarmigan (hereafter ptarmigan), when compared to other species in the genus Lagopus, have high survivorship and low fecundity [ 18 ]. Ptarmigan raise only a single brood in a breeding season but will renest if a nest is lost during egg laying or early incubation [ 19 ]. Ptarmigan in Colorado, where our study took place, eat primarily willow (Salix spp.) in winter and spring, and various alpine forbs and sedges in summer [ 20 ]. The diet of chicks consists almost entirely of invertebrates during the first few weeks of life [ 21 ]. Like other species in Tetraoninae, ptarmigan chicks are precocial and incapable of self-thermoregulation during their first weeks of life and must be brooded by hens for warmth (e.g., [ 22 ]). Ptarmigan are well adapted for life in the alpine, but there have been recent concerns the species is facing threats from climate warming due to their cold-adapted biology [ 23 ].

Animals living in alpine systems must cope with strong seasonal climate changes and short growing seasons when breeding occurs [ 11 , 12 ]. Species occurring in alpine systems, compared to those in lower elevation habitats with longer growing seasons, are limited in the number of breeding attempts in a breeding season (e.g., [ 12 ]), and annual productivity is generally lower in high-elevation systems [ 13 , 14 , 15 ]. Reduced breeding opportunities may cause greater variability in annual fecundity as stochastic events such as extreme spring weather delaying breeding should have larger effects in systems with short versus long breeding seasons [ 12 ]. For these reasons, animal populations occurring in alpine systems may be particularly vulnerable to extreme seasonal weather and climate. Warming may also positively impact vertebrate populations in alpine systems if longer growing seasons confer fitness benefits. For example, Ozgul et al. [ 7 ] found that yellow-bellied marmots (Marmota flaviventris) benefited from increased spring temperatures in Colorado because individuals awakening from hibernation earlier also bred earlier. Earlier breeding was associated with heavier offspring, and heavier offspring survived at higher rates than lighter individuals. Relationships between advanced breeding and fitness may occur in other taxa, such as some avian species, which are known to respond strongly to warming spring temperatures by breeding earlier (e.g., [ 16 ]).

Alpine ecosystems are extreme examples of high-elevation habitats and frequently cited as being imperiled due to climate change (e.g., [ 1 , 2 ]). Animal populations endemic to these systems may be threatened due to constraints to dispersing to higher habitats if physiological limitations to temperature (e.g., [ 3 , 4 ]) or changing structure and distribution of vegetation (e.g., [ 5 , 6 ]) make their current habitats unsuitable. Studies in alpine systems have linked climate change to different attributes of animal populations, such as physiology and demography in marmots (Marmota spp.) [ 7 ], body mass of chamois (Rupicapra rupicapra) [ 8 ], and distributional shifts in avian populations [ 9 ]. However, few studies have demonstrated links between climate change and population declines or extinctions in alpine systems (but see [ 10 ] for pika [Ocotona princeps] in the Great Basin). The lack of information is undoubtedly due in part to the difficulty of collecting population-level data in alpine systems relative to those occurring at lower elevations. As a result, alpine systems offer opportunities to study populations in extreme yet vulnerable environments.

Materials and Methods

Permits Banding permits were issued by Colorado Parks and Wildlife. Approval for handling wildlife (2009–2012) was provided through Colorado State University's Institutional Animal Care and Use Committee (IACUC).

Study areas We studied ptarmigan at two locations in central Colorado beginning in 1968. The Mt. Evans study area (hereafter ME) is roughly 17 km southwest of Idaho Springs (39° 35’ N, 105° 37’ W) and consists of 7.03 km2 of alpine habitat with an elevation range between 3535 and 4270 m. Data were collected continuously at ME from 1968 to 2012, with the exception of 1977 and 1999 when field work was limited. The ME study area was open to fall hunting (typically beginning in mid-September and ending in early October) until a permanent closure went into effect in 1994. The Rocky Mountain National Park study area (hereafter RM) consists of 9.11 km2 of alpine habitat along Trail Ridge (40° 25’ N, 105° 45’ W) with an elevation range between 3505 and 3688 m. Data were collected from RM continuously from 1968 to 2000, and again in 2011 and 2012. Both study sites have similar habitats characterized as alpine tundra with plant communities consisting of low-growing woody shrubs (e.g., Salix spp.), herbaceous forbs (e.g., Geum rossii, Polygonum spp., Ranunculus spp. Sedum spp.), sedges (e.g., Carex spp.), and grasses (e.g., Deschampsia spp., Poa spp., Trisetum spp.). The lands where research was conducted was managed by the U.S. Forest Service and National Park Service.

