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5 June 2017 Changed Arctic-alpine food web interactions under rapid climate warming: implication for ptarmigan research
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Abstract

Ptarmigan are herbivorous birds that are year-round residents of alpine and arctic ecosystems — presently subjected to the most rapid climate warming on earth. Yet, compared to other bird taxa there has been little climate impact research on ptarmigan. Ptarmigan population dynamics, in particular in the sub/low-arctic, appears to be strongly influenced by complex interactions with a suite of functionally diverse predators in the food webs. We review evidence supporting that the strength of such predator—ptarmigan interactions has been altered, most likely due to climate change, having led to rapidly declining ptarmigan populations and in some places national red listing. Predation-mediated population declines are likely linked to dampened population cycles of keystone mammal herbivores (inducing increased apparent competition/reduced apparent mutualism), altitudinal/latitudinal expansions of boreal mesopredators and possibly mismatched ptarmigan plumage colour in spring and fall. Yet, other rapid food web mediated impacts are likely to act bottom—up, such as phenological mismatches with food plants and competitive interactions with other irrupting herbivores. We advocate that ptarmigan researchers should team up with specialists on other taxa in order to adopt a food web approach to their research. Coordinated action of research teams, to make comparative studies among ptarmigan species or populations imbedded in food webs of varying structure or ambient climate, may be rewarding in the age of rapid ongoing climate changes.

Climate change has profound effects on biodiversity in a range of habitats across the earth (Sala et al. 2000, Parmesan and Yohe 2003, Parmesan 2006, Miller-Rushing et al. 2010), including significant impacts on the distribution and abundance of bird species (Crick 2004, Gregory et al. 2009, Møller et al. 2010, Jenouvrier 2013). The rate of warming in regions at high altitudes and latitudes has been much higher than the global average (Brunetti et al. 2009, Ims et al. 2013a), and consequently some of the largest ecological impacts of climate warming have been observed in the Arctic (Post et al. 2009b). Furthermore, the continued warming projected to take place during this century in these regions are so extreme (Xu et al. 2013), that they can be expected to radically transform alpine and Arctic ecosystems (Ims et al. 2013a). In this paper, we focus on the likely implications of climate change for ptarmigan — a genus of birds of great ecological and societal importance in alpine and arctic regions.

Ptarmigan Lagopus spp. are among the most intensively studied birds worldwide (Storch 2007, Moss et al. 2010). The historic attractiveness of these herbivorous birds to research can be explained by their role as important upland game species (Aanes et al. 2002), both for recreation and subsistence (Barth 1877), and their fascinating population dynamics, often characterized by multiannual density cycles (Moss and Watson 2001). Willow ptarmigan Lagopus lagopus and rock ptarmigan Lagopus muta have circumpolar distributions, whereas white-tailed ptarmigan Lagopus leucura are restricted to the western North America (Storch 2007, Potapov and Sale 2013). The willow ptarmigan, which is likely the Earths' most abundant tetranoid bird species, is continuously distributed in the low-arctic tundra and subarctic tundra—forest ecotone, while the rock and white-tailed ptarmigan are found in rocky habitats of high-arctic or highalpine tundra (Storch 2007). The rock ptarmigan has the widest distribution range, spanning temperate alpine habitats in Europe and Japan to high-arctic regions in Greenland and Svalbard.

Despite being among the most studied bird species worldwide, studies concerning ptarmigan's sensitivity to climate change are limited (cf. Møller et al. 2010, Ims et al. 2013a), which is in stark contrast to the generally prominent position of bird studies in climate—ecological research (Guillemain et al. 2013, Jenouvrier 2013). In their extensive review of climate change effects on birds, Møller et al. (2010) included just a single citation of a ptarmigan study (Wang et al. 2002), while the same book has plenty of references to studies of arctic mammals. Knowledge gaps are not necessarily due to higher resilience of ptarmigan to climate change than other bird species. It is perhaps rather because most studies of ptarmigan has focused on aspects of ptarmigan biology that are less relevant in context of climate change, or because of a general bias among ornithologists to focus on aspects of climate change impacts (e.g. timing of migration) that are not that relevant for ptarmigan (but see Tape and Gustine 2014).

In our paper, we highlight aspects of the ecology of arctic and alpine ptarmigan that may render the birds vulnerable to climate change, which we propose should constitute the main focus in future research on these birds. Change in research focus may now be especially pressing as many species and populations of grouse have declined during the last decades, and some even close to extinction. Climate change has been forwarded as a potential cause of several of these declines (Thirgood et al. 2000, Wang et al. 2002, Ludwig et al. 2006, Storch 2007, Aldridge et al. 2008, Kausrud et al. 2008, Novoa et al. 2008, Lehikoinen et al. 2011, Revermann et al. 2012, Imperio et al. 2013), but empirical evidence remains missing. The tenet of our proposal is that climate sensitivity of ptarmigan is largely determined by a set of direct and indirect food web interactions that requires other approaches and emphasises than what has been mainstream in studies of songbirds and seabirds — the two taxa that predominate in the climate—ecological literature on birds (Møller et al. 2010). We start out with a short review of the ecological function of ptarmigan populations in alpine and arctic food webs. Next, we propose and discuss the most likely mechanisms by which ptarmigan are impacted by climate change. Finally, we propose how future research could be focussed to achieve a better understanding of climate impacts on ptarmigan populations.

Ptarmigan ecology in perspective of food web structure and dynamics

Ptarmigan are obligate herbivores and mainly year-round resident birds in alpine and arctic ecosystems, and are closely linked to sympatric herbivorous mammals (Ims and Fuglei 2005). In particular, ptarmigan belong to the same trophic guild as arctic rodents (voles and lemmings), hares Lepus spp. and reindeer Rangifer tarandus, in the sense that they share food plants, habitats and predators in most seasons. Hence, climate change impacts that involve either direct bottom—up or top—down trophic interactions may act similarly on the entire trophic guild, or that climate change may induce more complex indirect interactions between the guild members via apparent competition or mutualism (Abrams et al. 1998). Arctic and alpine food webs differ much, however, depending on biogeography and bio-climate (Ims et al. 2013a). High-arctic rock ptarmigan populations are embedded in very simple food webs with relatively few herbivores or trophic links (in particular islands such as Iceland, Svalbard and Franz Josef Land; Fig. 1a), whereas continental willow ptarmigan populations are generally placed in more complex food webs (e.g. the Varanger peninsula; Fig. 1b). Notice also that migratory populations of willow ptarmigan (Tape and Gustine 2014) may be placed in somewhat different food webs (low-arctic versus sub-arctic) in different seasons.

The geographically contrasting food web contexts of different ptarmigan populations is associated with patterns of contrasting population dynamics (Moss and Watson 2001). We propose that in food webs with profound trophic interaction cycles involving keystone mammal herbivores (sensu Ims and Fuglei 2005), ptarmigan population dynamics becomes entrained to the dominant interaction cycle. The prime example of this is the 3–5-year “northern cycles” (sensu Elton 1942) with voles and lemmings as the engine (Krebs 2011, 2013). The rodent cycle is a communitylevel process in boreal and arctic ecosystems that underlies the synchronous cyclic dynamics of small to medium-sized vertebrates, especially in Eurasia (Elton 1942, Hörnfeldt et al. 1986, Hansson and Henttonen 1988, Gauthier et al. 2004, Ims and Fuglei 2005, Gilg and Yoccoz 2010, Krebs 2011). The snowshoe hare Lepus americanus possesses an equivalent keystone role in boreal and sub-arctic ecosystems of North America, causing a 10-year cycle in many vertebrate species, including forest grouse and ptarmigan (Martin et al. 2001, Krebs et al. 2014). Hence, different ptarmigan populations tend to exhibit highly contrasting dynamics depending on the complexity of terrestrial food webs. Some ptarmigan populations are embedded in food webs with no keystone mammal herbivores that could drive such community-wide dynamics. A lack of competitors characterizes the endemic high-arctic Svalbard rock ptarmigan Lagopus muta hyperborea and rock ptarmigan populations in the European Alps (Fig. 1b). These ptarmigan populations usually occur at low densities (e.g. 3–5 pairs per km2 in Svalbard) and with relatively little temporal variability (Bossert 1995, Nopp-Mayr and Zohmann 2007, Zohmann and Wöss 2007, Pedersen et al. 2012). In contrast, sub- and low-arctic willow ptarmigan populations, embedded in more complex food webs with key-stone mammal herbivores and several different guilds of predators (Fig. 1a), usually exhibit highly violent and complex population dynamics (Lindén and Pedersen 1997, Moss and Watson 2001).

