The Little Auk Alle alle: an ecological indicator of a changing Arctic and a model organism

Abstract

The Little Auk Alle alle is a small planktivorous auk breeding colonially in the High Arctic. Owing to its large population size and bi-environmental lifestyle, resulting in the large-scale transport of matter from sea to land, the Little Auk is one of the most important components of the marine and terrestrial ecosystems in the Arctic. As a result of globalization, which facilitates access to remote areas of the Earth, a growing number of studies is being dedicated to this endemic Arctic seabird. Research has focussed primarily on the importance of the Little Auk as an ecological indicator reacting to the climatic and oceanological changes that are particularly evident in the Arctic as a result of Arctic amplification (warming is more rapid in the Arctic than in any other region on Earth). Importantly, the species is also used as a model to investigate matter and energy flow through the ecosystem, mate choice, parental care and biological rhythms. Here, we review the natural history of the Little Auk, highlighting studies with the potential to provide answers to universal questions regarding the response of seabirds to climate variability and avian reproductive behaviour, e.g. threshold of foraging flexibility in response to environmental variability, carry-over effects between the breeding and non-breeding periods, the reasons for the transition from bi- to uni-parental care, parental coordination mechanisms.

Introduction

The Arctic is a unique region on Earth, characterized as it is by a lower biodiversity and less complex food webs compared to those encountered at lower latitudes (Gauthier et al. 2011; Legagneux et al. 2012). Such a system offers an excellent platform for various studies on behavioural and evolutionary ecology that would be hard to perform in more complex environments. It serves as a natural laboratory where one can carry out experiments under fairly controllable circumstances. The uniqueness of the Arctic is also highlighted in the context of ongoing climate changes, as this region is disproportionally affected by climate warming, a phenomenon known as Arctic amplification (Serreze and Barry 2011; Zonn et al. 2017; IPCC 2019). This is bringing about major changes to ecosystem productivity and species distributions (Holland et al. 2001; Steinacher et al. 2009; IPCC 2019), to which endemic species, adapted to harsh Arctic conditions, are particularly susceptible. Such species are therefore often excellent models for monitoring the condition and health of this polar environment.

The Little Auk or Dovekie Alle alle (Fig. 1) is one such endemic Arctic species. It is a small planktivorous auk, one of the most numerous seabirds of the Palearctic. The Little Auk breeds colonially amongst rock crevices on mountain slopes, exclusively within the seacoast zone of the High Arctic (Stempniewicz 2001). Taxonomically, it is unique in its genus but belongs to the Alcini tribe, together with Brünnich’s Guillemot Uria lomvia, Common Guillemot Uria aalge, Razorbill Alca torda and the extinct Great Auk Pinguinus impennis (Smith and Clarke 2015). The Little Auk’s abundance [> 37 million pairs worldwide (Wojczulanis-Jakubas et al. 2011b; Keslinka et al. 2019)] and position in the trophic network—being the only exclusively zooplanktivorous seabird in the Atlantic sector of the Arctic, it is an important consumer of zooplankton in this region—means that it plays a major ecological role in the Arctic marine ecosystem. For this reason, the Little Auk has been selected for the monitoring of Arctic seabird species by the Conservation of Arctic Flora and Fauna Working Group of the Arctic Council as part of the Circumpolar Biodiversity Monitoring Programme (Irons et al. 2015). Foraging at sea and nesting on land, the Little Auk also plays an important part in transporting organic matter from the marine ecosystem to the nutrient-poor Arctic tundra (Stempniewicz et al. 2007; González-Bergonzoni et al. 2017; Mosbech et al. 2018). This fertilization not only enriches the terrestrial part of the ecosystem, enhancing vegetation and invertebrate communities around Little Auk colonies (Zmudczyńska et al. 2012; Zwolicki et al. 2016a); it also attracts a variety of vertebrates that consume the lush vegetation (Jakubas et al. 2008b; Wojczulanis-Jakubas et al. 2008; Mosbech et al. 2018). From the human perspective, the Little Auk in the Qaanaaq region (Thule, NW Greenland) added resilience to human societies in times when marine mammals were difficult to access because of sea ice conditions and/or after the relevant hunting techniques had been forgotten (Mosbech et al. 2018). Traditional kiviaq is made from whole Little Auk bodies sewn in sealskin bags that ferment for several months (Mosbech et al. 2018).