Measuring reproductive success and phenology Surveys of the study areas occurred in spring (typically the second half of May and first week of June) and summer (typically the second half of August and first week of September). The number of surveys within each season varied by year, although in nearly all years and seasons the study sites were surveyed a minimum of 3 days with 8 or more hours of surveying occurring each day. This amount of time and effort allowed us to survey the extent of area and habitats within the defined study areas. Hens were located and captured in the spring by first locating territorial males using broadcasts of male calls [27]. Males that successfully attracted hens generally stayed in close proximity to their mates, and most hens were found by searching the area in the immediate vicinity of territorial males [27]. Broods were located in the summer by searching suitable habitats (e.g., moist meadows near rock cover) and broadcasting chick distress calls to elicit responses from hens with broods or hens that recently lost broods [27]. Once broods were located we attempted to capture all observed chicks using a noose at the end of a 5-m pole. Captured hens and chicks were marked with numbered State of Colorado aluminum leg bands. Hens also received unique combinations of colored plastic bandettes (between 2 to 4) for individual identification during subsequent resightings. Individual markings of hens greatly reduced the likelihood of double counting broods during surveys. All hens first captured on the study areas in the spring and observed in the summer were considered breeding residents, even if not observed on the study areas in the spring during subsequent years. We considered these hens breeding residents because hens found on the study area in spring exhibit high site fidelity, especially among adults [28]. Dispersal by females to other breeding territories in early spring (both within and outside the study area) is known to occur at low rates at ME and surrounding areas [29]. We assessed potential bias due to sampling effort in our field methodologies which are presented in supporting information (S1 Appendix). The reproductive measure of interest in this study was the number of chicks produced surviving to the summer count period per hen in the breeding population. Ptarmigan chicks generally remain with females for 8 to 10 weeks [17], although chicks can thermoregulate independently of hens when they reach 3 to 4 weeks of age [22], and may stay with hens beyond 10 weeks if separation does not occur earlier (CEB personal observation). Thus, age at independence is a gradual process and difficult to define [17]. The mean age of broods encountered during summer counts was between 5 to 7 weeks. We used counts of chicks and hens to measure annual variation in reproductive success. The number of chicks per hen was used as an overall measure of reproductive success. The number of chicks per hen was estimated using the total number of chicks observed in summer per hen in the spring population. We used spring hens rather than summer hens because unsuccessful summer hens may disperse long distances after nest or brood failures [29], either into or outside of the study areas. The open nature of ptarmigan populations in summer could introduce bias (e.g., poor reproductive success inside the study areas might lead to higher numbers of unsuccessful hens dispersing outside the study areas and result in a positive bias of reproductive success, and vice versa). It is important to note that the number of chicks available to count in the summer period is the combined product of number of females in the breeding population and, nest, renest, and chick survival probabilities. Hens were not monitored between spring and summer count periods and we could not estimate nest and chick survival. Chicks per hen is a reproductive measure that informs us of how many young per hen in the breeding population survived to the count period after nest and young chick mortality occurred. Previous studies at ME and elsewhere report reproductive rates and survival rates of chicks at various stages [17, 18, 19, 29]. Various body measurements were recorded from captured hens and chicks, including length measurements for primaries 1–10 (measured to the nearest millimeter). Chick ages can be accurately estimated to within a few days based on the length of the most recently replaced primary feather [30], and it was from these measurements that we calculated the date of hatch for each captured chick. An average date of hatch was calculated for every brood by summing the ages of individual chicks within the brood and dividing by the number of chicks assigned to the brood. However, ptarmigan are known to adopt chicks [31], in which case brood averages of date of hatch could be inaccurate if the age of adopted chicks is different from the biological offspring captured with hens. It was possible that hens could be encountered with chicks originating from different broods. If the estimated age of captured chicks differed by 6 days or more from other individuals within the group, we considered those chicks to have originated from a different brood and calculated separate averages. We used date of hatch (reported as the Julian day) as our measure of annual breeding phenology for ptarmigan. The first date of hatch (first brood to hatch in a year) and median date of hatch were response variables in our phenology analysis.