With regards to the key ecological factors that regulate ptarmigan populations, there has been highly conflicting views, and to some extent strong controversy (Moss and Watson 2001). Again, this ongoing debate may be attributed to the fact that ptarmigan populations are studied in very different food webs resulting from contrasting climate and management regimes. For instance, the most extensively studied Lagopus populations are found in the moorlands of northern England and Scotland, subjected to intensive ecosystem management directed towards the goal of maximizing production of red grouse Lagopus lagopus scotica. Strong control of predators is considered to be crucial for successful red grouse management, causing populations to reach such high densities (max 115 pairs km-2; Hudson and Rands 1988), where aggressive interactions during territoriality or high parasite loads act as strong population regulatory mechanisms (Mougeot et al. 2005). Hence, the case of the red grouse, and how it has been managed for centuries, is an implicit recognition of the often important role of predators as determinants of ptarmigan population dynamics (Fletcher et al. 2010).

Enemy — victim interactions: the importance of different predator guilds

Predation has also been highlighted as a key factor underlying the dynamics of ptarmigan populations in several other ecosystems (Moss and Watson 2001). However, the importance and outcome of the interaction between predators and ptarmigan is likely to be dependent on the complexity of the food web, and in particular, the structure and functioning of the predator guild. For instance, in the fairly simple terrestrial food web of Iceland, the 10-year population cycle of the rock ptarmigan is mainly driven by an interaction with its key specialist predator — the gyrfalcon Falco rusticolus (Nielsen 1999). The gyrfalcon acts on the ptarmigan population as a typical specialist predator both in terms of the numerical and functional response (Clum and Cade 1994, Booms and Fuller 2003). In contrast, ptarmigan populations in the low-arctic continents in both Eurasia and North America often find themselves in a more complex ecological setting with predator species belonging to three guilds (Fig. 1b) that may have significant impacts on different ptarmigan life stages. The gyrfalcon is present as a “ptarmigan specialist” (Tømmerås 1993), partly along with the golden eagle Aquila chrysaetos, which to some extent relies on adult ptarmigan as prey during the breeding season (Krebs et al. 2001, Nyström et al. 2006). The golden eagle also partly belongs to a guild of “generalist predators” that to a large degree subsist on ungulate carrion in winter (Killengreen et al. 2012, Henden et al. 2014). Other prominent members in the guild of generalists are raven Corvus corax, hooded crow Corvus cornix and red fox Vulpes vulpes, which are important ptarmigan predators, particularly on eggs and chicks (Erikstad et al. 1982, Parker 1984, Munkebye et al. 2003, Fletcher et al. 2010). The last predator guild of interest are “facultative rodent specialists” where small mustelids probably are the most important ptarmigan predators (Parker 1984). Specialist rodent predators, and to some extent those of the generalist predators that responds functionally and numerically to the cyclic rodent dynamics (Ims et al. 2013b), have been proposed to cause 3–5-year cycles in Fennoscandian willow ptarmigan through the “alternative prey mechanism” (Hagen 1952, Myrberget 1982, Moss and Watson 2001, Ims and Fuglei 2005).

Figure 1.

Ptarmigan in low-arctic and high-arctic food webs in Norway with contrasting complexities. Three functional groups of predators are distinguished. Only species or functional groups (directly or indirectly) linked to ptarmigan through trophic interactions (arrows) are included in the diagrams (modified from Ims et al. 2013c).

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Climate warming and changed enemy-victim interactions

Synchronized cycles of small rodents and willow ptarmigan were clear from time series data from Fennoscandia until the 1980s (Myrberget 1982, 1985, Steen et al. 1988) when the synchrony and cyclicity has become weaker and even vanished in many areas (Kausrud et al. 2008, Henden et al. 2011). The classical small rodent population cycle with high amplitude peak densities, has recently changed into non-cyclic low amplitude dynamics or a dynamic with longer periodicity in large parts of Fennoscandia (Holmstad et al. 2005, Ims et al. 2008, Kausrud et al. 2008) and elsewhere (Schmidt et al. 2012, Cornulier et al. 2013). Changes in small rodent population cycles have been attributed to increasing frequencies of freeze-melt events during winter (Korslund and Steen 2006). Accordingly, Kausrud et al. (2008) showed that willow ptarmigan populations rapidly declined and cyclicity was lost simultaneously with the sudden collapse of the small rodent cycle in an alpine region in southern Norway. Based on the alternative prey hypothesis, they attributed the decline of the willow ptarmigan to increased predation impact from specialist rodent predators (Fig. 1b) after the rodent population cycle collapse. However, Henden et al. (2011) could not find any effect of the different phases of the rodent cycle on temporal dynamics of willow ptarmigan in low-arctic northern Norway, where the rodent cycle has prevailed. That is, the decline rate of the ptarmigan population appeared to be unaffected by the increase, peak and crash phases of the rodent population (but see Kvasnes et al. 2014). Due to the strong trophic link between typical small rodent predators and their primary prey (Hanski et al. 1991) one would not expect such predators to exert a sustained negative impact on alternative prey (e.g. ptarmigan). Hence, as their main prey source of small rodents collapse, these predators would also decline to very low densities or even be extirpated as they have done in high-arctic Greenland (Schmidt et al. 2012). Hence, other factor(s) than those predators that usually act to cause synchronous dynamics of rodents and ptarmigan, are likely responsible for the long-term depression of ptarmigan population growth in this region.

There are reasons to suspect that increasing abundance of generalist predators may be acting on several ptarmigan populations in a negative way. Generalist predators such as foxes and corvids have increased in abundance worldwide in recent decades, expanding their distribution into arctic and alpine areas (Tapper 1992, Gregory and Marchant 1996, Tannerfeldt et al. 2002). Groundnesting species are particularly susceptible to predation by avian and mammalian predators, and negative impacts of predation have been documented for game birds and waterfowl (Marcström et al. 1988, Newton 1993, Fletcher et al. 2010, McKinnon et al. 2010). Recently, Fletcher et al. (2010) found that a large-scale reduction in abundance of carrion crow Corvus corone (−78%) and red fox (−43%) led to an average threefold increase in breeding success of red grouse, highlighting the potential high impact of such generalist predators. Moreover, there are indications that corvids may play a similar role in the decrease of sage grouse Centrocercus spp. in North America (Bui et al. 2010, Coates and Delehanty 2010). With a warmer climate, such predators may increase in tundra or alpine areas simply due to lower physiological demands at higher temperatures or even as a direct consequence of increased human activity or settlements in alpine and arctic regions (Hersteinsson and Macdonald 1992). More important in the case of northern Fennoscandia and North America, is increased availability of human-mediated subsidies or carcasses from large herbivores (Côté et al. 2004, Henden et al. 2014). In northern Fennoscandia, the availability of reindeer carcasses have increased due to changed management policies combined with more variable winters with ice-crust formation (Hausner et al. 2011, Killengreen et al. 2012), while in high-arctic Svalbard mortality rates of reindeer increase in winters with high frequency of “rain-on-snow” events (Stien et al. 2012, Hansen et al. 2013). Crows and red fox were recently able to establish and breed at the Yamal peninsula in the Russian arctic after a winter with catastrophic reindeer mortality due to an extreme rain-on-snow event (Sokolov et al. 2016). Generalist predators stabilise at high densities in response to high reindeer abundance, due to increased access to carcasses during the long and limiting winter period (Henden et al. 2014). This, in turn, is likely to promote strong and continuous predation pressure on ground nesting species in the summer (Fletcher et al. 2010, Ims et al. 2013b). Moreover, as many generalist predators are known to respond numerically and functionally to small rodents and other keystone herbivores (Ims et al. 2013b), changes in the dynamics of these keystone herbivores will likely be transferred to alternative prey species, such as ptarmigan. Recent changes in small rodent dynamics in Fennoscandia and elsewhere may therefore have resulted in additional and more continuous predation pressure on ptarmigan, as ptarmigan are increasingly deprived of predation-free years associated with small rodent peak years (Gilg and Yoccoz 2010). Thus, the fact that low-arctic ptarmigan populations are subjected to the simultaneous impacts of up to three guilds of predators (generalists, rodent specialists and ptarmigan specialists), with different numerical and functional responses as well as different responses to climate change, provides a scope for complex cumulative impacts on ptarmigan populations that cannot be ignored.