Fig. 1

Breeding cycle of the Little Auk (from left to right and top to bottom): copulation/mating (photo Tomasz Kasiak), egg in the nest chamber/incubation, an adult feeding the chick/chick rearing and a group of adults in the colony (photo Cornelius Nelo)

In the context of the breeding range, population size, diet and its importance for the High Arctic ecosystem, the Little Auk is an excellent model species for studying the response of endemic High Arctic organisms to ongoing climatic and anthropogenic changes, and may act as an ecological indicator of global changes, particularly well-pronounced in the Arctic. Being a seabird, with a high annual adult survival, social and genetic monogamy, bi-parental care and a single-egg clutch (Stempniewicz 2001; Wojczulanis-Jakubas et al. 2009a), the Little Auk also constitutes a perfect model species for studying behavioural and evolutionary ecology, whenever such a system refers to birds with similar characteristics and/or life strategies.

Given the importance of the Little Auk for the functioning of the Arctic ecosystem, as well as the growing interest in polar research, we review here studies on the Little Auk’s ecology, stressing their contributions to ecology and beyond. We also point out recent progress and as yet unfulfilled potential for studies focussing on this species and discuss its advantages and disadvantages as an ecological indicator and a model species.

Materials and methods

We searched the Scopus database for documents (type “article” or “review”) using the expressions “little Auk”, “dovekie”, “Alle alle” or “Plautus alle” in the title, abstract or keywords (accessed 01.11.2021). We found a total of 281 papers published from 1921 to 2021. We chose studies, the results of which illustrate the role of the Little Auk as an indicator and/or model species, and summarized them in order to highlight the most important features of the species and to provide examples of its usefulness in various types of research. To compare the number of documents about another “iconic” or “charismatic” Arctic species, the Polar Bear Ursus maritimus, we also searched the Scopus database for documents (type “article” or “review”) using the expressions “polar bear” or “Ursus maritimus” in the title, abstract, or keywords (accessed 01.11.2021). Here, we found 1789 documents published between 1917 and 2022.

Results and discussion

Being a small pelagic seabird, and breeding in remote Arctic archipelagos (i.e. difficult to access), the Little Auk has long been neglected as a study species. However, rapid globalization and human expansion into the polar regions, as well as the development and miniaturization of various tracking technologies, have greatly reduced the challenge associated with the study of the Little Auk’s ecology. The number of documents found in the Scopus database has increased considerably in the last decade (20 in 1921–1989, 38 in 1990–1999, 63 in 2000–2009, 142 in 2010–2019 and 18 in 2020–2021). Obviously, that is far less than what is available for the iconic Polar Bear (184 in 1917–1989, 225 in 1990–1999, 436 in 2000–2009, 793 in 2010–2019 and 151 in 2020–2022). Nonetheless, the Little Auk has recently received much well-deserved research attention, indicating its usefulness as an ecological indicator and model species.

The Little Auk: key life-history facts

A numerous and exclusively High Arctic breeder

The breeding range of the Little Auk is circumpolar and limited to High Arctic archipelagos, with the largest colonies extending between 70° and 80°N. The breeding population is very hard to estimate because of its habit of nesting in rock crevices in mountain scree. The world population is estimated at 37–40 million pairs (Wojczulanis-Jakubas et al. 2011b; Keslinka et al. 2019), with the largest breeding aggregations in Greenland and on Spitsbergen (Fig. 2). The present abundance of Little Auks is assumed to be the effect of the extermination of the Greenland Whale Balaena mysticetus in Spitsbergen in the seventeenth century, which released a vast amount of zooplankton that would be otherwise have been consumed by those Arctic whales (Wȩsławski et al. 2000).

Fig. 2

(mean for July 2003–2017; source: Moderate-resolution Imaging Spectroradiometer (MODIS) Aqua satellite data from Ocean Color Data webpage, https://oceandata.sci.gsfc.nasa.gov/MODIS-Aqua) and sea ice distribution [July 2009 as an example; source: Multisensor Analysed Sea Ice Extent—Northern Hemisphere (MASIE-NH), Version 1 with 4 km grid cell size (National Ice Center (NIC) and NSIDC 2010)]. Location of Arctic zones according to (CAVM Team 2003). Little Auk population estimates after Keslinka et al. (2019)

Breeding distribution of the Little Auk (colonies indicated by red dots) with sea surface temperature

Wintering quarters have only recently been identified, following the deployment of miniaturized light-based loggers. Results so far indicate that the wintering areas are to some extent specific to particular breeding colonies, but overall are situated in the NW Atlantic, off Newfoundland and SW Greenland, and in the Norwegian and North Seas (Fort et al. 2013; Dufour et al. 2021; SEATRACK project website http://seatrack.seapop.no/map/).