Covariates Weather data were obtained from the Niwot Ridge Long Term Ecological Research site. This was the closest location available for our study areas that included the weather variables of interest dating to the beginning of our study. The D1 weather station at Niwot Ridge is at an elevation and topographic position similar to the study locations. ME and RM study areas are 49 km south and 42 km north from the D1 weather station, respectively. Spring weather data used as explanatory variables for date of hatch included the sum of maximum temperature (warmth sum; WS), cumulative precipitation (CP), and number of growing degree days (GDD). Number of growing degree days was obtained by summing the number of daily growing degrees, which was calculated as: (T max −T min )/2 − T base , where T max and T min are the daily maximum and minimum temperatures, and T base is the base temperature below which plant growth will not occur. We set T base equal to 0°C and also set a cap equal to 30°C [32]. The choice of temperature explanatory variables was based on previous studies relating weather data to nesting phenology [24, 33, 34]. Past work has shown that weather events occurring up to 2 months prior to the onset of nesting can have strong effects on breeding phenology in avian species [24]. The average nest initiation date in our study populations was estimated to occur on 8 June at ME and 15 June at RM [17]. We used the period 2 months prior to these dates (8 April to 8 June for ME; 15 April to 15 June for RM) to calculate the variables warmth sum, cumulative precipitation, and number of growing degree days. We examined relationships between reproductive success and weather occurring over seasonal periods for the reproductive analysis. We used weather data for three seasonal periods, including a pre-nesting period covering one month prior to the average onset of egg laying (10 May to 8 June for ME; 17 May to 15 June for RM), a nesting period covering the average times between the onset of egg laying and nest hatching (9 June to 7 July for ME; 16 June to 14 July for RM), and a brood-rearing period covering a two-week period post hatch when chicks are most sensitive to weather (8 July to 21 July for ME; 15 July to 28 July for RM). These periods were defined based on our prior knowledge of reproductive events in the study areas (Braun et al. 1993). Weather variables examined for the seasonal periods included cumulative precipitation (CP), number of growing degree days (GDD), and an index of seasonal wetness and dryness (SIND = GDD/CP). We used a simple naming convention for weather variables presented in models where “S” followed by the season number (1 = spring, 2 = pre-nesting, 3 = nesting, 4 = brood rearing) denotes the period to which we are referring (e.g., S1.GDD is the number of growing degree days during the spring period). A description of the covariates is summarized in Table 1. The spring weather covariates used for the phenology analysis were also considered to affect reproductive success and included in the reproduction analysis. PPT PowerPoint slide

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larger image TIFF original image Download: Table 1. Terms used for response variables, covariates, and periods over which weather data were measured. A description for each term is provided. Covariates are presented in the model results with a prefix for the specific period they represent. Study sites were at Mt. Evans (ME) and Trail Ridge at Rocky Mountain National Park (RM) in Colorado. https://doi.org/10.1371/journal.pone.0158913.t001 We were also interested in site, hen age, and density-dependent effects in addition to weather covariates. Site effects were measured using a categorical variable (SITE) to code for each of our two sites. Hen age is an important factor influencing reproductive success in ptarmigan [19], but it could not be directly assessed in our analysis because we modeled annual counts as the response variable. To consider age, we included a covariate that was calculated as the ratio of yearlings to adults in the spring population as a measure of age structure. Density-dependent effects were measured based on the spring density of ptarmigan at our study sites. Intercept only models were used to test the explanatory power of our covariates versus a mean with no annual variation. In the case of weather covariates, we also included site as an additive or interactive effect because weather was examined over slightly different periods (i.e., 7-day difference in first and last dates of seasonal windows) for each site. Log transformations were used on some covariates to better approximate a normal distribution.