Compared to the complex impacts that may be implied by the functionally diverse predator community in lowand sub-arctic areas, predator impacts on high-arctic and high-alpine rock ptarmigan is likely to be simpler. For instance, in high-arctic Svalbard predation is mainly due to one terrestrial predator species — the arctic fox Vulpes lagopus (Fig. 1a). While the impact of arctic fox predation on the Svalbard rock ptarmigan is mostly unknown (but see Steen and Unander 1985), it has been proposed that, owing to the lack of lemming cycles, arctic fox predation rates on ground breeding birds is likely to be continuously high (Gilg and Yoccoz 2010). Still, temporal and spatial variability in predation rates on Svalbard rock ptarmigan may be caused by climate induced fluctuations in the abundance of alterative food sources for the arctic fox, such as reindeer carrion and breeding geese (Fuglei et al. 2003, Eide et al. 2012).

Camouflage is likely essential for ptarmigan as they live year-round in open areas where they are particularly vulnerable to predation. There is now evidence for an increasingly later onset of snow cover in autumn and an advanced spring with earlier snow melt in both arctic and alpine areas (cf. Ims et al. 2013a). Hence, a white plumage against bare ground represents a conspicuous contrast that could increase predation risk (Montgomerie et al. 2001, Mills et al. 2013). Considering that predation constitute the main form of adult mortality in most ptarmigan populations (Smith and Willebrand 1999, Martin 2001, Munkebye et al. 2003), the impact of a mismatch between moult and onset of winter snowfalls and spring snowmelt can be high. For instance, as autumn is the season when willow ptarmigan mortality is the highest due to natural predation (Smith and Willebrand 1999) and tend to coincide with the timing of snow fall (Sandercock et al. 2011), such mismatch in plumage coloration due to late snowfall could lead to a higher vulnerability in this part of the year. Ptarmigan can likely cope with potential mismatch, at least to a certain degree, with behavioral mechanisms such as plumage maintenance (Montgomerie et al. 2001), and by selective use of different microhabitats (Steen et al. 1992). However, as winter moult is mainly triggered by changes in the photoperiod (Höst 1942), it will be increasingly difficult for ptarmigan to forecast such changing and variable weather events precisely and consequently respond by behavioural mechanisms. The impact of mismatched plumage coloration on the dynamics of ptarmigan populations is likely to depend on food web structure and in particular on the relative abundance of different predator guilds (Fig. 1). It could be expected to be strongest in food webs with abundant predators that use mainly vision for detecting and pursuing prey; i.e. raptors like the golden eagle and the gyrfalcon. We are not aware of empirical studies that have targeted the issue of plumage coloration mismatch in boreal, alpine and arctic vertebrates beyond those on the snowshoe hare (Mills et al. 2013).

Climate change will likely also induce changed geographic distributions and changed dynamics of parasites and infectious diseases (Lioseau et al. 2012, Harvell et al. 2002, Kutz et al. 2005). Climate warming is expected to lead to expansion of the geographical northern range of parasites, it may modify the timing of parasite life cycles (Kutz et al. 2005) and thereby possibly enhancing transmission and outbreaks (Laaksonen et al. 2010, Loiseau et al. 2012). In particular, new pathogens and parasites arriving from the south may constitute a threat to Arctic and Alpine birds given that they constitute naïve hosts. Transmission, spread and infection by novel pathogens will, however, likely depend on the density of the host populations. Thus colonial species such as seabirds, may be more prone to outbreaks of parasites and diseases than low-density Arctic and Alpine ptarmigan.

Changed food web interactions involving plants

Increased interspecific competition due to facilitated growth of certain species is one of the main hypothesised consequences of climate change (Root and Schneider 2006, Hitch and Leberg 2007). Ptarmigan are herbivorous birds that share food plants with other herbivores, both in the high- and low-Arctic (Fig. 1), thus a potential for intra-guild competition is present. Three cases of increased abundances of competing herbivores may be of concern in the arctic: reindeer, arctic geese and forest insects.

Rock and white-tailed ptarmigan prefer rocky ridges, diversely structured slopes and boulders offering good viewpoints and shelter (Watson 1972, Marti and Bossert 1985, De Juana 1994) where they forage on sparse vegetation composed of dwarf shrubs and herbaceous plants (Savory 1989). In Fennoscandia, the transition zone between the heath and rocky ridges is heavily used by reindeer (Ims et al. 2007), especially when temperatures and insect harassment peak during summer. Consequently, increased competition between reindeer and rock ptarmigan for limited food resources as summer warming increases could potentially be a catalyst for negative impacts on ptarmigan numbers. In winter, competition could intensify when ice-crusts from ‘rain-on-snow’ events limit the available foraging habitats for both reindeer and rock ptarmigan. Ims et al. (2007) found a negative spatial association between the abundance of reindeer and rock ptarmigan in northern Norway, but were not able to pinpoint the underlying mechanism.

In the high-Arctic, intraguild competition from climate induced increases of pink-footed goose Anser brachyrhynchus is more important and a possible threat to the rock ptarmigan. For instance, in Svalbard the populations of pinkfooted geese has increased substantially over the last decades, with climate change suggested as one of the major drivers, especially in recent years (Madsen and Williams 2012). Hence, the impact of this rapidly increasing population of pink-footed geese on vegetation, which already is substantial, is a key concern (Madsen and Williams 2012). The necessary condition for competition to take place is that geese and ptarmigan overlap in habitat use, share food plants, and food availability is limited (Van Der Wal et al. 2000). The pink-footed goose share key food plants with the Svalbard rock ptarmigan (Unander et al. 1985, Fox and Bergersen 2005), and it is well known that intensive goose grazing and grubbing may reduce plant biomass, and cause habitat degradation (Speed et al. 2009). Currently these effects are most profound in wetland habitats that are relatively unimportant to the rock ptarmigan, but it is not known to what extent the two species will overlap in habitat use if the geese population continues to grow and/or have depleted their food plants in optimal goose habitats (Jensen et al. 2008). In the Canadian arctic, population declines in ptarmigan (Sandercock et al. 2005) have been attributed to expanding populations and severe habitat destruction impacts from snow geese Anser caerulescens, which substantiate the possibility that a similar situation may develop in Svalbard and elsewhere with increasing populations of geese.