Despite breeding under continuous daylight conditions at high latitudes, the Little Auk at the population level exhibits a daily rhythm of activity in the colony, although particular individuals may become arrhythmic with regard to the 24-h cycle (Stempniewicz 1986; Wojczulanis-Jakubas et al. 2020b).

Morphological variation

This exists across the worldwide geographical range of the Little Auk (Fig. 2), with a longitudinal increase in body size from west to east. The smallest birds breed in the western part of the population range (Greenland and Jan Mayen), medium-sized individuals in Svalbard and the largest birds (the subspecies A. a. polaris) in the eastern part of the study area, i.e. Franz Josef Land. The trend is negatively correlated with air temperature during the summer; whilst this may be adaptive, more studies are needed in order to draw definitive conclusions (Wojczulanis-Jakubas et al. 2011b).

Weak genetic population differentiation

Based on the model of isolation by distance, such differentiation has been documented for the Little Auk (Wojczulanis-Jakubas et al. 2014c). Even the two morphologically different Little Auk subspecies are quite similar with respect to both mitochondrial DNA and microsatellite loci (Wojczulanis-Jakubas et al. 2015b). The genetic similarity of the breeding populations across the whole range, including both subspecies, is likely to be an effect of strong gene flow between populations, which may well be facilitated by the overlapping wintering areas of the various breeding populations (SEATRACK project website http://seatrack.seapop.no/map/).

Metabolic rate of the Little Auk

Corrected for body size, it is the highest of all seabirds studied (Gabrielsen et al. 1991). This is due to the wing-propelled locomotion during diving, and the combination of flapping flight, high wing-loading and long foraging distances (Stempniewicz 1982; Gabrielsen et al. 1991; Konarzewski et al. 1993; Jakubas et al. 2013).

The only exclusively zooplanktivorous seabird in the North Atlantic

During the breeding season, adult Little Auks supply their chick with energy-rich copepods associated with cold water masses from the genus Calanus, especially C. glacialis and C. hyperboreus. Little Auks from colonies that are situated at a cost-effective distance from the marginal ice zone may also forage on the sympagic amphipod Apherusa glacilis (Karnovsky et al. 2010; Kwasniewski et al. 2010; Jakubas et al. 2011; Frandsen et al. 2014; Møller et al. 2018). Adults use the sublingual sack, also called the gular pouch, to deliver food to the chick (Fig. 1; useful for identifying dietary components as the prey items are still fresh). Whilst foraging under water, Little Auks capture copepods by visually guided suction feeding, achieved through an extension of their gular pouch (Enstipp et al. 2018). Thus, the highest densities of foraging Little Auks in the vicinity of one of the largest breeding aggregations in Svalbard were observed in areas with abundant C. glacialis and high water transparency (Stempniewicz et al. 2013, 2021). The maximum depth (mean ± SD) recorded during foraging dives by Little Auks from colonies on Spitsbergen and on Greenland was 9.9 ± 6.9 m, whilst the maximum depth attained by any bird was 37.8 m (Karnovsky et al. 2011). The diet of adults is less well known, but the similar δ¹⁵N isotopic values in chick and adult blood samples strongly suggest that adult and young Little Auks feed on similar prey (Fort et al. 2010). The diet of the Little Auk during the non-breeding period is not known for certain, but existing studies indicate that it probably consists mostly of krill, amphipods and small fish (Rosing-Asvid et al. 2013).

The Little Auk as an ecological indicator of global changes

Indicator of environmental changes

The Arctic is undergoing dramatic climate changes, recently called Arctic borealization (Box et al. 2019) or Atlantification, which are transforming this unique polar ecosystem in certain areas of the Arctic into an average North Atlantic ecosystem (Csapó et al. 2021; Descamps and Strøm 2021). This is affecting a great many marine and terrestrial organisms adapted to the conditions hitherto specific to polar regions (Wassmann et al. 2011; Descamps et al. 2017). There is thus an urgent need for research on the fate of species emblematic of the Arctic. In the light of the fact that its breeding range is restricted to the High Arctic, its food preferences during the breeding period (energy rich zooplankton associated with cold water masses) and high energy requirements, the Little Auk is regularly studied in the context of avian responses to environmental variability. Some Little Auk responses to environmental variability serve as ‘footprints’ of climate change [sensu (Wassmann et al. 2011), i.e. referring to documented changes in the range, community structure, abundance, phenology, behaviour, growth or condition of marine organisms in the Arctic consistent with or apparently in response to current climate change]. The footprints documented for Little Auks include changes in dietary composition, reproductive output, adult survival and phenology; they are summarized below.