Model-based projections of vegetation responses to climate change in boreal, arctic and alpine ecosystems yields positive plant growth effects (Xu et al. 2013), in particular of shrubs in tundra, which is now confirmed by many empirical observations (Myers-Smith et al. 2015). In turn, this may be expected to increase the habitats for shrub-dependent species like the willow ptarmigan. However, the most recent remote sensing based studies have shown surprising recent declines in the biomass in arctic tundra — so-called “tundra browning” (Epstein et al. 2015). In northernmost Fennoscandia, large tracts of sub-arctic birch forest, including the sensitive tundra—forest ecotone, have been transformed by outbreaks of temperature sensitive forest pest insects (Jepsen et al. 2012). These insect outbreaks have caused a vegetation state shift from dwarf shrubs to a community dominated by graminoids (Karlsen et al. 2013) and with a concurrent shift in the herbivore guild from a dominance of browsers to grazers (Jepsen et al. 2013). Outbreaks of shrub-defoliating insects have also been documented in arctic Greenland (Post and Pedersen 2008). Intensified outbreaks of forest insects, as climate warming intensifies, may constitute a rapid and large negative impact on low- and sub-arctic ptarmigan species, through removal of key food plants. It is important to note that such outbreaks often result from non-linear responses that are hard to predict (Hagen et al. 2008). On the other hand, model-based predictions from many alpine areas have shown that habitat availability is predicted to decline and become increasingly fragmented, especially in summer (Revermann et al. 2012, Jackson et al. 2015). Some studies have already shown elevational shifts in the distribution of Alpine ptarmigan populations leading to a considerable shrinkage in the distributional area (Revermann et al. 2012, Pernollet et al. 2015). Many Alpine populations are thus in danger of being pushed off the mountaintops as available habitat will be confined to increasingly fragmented mountain tops. Hence, Alpine ptarmigan may be especially vulnerable as the spatial climate gradient is much steeper and their distribution is more patchy leading to more fragmentation and edge effects.

Summer food availability has been suggested as a critical factor influencing grouse chick mortality (Ludwig et al. 2010). Ptarmigan might be affected through climate-induced temporal asymmetry between the availability of important food resources and ptarmigan reproduction, a phenomenon called trophic mismatch (cf. Post and Forchhammer 2008) and for which many bird studies have offered illustrative cases (Møller et al. 2010). Young rock and willow ptarmigan chicks typically consume large quantities of invertebrates (Ford et al. 1938, Spidsø 1980, Jørgensen and Schytte Blix 1985, Savory 1989) and newly emerged and highly nutritious reproductive plant parts (Dixon 1927, Choate 1963, Weeden 1969, Savory 1977, Spidsø 1980, Williams et al. 1980, Pullianen and Eskonen 1982) to meet growth and energetic demands. This highlights the potential of chicks to be particularly vulnerable to changes in the phenology of important food resources. A trophic mismatch would depend on the climate sensitivity of bird life-history events and/or food items that are particularly important. In general, graminoids and forbs show greater variability in reproductive phenology than shrubs (Molau et al. 2005). For instance, reproduction in the forb Bistorta vivipara (syn. Polygonum bistortum), known to be an important food item for ptarmigan (Unander et al. 1985), has been found to fail in the warmer parts of its distributional range (Doak and Morris 2010). On the other hand, Williams et al. (1980) found in a study from Alaska that willow ptarmigan chicks can alter food preferences in consecutive years. Thus, as willow and rock ptarmigan seem capable of switching between different food sources depending on their availability (Spidsø 1980, Williams et al. 1980), phenological mismatch may not constitute the most imminent threat to ptarmigan, at least in low-arctic habitats.

In contrast, in the high-Arctic, with its less diverse plant communities and limited access to above-ground macroinvertebrates, alternative food resources may be less available to ptarmigan chicks. Consequently, the Svalbard rock ptarmigan has a highly specialised diet during the early chick stage (Unander et al. 1985), where newly hatched chicks almost entirely feed on protein-rich bulbils of B. vivipara (Unander et al. 1985). Hence, this arctic endemic rock ptarmigan may be more prone to trophic mismatch than ptarmigan in the low-Arctic. Reported egglaying dates in Svalbard span a limited range, coinciding with ambient temperatures above freezing (Steen and Unander 1985). The phenotypic plasticity in time of egglying is likely to be limited by a genetically determined photoperiodic effect on gonadal development (Stokkan et al. 1986), which suggests that the high-arctic Svalbard rock ptarmigan may be vulnerable to rapid changes in climate that affect the phenology of its key food plants. With climate warming, soil temperature and soil nutrient availability likely increase in most habitats (Sjögersten et al. 2008). Hence, one might expect increased bulbil production. However, the amount of energy allocated to flower production rather than bulbil production has also been shown to increase with temperature along both altitudinal and latitudinal gradients (Bauert 1993, Fan and Yang 2009). Thus, climate warming may result in less bulbil production and higher seed production, with seeds available later in the growing season than bulbils, and thereby reducing food availability for chicks. The highly specialised diet of the Svalbard rock ptarmigan and the simplicity of the food web (Ims et al. 2013a, 2014) makes this ptarmigan species an interesting case for studying the possibility that arctic ptarmigan populations may be impacted by climate change though a trophic mismatch.

Direct climate effects: adverse effect of weather

Young chicks of ptarmigan are highly sensitive to adverse conditions, and survival of chicks through the first few weeks is a critical component of the demography in grouse and ptarmigan populations (Hannon and Martin 2006, Ludwig et al. 2006). Adverse weather conditions shortly after hatching has been shown to be detrimental for chick survival (Erikstad and Spidsø 1982, Erikstad and Andersen 1983, Steen and Unander 1985, Ludwig et al. 2006, Novoa et al. 2008, Kobayashi and Nakamura 2013). If climate change involves an increased frequency of extreme weather events such as heavy rain or drought during this critical life stage, it may represent a strong direct impact on arctic ptarmigan populations.

As ptarmigan are adapted to the harsh and cold environments of the arctic and high-alpine areas (Martin 2001, Martin and Wiebe 2004), increasing temperatures in spring and summer could be unfavourable. While several studies have found a positive effect of advanced snowmelt on ptarmigan reproductive success (Novoa et al. 2008, Imperio et al. 2013, García-González et al. 2016), some studies have indicated potential negative effects of increased temperatures during the summer season (Imperio et al. 2013). Revermann et al. (2012) found, in a study of rock ptarmigan in the Swiss Alps, that areas with lower temperatures and higher amounts of precipitation in July represented more suitable habitats. Hence, because of their adaptation to cold environments, ptarmigan might have temperature constraints with regard to their ability to dissipate body heat. According to the “heat dissipation hypothesis” (cf. Speakman and Król 2010), endothermic animals might be limited by their ability to dissipate body heat rather than by the competition for a limited energy supply. Hence, ptarmigan species may therefore be favoured by an early snowmelt, likely mediated by early plant growth and thereby foraging conditions before egglaying (Watson et al. 1998, Høye et al. 2007), but simultaneously negatively affected by high summer temperatures, mediated through hyperthermia, despite the potential increased resource availability in warmer years.

Perspectives for ptarmigan research in the age of rapid climate change

Human impacts on the planet, including anthropogenic climate change, affect arctic and alpine tundra ecosystem structure and functioning in unprecedented ways (Ims et al. 2013a). If we are to meet the challenge of conserving biodiversity and ecosystem integrity in a rapidly changing world, we must understand how species and communities and their food web interactions respond to novel conditions (Post et al. 2009a). In the Arctic and in alpine environments this is especially pressing, as the rate of warming in regions at high altitudes and latitudes has been much higher than the global average (Brunetti et al. 2009, Ims et al. 2013a), and consequently some of the largest ecological impacts of climate warming are documented in the Arctic (Post et al. 2009b). In this paper, we have shown that arctic and alpine ptarmigan potentially face a multitude of challenges that involves both direct and complex indirect bottom—up and top-down trophic interactions, mediated through changes in predation pressure, vegetation and competition from other herbivores. We have argued that the nature of these impacts will depend on the food web setting of the different ptarmigan populations because arctic and alpine food webs differ much, depending on biogeography and bio-climate. Hence, we suggest that ptarmigan research in light of climate change requires a food web approach, which currently lacks almost entirely in the mainstream studies of ptarmigan, but also generally in birds as noted by Møller et al. (2010). A food web approach has several advantages. Academically, it provides a structured framework for simultaneously assessing alternative hypothesis and the partial strength of multiple impacts. This approach is also management relevant. For instance, some detrimental food web interactions resulting from climate change (i.e. invasive predators—native prey interaction) can be subjected to management interventions. Moreover, knowing that low-density and/or declining ptarmigan populations are subjected to enhanced top—down control due to dampened populations cycles of key-stone mammal herbivores, is useful for devising sustainable harvesting strategies. This is because harvest mortality is likely to be additive under such circumstances.

Figure 2.

Conceptual ‘path’ models for the expected effects of climate and climate change on ptarmigan populations in the Low Arctic Varanger peninsula and High Arctic Svalbard. The two ‘climate-effect-chain’ models are taken from the ptarmigan module in the COAT monitoring science plan (Ims et al. 2013c, COAT Science Plan), depicting the most likely climate sensitive aspects for ptarmigan in each food web setting (Fig. 1), based on the current knowledge of the systems. Also highlighted is how management actions can be implemented to buffer unwarranted effects. Note that the COAT monitoring program consists of eight monitoring modules. Hence, in the ‘path’ models for ptarmigan, the Predictor targets and Indirect predictor targets represents Response targets in other modules.

f02_01.jpg

We advocate that ptarmigan researchers should team up with specialists on other taxa in order to adopt a food web approach to their research. A necessary and productive start is to outline the food web for the system under study, centred around the species in focus; e.g. as (cf. Krebs 2012) did for boreal snowshoe hare and arctic lemming in Canada, and as we have here done for ptarmigan at our two study sites in the Norwegian arctic (Fig. 1). A next step could then be to develop a conceptual model that specify the pathways for how climate is most likely to affect the focal ptarmigan populations. Figure 2 outlines such ‘climate impact path models’ for ptarmigan in the two food webs depicted in Fig. 1. These models were developed in collaboration with 20 colleagues within the Norwegian COAT initiative (Climate-ecological Observatory for Arctic Tundra; Ims et al. 2013c). The conceptual models reflect what our team assessed to be the most rapid and imminent threats to ptarmigan at the two sites. Specifically, for the low-Arctic food web on Varanger Peninsula an enhanced top-down impact from the functionally diverse community of predators, under a dampened small rodent cycle and increased abundance of carrion from reindeer, was assessed to be more important than any climate-induced changes in the plant community. In contrast, bottom—up impact from food plants was assessed to be important for the high-Arctic Svalbard food web through an increased potential for phonological mismatch and intensified competition with increasing populations of geese.

The developments of such conceptual models is beneficial in several respects (cf. Lindenmayer and Likens 2010). 1) It forces researchers to delimit the general scope of their future research based on the current knowledge of the system. 2) It demands that priorities are made on the most likely hypotheses among many possible. 3) It helps to highlight critical components and links in the food web that presently misses data essential for empirical testing or that require theoretical modelling for checking assumptions. 4) Simplified food web diagrams (Fig. 1) and conceptual climate impact models (Fig. 2) provides, in our experience, a very structured way to communicate knowledge and ideas among researchers and between researchers and managers. Concerning the last point, we believe that our approach can facilitate important comparative studies across the arctic and alpine biomes that can allow insights into how climate shapes the current dynamics and future fate of ptarmigan in a rapidly warming world.

Acknowledgements

We thank our colleagues in the COAT team for important input to the development of Fig. 1 and 2. COAT is financed by Research Council of Norway, Tromsø Research Foundation and the Fram Centre. This paper is a contribution from the SUSTAIN project.

References

  1. Aanes, S. et al. 2002. Sustainable harvesting strategies of willow ptarmigan in a fluctuating environment. — Ecol. Appl. 12: 281–290. Google Scholar

  2. Abrams, P. A. et al. 1998. Apparent competition or apparent mutualism? Shared predation when populations cycle. — Ecology 79: 201–212. Google Scholar

  3. Aldridge, C. L. et al. 2008. Range-wide patterns of greater sagegrouse persistence. — Divers. Distrib. 14: 983–994. Google Scholar

  4. Barth, J. B. 1877. Naturskildringer og optegnelser fra mit jæger- og reiseliv. — Cammermeyer, Kristiania, pp. 385. Google Scholar

  5. Bauert, M. R. 1993. Vivipary in Polygonum viviparum: an adaptation to cold climate? — N. J. Bot. 13: 473–480. Google Scholar

  6. Booms, T. L. and Fuller, M. R. 2003. Gyrfalcon diet in central west Greenland during the nesting period. — Condor 105: 528–537. Google Scholar

  7. Bossert, A. 1995. Bestandsentwicklung und Habitatnutzung des Alpenschneehuhns Lagopus mutus im Aletschgebiet (Schweizer Alpen). — Ornithol. Beobachter 92: 307–314. Google Scholar

  8. Brunetti, M. et al. 2009. Climate variability and change in the Greater Alpine Region over the last two centuries based on multi-variable analysis. — Int. J. Climatol. 29: 2197–2225. Google Scholar

  9. Bui, T. D. et al. 2010. Common raven activity in relation to land use in western Wyoming — implications for greater sage-grouse reproductive success. — Condor 112: 65–78. Google Scholar

  10. Choate, T. S. 1963. Habitat and population dynamics of white-tailed ptarmigan in Montana. — J. Wildl. Manage. 27: 684–699. Google Scholar

  11. Clum, N. J. and Cade, T. J. 1994. Gyrfalcon (Falco rusticolus). — In: Poole, A. and Gill, F. (eds), The birds of North America, No.114. The Academy of Natural Sciences, Philadelphia, PA, and The American Ornithologists' Union, Washington, DC. Google Scholar

  12. Coates, P. S. and Delehanty, D. J. 2010. Nest predation of greater sage grouse in relation to microhabitat factors and predators. — J. Wildl. Manage. 74: 240–248. Google Scholar

  13. Cornuher, T. et al. 2013. Europe-wide dampening of population cycles in keystone herbivores. — Science 340: 63–66. Google Scholar

  14. Côté, S. D. et al. 2004. Ecological impacts of deer overabundance. — Annu. Rev. Ecol. Evol. Syst. 35: 113–147. Google Scholar

  15. Crick, H. Q. P. 2004. The impact of climate change on birds. — Ibis 146: 48–56. Google Scholar

  16. De Juana, E. 1994. The rock ptarmigan. New world vultures to guineafowl. — In: Del Hoyo, J. et al. (eds), Handbook of the birds of the world, vol. 2. Lynx, p. 403. Google Scholar

  17. Dixon, J. S. 1927. Contribution to the life history of the Alaska willow ptarmigan. — Condor 29: 213–223. Google Scholar

  18. Doak, D. F. and Morris, W. F. 2010. Demographic compensation and tipping points in climate-induced range shifts. — Nature 467: 959–962. Google Scholar

  19. Eide, N. E. et al. 2012. Reproductive responses to spatial and temporal prey availability in a coastal Arctic fox population. — J. Anim. Ecol. 81: 640–648. Google Scholar

  20. Elton, C. S. 1942. Voles, mice and lemmings: problems in population dynamics. — Clarendon Press. Google Scholar

  21. Epstein, H. E. et al. 2015. Tundra greenness. — Arctic Report Card < www.arctic.noaa.gov/reportcard/tundra_greenness.html>. Google Scholar

  22. Erikstad, K. E. and Spidsø, T. K. 1982. The Influence of weather on food intake, insect prey selection and feeding behaviour in willow grouse chicks in northern Norway. — Ornis Scand. 13: 176–182. Google Scholar

  23. Erikstad, K. E. and Andersen, R. 1983. The effect of weather on food intake, insect prey selection and feeding time in different sized willow grouse broods. — Ornis Scand. 14: 249–252. Google Scholar

  24. Erikstad, K. E. et al. 1982. Territorial hooded crows as predators on willow ptarmigan nests. — J. Wildl. Manage. 46: 109–114. Google Scholar

  25. Fan, D. M. and Yang, Y. P. 2009. Altitudinal variations in flower and bulbil production of an alpine perennial, Polygonum viviparum L. (Polygonaceae). — Plant Biol. 11: 493–497. Google Scholar

  26. Fletcher, K. et al. 2010. Changes in breeding success and abundance of ground-nesting moorland birds in relation to the experimental deployment of legal predator control. — J. Appl. Ecol. 47: 263–272. Google Scholar

  27. Ford, J. et al. 1938. The food of partridge chicks (Perdix perdix) in Great Britain. — J. Anim. Ecol. 7: 251–265. Google Scholar