A multiyear (2001–2008) study on oceanographic conditions and the zooplankton community in the foraging area of Little Auks from a colony on Spitsbergen has demonstrated that food quality and quantity varies greatly amongst years, but within a range that still allows parental birds to provide chicks with lipid-rich Arctic copepods (Kwasniewski et al. 2012). To some extent, Little Auks are capable of buffering suboptimal environmental and food conditions. Even where and when the preferred Arctic zooplankton is less abundant, they have been able to breed successfully with no negative consequences on chick survival, stress levels, or the body masses of adults and chicks (Kwasniewski et al. 2010; Jakubas et al. 2011, 2017; Grémillet et al. 2012). However, some studies have reported serious consequences of suboptimal foraging conditions—a slower chick growth rate (Jakubas et al. 2013, 2020; Kidawa et al. 2015), a decrease in interannual survival rates of adult Little Auks (Hovinen et al. 2014a) with a potentially strong effect on population dynamics and viability in such a long-lived species (Sæther and Bakke 2000). It has been found that interannual changes in sea ice phenology and primary productivity pulses (affecting the transfer of biomass and energy through Arctic food webs) in Svalbard affected the breeding performance of Little Auks: chick survival decreased with the increasing time lag between the annual peaks of sea ice extent and primary production (Ramírez et al. 2017). In the E Greenland population, adult body condition and chick growth rate were negatively linked to sea ice concentration and mercury contamination (Amélineau et al. 2019). All these factors indicate that despite the apparent flexibility of Little Auks as regards foraging (Jakubas et al. 2011, 2017; Grémillet et al. 2012; Amélineau et al. 2016b), deteriorating oceanographic conditions pose a threat to the population of this abundant endemic Arctic seabird. Little Auk populations from Iceland and S Greenland, breeding at the species’ southernmost range margin, collapsed following the nineteenth century shift in sea currents and plankton dispersal and harvest (Stempniewicz 2001; Jakubas et al. 2022). Models of future foraging habitat suitability assuming scenarios of 1 °C and 2 °C SST increases and the lack of sea ice, have predicted losses of suitable foraging habitat for the majority of Little Auk colonies in Svalbard (Jakubas et al. 2017). Thus, over longer time scales, the negative consequences of global warming on the Little Auk population appear inevitable.

Little Auks have also been reported to react to changes in air temperature in terrestrial ecosystems. For a colony on Spitsbergen, the median hatching date became 4.5 days earlier over 1963–2008 in response to the increase in spring air temperatures (0.9 °C per decade). Little Auks occupy nest chambers within the rock debris as soon as the snow cover has melted sufficiently to allow access to them. Therefore, the timing of egg-laying appears to be strongly determined by air temperature affecting snow melt in the colony (Moe et al. 2009).

Indicator of environmental contamination

The Little Auk may also serve as a good model for studying the bioaccumulation and biomagnification of toxic elements (e.g. mercury, Hg). Being a top predator in the marine Arctic environment, the Little Auk can be a true sentinel of anthropogenic influence in this region. It moults twice a year, with different feather types being grown at different times of the year and locations (breeding/non-breeding grounds), which allows investigation of the exposure of Little Auks to elements throughout the annual cycle (Fort et al. 2013). Recent studies have revealed spatial and temporal variations in Hg concentrations in Little Auks, indicating greater exposure during the non-breeding period in the wintering areas than during the breeding season (Renedo et al. 2020; Pacyna-Kuchta et al. 2020; Albert et al. 2021). Although for now, overall Hg concentrations in Little Auks are relatively low compared to other Arctic seabirds (Albert et al. 2021), females with high Hg levels tend to lay smaller eggs (Fort et al. 2014). It remains to be explored whether smaller eggs are related to poorer breeding success, or whether there are other negative consequences of Hg contamination, but the few existing studies clearly show that even species living in supposedly pristine environments, such as the Little Auk, are not free of contaminants. Recent studies have revealed microplastics in Little Auks (Amélineau et al. 2016a; Avery-Gomm et al. 2016); although overall the number and mass of plastics ingested was small, these may be increasing. Arctic seabirds thus continue to face threats from a rapidly changing marine environment (Fife et al. 2015; Avery-Gomm et al. 2016).