  28. Fox, A. D. and Bergersen, E. 2005. Lack of competition between barnacle geese Branta leucopsis and pink-footed geese Anser brachyrhynchus during the pre-breeding period in Svalbard. — J. Avian Biol. 36: 173–178. Google Scholar

  29. Fuglei, E. et al. 2003. Local variation in arctic fox abundance on Svalbard, Norway. — Polar Biol. 26: 93–98. Google Scholar

  30. García-González, R. et al. 2016. Influence of snowmelt timing on the diet quality of Pyrenean rock ptarmigan (Lagopus muta pyrenaica): implications for reproductive success. — PLoS ONE 11: e0148632. Google Scholar

  31. Gauthier, G. et al. 2004. Trophic interactions in a high arctic snow goose colony. — Integr. Compar. Biol. 44: 119–129. Google Scholar

  32. Gilg, O. and Yoccoz, N. G. 2010. Explaining bird migration. — Science 327: 959–959. Google Scholar

  33. Gregory, R. D. and Marchant, J. H. 1996. Population trends of jays, magpies, jackdaws and carrion crows in the United Kingdom. — Bird Study 43: 28–37. Google Scholar

  34. Gregory, R. D. et al. 2009. An indicator of the impact of climatic change on European bird populations. — PLoS ONE 4: e4678. Google Scholar

  35. Guillemain, M. et al. 2013. Effects of climate change on European ducks: what do we know and what do we need to know? — Wildl. Biol. 19: 404–419. Google Scholar

  36. Hagen, S. B. et al. 2008. Anisotropic patterned population synchrony in climatic gradients indicates nonlinear climatic forcing. — Proc. R. Soc. B 275: 1509–1515. Google Scholar

  37. Hagen, Y. 1952. Rovfuglene og viltpleien. — Gyldendal Norsk forlag, Oslo. Google Scholar

  38. Hannon, S. J. and Martin, K. 2006. Ecology of juvenile grouse during the transition to adulthood. — J. Zool. 269: 422–433. Google Scholar

  39. Hansen, B. B. et al. 2013. Climate events synchronize the dynamics of a resident vertebrate community in the High Arctic. — Science 339: 313–315. Google Scholar

  40. Hanski, I. et al. 1991. Specialist predators, generalist predators, and the Microtine rodent cycle. — J. Anim. Ecol. 60: 353–367. Google Scholar

  41. Hansson, L. and Henttonen, H. 1988. Rodent dynamics as community processes. — Trends Ecol. Evol. 3: 195–200. Google Scholar

  42. Harvell, C. D. et al. 2002. Climate warming and disease risks for terrestrial and marine biota. — Science 296: 2158–2162. Google Scholar

  43. Hausner, V. H. et al. 2011. The ghost of development past: the impact of economic security policies on Saami pastoral ecosystems. — Ecol. Soc. 16: 4. Google Scholar

  44. Henden, J.-A. et al. 2011. Declining willow ptarmigan populations: the role of habitat structure and community dynamics. — Basic Appl. Ecol. 12: 413–422. Google Scholar

  45. Henden, J.-A. et al. 2014. Community-wide mesocarnivore response to partial ungulate migration. — J. Appl. Ecol. 51: 1525–1533. Google Scholar

  46. Hersteinsson, P. and Macdonald, D. W. 1992. Interspecific competition and the geographical-distribution of red and arctic foxes Vulpes vulpes and Alopex lagopus. — Oikos 64: 505–515. Google Scholar

  47. Hitch, A. T. and Leberg, P. L. 2007. Breeding distributions of North American bird species moving north as a result of climate change. — Conserv. Biol. 21: 534–539. Google Scholar

  48. Holmstad, P. R. et al. 2005. Can parasites synchronise the population fluctuations of sympatric tetraonids? Examining some minimum conditions. — Oikos 109: 429–434. Google Scholar

  49. Hudson, P. J. and Rands, M. R. W. 1988. Ecology and management of gamebirds. — BSP Professional Books, Oxford, UK. Google Scholar

  50. Hörnfeldt, B. et al. 1986. Cycles in voles and small game in relation to variations in plant-production indexes in northern Sweden. — Oecologia 68: 496–502. Google Scholar

  51. Höst, P. 1942. Effect of light on the moults and sequences of plumage in the willow ptarmigan. — Auk 59: 388–403. Google Scholar

  52. Høye, T. T. et al. 2007. Rapid advancement of spring in the high arctic. — Curr. Biol. 17: R449–R451. Google Scholar

  53. Imperio, S. et al. 2013. Climate change and human disturbance can lead to local extinction of Alpine rock ptarmigan: new insight from the western Italian Alps. — PLoS ONE 8: e81598. Google Scholar

  54. Ims, R. A. and Fuglei, E. 2005. Trophic interaction cycles in tundra ecosystems and the impact of climate change. — BioScience 55: 311–322. Google Scholar

  55. Ims, R. A. et al. 2007. Can reindeer overabundance cause a trophic cascade? — Ecosystems 10: 607–622. Google Scholar

  56. Ims, R. A. et al. 2008. Collapsing population cycles. — Trends Ecol. Evol. 23: 79–86. Google Scholar

  57. Ims, R. A. et al. 2013a. Terrestrial ecosystems. — In: Meltofte, H. (ed.), Arctic biodiversity assessment. Status and trends in Arctic biodiversity. Conservation of Arctic Flora and Fauna, Akureyri. Google Scholar

  58. Ims, R. A. et al. 2013. Indirect food web interactions mediated by predator—rodent dynamics: relative roles of lemmings and voles. — Biol. Lett. 9: 1–4. Google Scholar

  59. Ims, R. A. et al. 2013c. Science plan for COAT: Climate-Ecological Observatory for Arctic Tundra. Fram Centre Report Series No. 1. < www.framsenteret.no/getfile.php/2435814.1574.xyxruwywpp/FinalPDF_COAT.pdf>. Google Scholar

  60. Ims, R. A. et al. 2014. An assessment of MOSJ — The state of the terrestrial environment in Svalbard. — Norw. Polar. Inst. Rep. Ser. 144: 1–44. Google Scholar

  61. Jackson, M. M. et al. 2015. Effects of climate change on habitat availability and configuration for an endemic coastal Alpine bird. — PloS ONE 10: e0142110. Google Scholar

  62. Jenouvrier, S. 2013. Impacts of climate change on avian populations. — Global Change Biol. 19: 2036–2057. Google Scholar

  63. Jensen, R. A. et al. 2008. Prediction of the distribution of Arcticnesting pink-footed geese under a warmer climate scenario. — Global Change Biol. 14: 1–10. Google Scholar

  64. Jepsen, J. U. et al. 2013. Ecosystem impacts of a range expanding eorest defoliator at the forest-tundra ecotone. — Ecosystems 16: 561–575. Google Scholar

  65. Jørgensen, E. and Schytte Blix, A. 1985. Effects of climate and nutrition on growth and survival of willow ptarmigan chicks. — Ornis Scand. 16: 99–107. Google Scholar

  66. Karlsen, S. R. et al. 2013. Outbreaks by canopy-feeding geometrid moth cause state-dependent shifts in understorey plant communities. — Oecologia 173: 859–870. Google Scholar

  67. Kausrud, K. L. et al. 2008. Linking climate change to lemming cycles. — Nature 456: 93–97. Google Scholar

  68. Killengreen, S. T. et al. 2012. How ecological neighbourhoods influence the structure of the scavenger guild in low arctic tundra. — Divers. Distrib. 18: 563–574. Google Scholar

  69. Kobayashi, A. and Nakamura, H. 2013. Chick and juvenile survival of Japanese rock ptarmigan Lagopus muta japonica. — Wildl. Biol. 19: 358–367. Google Scholar

  70. Korslund, L. and Steen, H. 2006. Small rodent winter survival: snow conditions limit access to food resources. — J. Anim. Ecol. 75: 156–166. Google Scholar

  71. Krebs, C. J. 2011. Of lemmings and snowshoe hares: the ecology of northern Canada. — Proc. R. Soc. B 278: 481–489. Google Scholar

  72. Krebs, C. J. 2012. Biodiversity monitoring in Canadas Yukon: the community ecological monitoring program. — In: Lindenmayer, D. (ed.), Biodiversity monitoring in Australia. CSIRO Press, pp. 151–156. Google Scholar

  73. Krebs, C. J. 2013. Population fluctuations in rodents. — Univ. of Chicago Press. Google Scholar

  74. Krebs, C. J. et al. 2001. Ecosystem dynamics of the boreal forest — The Kluane project. — Oxford Univ. Press. Google Scholar

  75. Krebs, C. J. et al. 2014. Trophic dynamics of the boreal forests of the Kluane Region. — Arctic (Suppl.) 67: 71–81. Google Scholar

  76. Kutz, S. J. et al. 2005. Global warming is changing the dynamics of Arctic host—parasite systems. — Proc. R. Soc. B 272: 2571–2576. Google Scholar

  77. Kvasnes, M. J. et al. 2014. Large-scale climate variability and rodent abundance modulates recruitment rates in willow ptarmigan (Lagopus lagopus). — J. Ornithol. 155: 891–903. Google Scholar

  78. Laaksonen, S. et al. 2010. Climate change promotes the emergence of serious disease outbreaks of Filarioid nematodes. — Ecohealth 7: 7–13. Google Scholar

  79. Lehikoinen, A. et al. 2011. The impact of climate and cyclic food abundance on the timing of breeding and brood size in four boreal owl species. — Oecologia 165: 349–355. Google Scholar

  80. Lindén, H. and Pedersen, H. C. 1997. Willow grouse, Lagopus lagopus. — In: Hagemeijer, W. J. M. and Blair, M. J. (eds), The EBCC atlas of European breeding birds: their distribution and abundance. T & AD Poyser, pp. 196–197. Google Scholar

  81. Lindenmayer, D. B. and Likens, G. E. 2010. Effective ecological monitoring. — Earthscan, London, UK. Google Scholar

  82. Loiseau, C. et al. 2012. First evidence and predictions of Plasmodium transmission in Alaskan bird populations. — PLoS ONE 7: e44729. Google Scholar

  83. Ludwig, G. X. et al. 2006. Short- and long-term population dynamical consequences of asymmetric climate change in black grouse. — Proc. R. Soc. B 273: 2009–2016. Google Scholar

  84. Ludwig, G. X. et al. 2010. Individual and environmental determinants of early brood survival in black grouse Tetrao tetrix. — Wildl. Biol. 16: 367–378. Google Scholar

  85. Madsen, J. and Williams, J. H. 2012. International species management plan for the Svalbard population of the pink-footed goose Anser brachyrhynchus. — AEWA Tech. Ser. No. 48. Bonn, Germany. Google Scholar

  86. Marcström, V. et al. 1988. The impact of predation on boreal tetraonids during vole cycles: an experimental study. — J. Anim. Ecol. 57: 859–872. Google Scholar

  87. Marti, C. and Bossert, A. 1985. Beobachtungen zur Sommeraktivität und Brutbiologie des Alpenschneehuhns (Lagopus mutus) im Aletschgebiet (Wallis). — Ornithol. Beob. 82: 153–168. Google Scholar

  88. Martin, K. 2001. Wildlife communities in alpine and sub-alpine habitats. — In: Johnson, D. H. and O'Neil, T. A, (eds), Wildlife — habitat relationships in Oregon and Washington. — Oregon State Univ. Press, pp. 285–310. Google Scholar

  89. Martin, K. and Wiebe, K. L. 2004. Coping mechanisms of Alpine and Arctic breeding birds: extreme weather and limitations to reproductive resilience. — Integr. Compar. Biol. 44: 177–185. Google Scholar

  90. Martin, K. et al. 2001. Forest grouse and ptarmigan. Chapter 11. — In: Krebs, C. J. et al. (eds), Ecosystem dynamics of the boreal forest: The Kluane Project. Oxford Univ. Press, pp. 240–260. Google Scholar

  91. McKinnon, L. et al. 2010. Lower predation risk for migratory birds at high latitudes. — Science 327: 326–327. Google Scholar

  92. Miller-Rushing, A. et al. 2010. Conservation consequences of climate change for birds. — In: Møller, A. P. et al. (eds,) Effects of climate change on birds: 295–309. Oxford Univ. Press, pp. 295–309. Google Scholar

  93. Mills, L. S. et al. 2013. Camouflage mismatch in seasonal coat color due to decreased snow duration. — Proc. Natl Acad. Sci. USA 110: 7360–7365. Google Scholar

  94. Molau, U. et al. 2005. Onset of flowering and climate variability in an alpine landscape: a 10-year study from Swedish Lapland. — Am. J. Bot. 92: 422–431. Google Scholar

  95. Montgomerie, R. et al. 2001. Dirty ptarmigan: behavioral modification of conspicuous male plumage. — Behav. Ecol. 12: 429–438. Google Scholar

  96. Moss, R. and Watson, A. 2001. Population cycles in birds of the grouse family (Tetraonidae). — Adv. Ecol. Res. 32 32: 53–111. Google Scholar

  97. Moss, R. et al. 2010. Trends in grouse research. — Wildl. Biol. 16: 1–11. Google Scholar

  98. Mougeot, F. et al. 2005. Interactions between population processes in a cyclic species: parasites reduce autumn territorial behaviour of male red grouse. — Oecologia 144: 289–298. Google Scholar

  99. Munkebye, E. et al. 2003. Predation of eggs and incubating females in willow ptarmigan Lagopus l. lagopus. — Fauna Norv. Ser. C 23: 1–8. Google Scholar

  100. Myers-Smith, I. H. et al. 2015. Climate sensitivity of shrub growth across the tundra biome. — Nat. Climate Change 5: 887–891. Google Scholar

  101. Myrberget, S. 1982. Fluctuations in Norwegian populations of willow grouse, Lagopus lagopus, 1932–1971 (in Norwegian, with English summary). — Medd. Norsk Viltforskning 3: 1–31. Google Scholar

  102. Myrberget, S. 1985. Egg predation on an island population of willow grouse Lagopus lagopus. — Fauna Norv. Ser. C 8: 82–87. Google Scholar

  103. Møller, A. P. et al. 2010. Effects of climate change on birds. — Oxford Univ. Press. Google Scholar

  104. Newton, I. 1993. Predation and limitation of bird numbers. — In: Power, D. M. (ed.), Current ornithology, vol. 11. Plenum Press, pp. 143–198. Google Scholar

  105. Nielsen, Ó. K. 1999. Gyrfalcon predation on ptarmigan: numerical and functional responses. — J. Anim. Ecol. 68: 1034–1050. Google Scholar

  106. Nopp-Mayr, U. and Zohmann, M. 2007. Spring densities and calling activities of rock ptarmigan (Lagopus muta helvetica) in the Austrian Alps. — J. Ornithol. 149: 135–139. Google Scholar

  107. Novoa, C. et al. 2008. Effect of weather on the reproductive rate of rock ptarmigan Lagopus muta in the eastern Pyrenees. — Ibis 150: 270–278. Google Scholar

  108. Nyström, J. et al. 2006. Golden eagles on the Swedish mountain tundra — diet and breeding success in relation to prey fluctuations. — Ornis Fenn. 83: 145–152. Google Scholar

  109. Parker, H. 1984. Effect of corvid removal on reproduction of willow ptarmigan and black grouse. — J. Wildl. Manage. 48: 1197–1205. Google Scholar

  110. Parmesan, C. 2006. Ecological and evolutionary responses to recent climate change. — Annu. Rev. Ecol. Syst. 37: 637–669. Google Scholar

  111. Parmesan, C. and Yohe, G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. — Nature 421: 37–42. Google Scholar

  112. Pedersen, Å. Ø. et al. 2012. Monitoring Svalbard rock ptarmigan: distance sampling and occupancy modeling. — J. Wildl. Manage. 76: 308–316. Google Scholar

  113. Pernollet, C. A. et al. 2015. Regional changes in the elevational distribution of the Alpine rock ptarmigan Lagopus muta helvetica in Switzerland. — Ibis 157: 823–836. Google Scholar

  114. Post, E. and Forchhammer, M. C. 2008. Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. — Phil. Trans. R. Soc. B 363: 2369–2375. Google Scholar

  115. Post, E. and Pedersen, C. 2008. Opposing plant community responses to warming with and without herbivores. — Proc. Natl Acad. Sci. USA 105: 12353–12358. Google Scholar

  116. Post, E. et al. 2009a. Global population dynamics and hot spots of response to climate change. — BioScience 59: 489–497. Google Scholar

  117. Post, E. et al. 2009b. Ecological dynamics across the Arctic associated with recent climate change. — Science 325: 1355–1358. Google Scholar

  118. Potapov, R. and Sale, R. 2013. Grouse of the World. — New Holland Publishers. Google Scholar

  119. Puihanen, E. and Eskonen, H. 1982. Chemical composition of plant matter eaten by young chicks of the willow grouse Lagopus lagopus in northern Finland. — Ornis Fenn. 59: 146–148. Google Scholar

  120. Revermann, R. et al. 2012. Habitat at the mountain tops: how long can rock ptarmigan (Lagopus muta helvetica) survive rapid climate change in the Swiss Alps? A multi-scale approach. — J. Ornithol. 153: 891–905. Google Scholar

  121. Root, T. L. and Schneider, H. 2006. Conservation and climate change: the challenges ahead. — Conserv. Biol. 20: 706–708. Google Scholar

  122. Sala, O. E. et al. 2000. Global biodiversity scenarios for the year 2100. — Science 287: 1770–1774. Google Scholar

  123. Sandercock, B. K. et al. 2005. Demographic consequences of agestructure in extreme environments: population models for arctic and alpine ptarmigan. — Oecologia 146: 13–24. Google Scholar

  124. Sandercock, B. K. et al. 2011. Is hunting mortality additive or compensatory to natural mortality? Effects of experimental harvest on the survival and cause-specific mortality of willow ptarmigan. — J. Anim. Ecol. 80: 244–258. Google Scholar

  125. Savory, C. J. 1977. The food of red grouse chicks Lagopus l. scoticus. — Ibis 119: 1–9. Google Scholar

  126. Savory, C. J. 1989. The importance of invertebrate food to chicks of gallinaceous species. — Proc. Nutr. Soc. 48: 113–133. Google Scholar

  127. Schmidt, N. M. et al. 2012. Response of an arctic predator guild to collapsing lemming cycles. — Proc. R. Soc. B 279: 4417–4422. Google Scholar

  128. Sjögersten, S. et al. 2008. Habitat type determines herbivory controls over CO9 fluxes in a warmer Arctic. — Ecology 89: 2103–2116. Google Scholar

  129. Smith, A. and Willebrand, T. 1999. Mortality causes and survival rates of hunted and unhunted willow grouse. — J. Wildl. Manage. 63: 722–730. Google Scholar

  130. Sokolov, A. A. et al. 2016. Emergent rainy winter warm spells may promote boreal predator expansion into the Arctic. — Arctic 69: 121–129. Google Scholar

  131. Speakman, J. R. and Król, E. 2010. Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. — J. Anim. Ecol. 79: 726–746. Google Scholar

  132. Speed, J. D. M. et al. 2009. Predicting habitat utilization and extent of ecosystem disturbance by an increasing herbivore population. — Ecosystems 12: 349–359. Google Scholar

  133. Spidsø, T. K. 1980. Food selection by willow grouse Lagopus lagopus chicks in northern Norway. — Ornis Scand. 11: 99–105. Google Scholar

  134. Steen, J. and Unander, S. 1985. Breeding biology of the Svalbard rock ptarmigan Lagopus mutus hyperboreus. — Ornis Scand. 16: 191–197. Google Scholar

  135. Steen, J. B. et al. 1988. Microtine density and weather as predictors of chick production in willow ptarmigan, Lagopus l. lagopus. — Oikos 51: 367–373. Google Scholar

  136. Steen, J. B. et al. 1992. Cryptic behaviour in moulting hen willow ptarmigan Lagopus l. lagopus during snow melt. — Ornis Scand. 23: 101–104. Google Scholar

  137. Stien, A. et al. 2012. Congruent responses to weather variability in high arctic herbivores. — Biol. Lett. 8: 1002–1005. Google Scholar

  138. Stokkan, K. A. et al. 1986. The annual breeding cycle of the high-arctic Svalbard ptarmigan (Lagopus mutus hyperboreus). — Gen. Compar. Endocrinol. 61: 446–451. Google Scholar

  139. Storch, I. 2007. Grouse status survey and conservation action plan 2006–2010. — WPA/BirdLife/SSC Grouse Specialist Group. IUCN, Gland and World Pheasant Ass. Fordingbridge, UK, pp. 112. Google Scholar

  140. Tannerfeldt, M. et al. 2002. Exclusion by interference competition? The relationship between red and arctic foxes. — Oecologia 132: 213–220. Google Scholar

  141. Tape, K. D. and Gustine, D. D. 2014. Capturing migration phenology of terrestrial wildlife using camera traps. — BioScience 64: 117–124. Google Scholar

  142. Tapper, S. C. 1992. Game heritage: an ecological review from shooting and gamekeeping records. — Game Conservancy, Fordingbridge, UK. Google Scholar

  143. Thirgood, S. J. et al. 2000. Habitat loss and raptor predation: disentangling long- and short-term causes of red grouse declines. — Proc. R. Soc. B 267: 651–656. Google Scholar

  144. Tømmerås, P. J. 1993. The status of gyrfalcon Falco rusticolus research in northern Fennoscandia 1992. — Fauna Norv. Ser. C 16: 75–82. Google Scholar

  145. Unander, S. et al. 1985. Crop content of the Svalbard rock ptarmigan (Lagopus mutus hyperboreus). — Polar Res. 3: 239–243. Google Scholar

  146. Van Der Wal, R. et al. 2000. Effects of resource competition and herbivory on plant performance along a natural productivity gradient. — J. Ecol. 88: 317–330. Google Scholar

  147. Wang, G. et al. 2002. Relationships between climate and population dynamics of white-tailed ptarmigan Lagopus leucurus in Rocky Mountain National Park, Colorado, USA. — Climate Res. 23: 81–87. Google Scholar

  148. Watson, A. 1972. The behaviour of ptarmigan. — Br. Birds 65: 6–26. Google Scholar

  149. Watson, A. et al. 1998. Population dynamics of Scottish rock ptarmigan cycles. — Ecology 79: 1174–1192. Google Scholar

  150. Weeden, R. B. 1969. Foods of rock and willow ptarmigan in central Alaska with comments on interspecific competition. — Auk 86: 271–281. Google Scholar

  151. Williams, J. B. et al. 1980. Foraging ecology of ptarmigan at Meade River, Alaska. — Auk 92: 341–351. Google Scholar

  152. Xu, L. et al. 2013. Temperature and vegetation seasonality diminishment over northern lands. — Nat. Climate Change 3: 581–586. Google Scholar

  153. Zohmann, M. and Wöss, M. 2007. Spring density and summer habitat use of alpine rock ptarmigan Lagopus muta helvetica in the southeastern Alps. — Eur. J. Wildl. Res. 54: 379–383. Google Scholar

© 2016 The Authors. This is an Open Access article This work is licensed under a Creative Commons Attribution 4.0 International License (CC-BY). The license permits use, distribution and reproduction in any medium, provided the original work is properly cited.
John-André Henden, Rolf Anker Ims, Eva Fuglei, and Åshild Ønvik Pedersen "Changed Arctic-alpine food web interactions under rapid climate warming: implication for ptarmigan research," Wildlife Biology 2017(SP1), (5 June 2017). https://doi.org/10.2981/wlb.00240
Accepted: 4 June 2016; Published: 5 June 2017
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