Population size monitoring

Because of the difficulties in estimating the population size of this species, breeding as it does in large aggregations in remote areas on stony slopes, the few reliable counts of local population size are based on indirect methods (aerial images of a colony, extrapolation of densities from small patches of a colony, the proportion of resightings of marked birds in a study plot followed by comparisons with the number of unmarked birds observed in the plot) (Evans 1981; Stempniewicz 1981; Isaksen and Bakken 1995; Kampp et al. 2000; Mosbech et al. 2017; Keslinka et al. 2019). Since Little Auks are vulnerable to the consequences of climate warming, not to mention additional threats from oil-drilling activities in the sub-Arctic and Arctic zone, the expansion of shipping routes and the long-distance transport of contaminants (Fort et al. 2013), monitoring of the Little Auk’s population trends has been recommended by the Conservation of Arctic Flora and Fauna and Protection of the Arctic Marine Environment working group of the Arctic Council (Irons et al. 2015). Establishing integrated monitoring programmes of Little Auks, amongst the most numerous High Arctic seabirds, is crucial in order to support adaptive management in the rapidly changing High Arctic environment.

The Little Auk as a model species in ecological studies

Mate choice

Given its modest ornamentation and negligible sexual dimorphism (Jakubas and Wojczulanis 2007), the Little Auk may not be a prime species for studying mate choice as regards sexually selected traits. However, male and female Little Auks do differ in a few traits (morphological, biometrical, hormonal and behavioural), and that makes the species an interesting model for examining the question of mate choice. This is especially relevant in the context of other Little Auk characteristics, like genetic monogamy (Wojczulanis-Jakubas et al. 2009a), high partner fidelity (Wojczulanis-Jakubas et al. 2020a) and extensive, coordinated parental care (Harding et al. 2004; Wojczulanis-Jakubas et al. 2018a); these are all closely related to the choice of breeding partner. An assortative mating pattern has been found in the Little Auk in both fixed and labile traits. Assortative mating with respect to wing length may be a reflection of their migration patterns. As migration distance can be heritable, a positive correlation between pair members with regard to such a trait could prevent the production of offspring that would have a non-adaptive mixture of migration distance programmes resulting in an unclear migration area (Wojczulanis-Jakubas et al. 2018b). The significant and positive correlation between pair members that has been reported in hormonal stress response may also be adaptive. If conditions in foraging areas are unfavourable, both parents need to increase their efforts in a coordinated manner to ensure that a given breeding attempt is successful (Wojczulanis-Jakubas et al. 2018b).

Parental care

The long and extensive bi-parental care (1 month of incubation + 1 month of chick rearing, possibly post-fledging care), required to raise the single chick successfully (Stempniewicz 2001), creates an excellent reproductive system in which to examine the cause and effect of sexual differences in parental efforts (Wojczulanis et al. 2006; Wojczulanis-Jakubas et al. 2012, 2014a, 2015a). This topic has long been explored with regard to sexual conflict, including some Little Auk studies, e.g. (Wojczulanis-Jakubas et al. 2012). Currently, parental care is being intensively studied in the context of cooperation between the breeding partners (Griffith 2019; Wojczulanis-Jakubas 2021), where the Little Auk has been found to be a particularly useful model species (Wojczulanis-Jakubas et al. 2018a). Recent results have demonstrated that Little Auk parents not only both provide food for their chick at an equal rate, but also coordinate their foraging trips so as to minimize the time between feedings (Wojczulanis-Jakubas et al. 2018a; Grissot et al. 2019).

Despite the similar contributions made by male and female Little Auks to parental care for most of the breeding season, it is the males that take over all parental duties at the end of the nesting period, when females desert the colony (Harding et al. 2004; Wojczulanis-Jakubas and Jakubas 2012). As paternal care resulting from brood desertion by the female is rather unusual in monogamous birds [if only one sex deserts, it is more likely to be the male (Wojczulanis-Jakubas et al. 2020a)], the Little Auk system provides a quite unique perspective within which to fully understand the evolution and adaptive value of such behaviour in birds. This is especially true, given that none of several hypotheses proposed to explain this aspect of female behaviour [i.e. (1) decline in female body condition as the breeding season progresses because of higher primary reproductive investments, (2) remating with a new partner, (3) male aptitude for escorting the fledgling to sea, (4) reduced winter survival after the breeding season], seem to be fully applicable to the Little Auk (Wojczulanis-Jakubas et al. 2009b, 2012; Wojczulanis-Jakubas and Jakubas 2012; Jakubas and Wojczulanis-Jakubas 2013; Wojczulanis-Jakubas et al. 2013, 2014a, b, 2015a, 2018c, 2020a).

The single-egg/chick raised by the Little Auk in a hidden nest chamber also creates an excellent study system for parent–offspring recognition and communication. First, this simple configuration greatly facilitates the investigation of signal transmission between the partners. Second, it provides a control case for other systems with multiple individuals in the brood. Given the single chick in the brood and its “fixed” position in the nest, Little Auk parents theoretically do not need a signal to recognize their offspring. Since the costs of foraging are considerable (Gabrielsen et al. 1991; Konarzewski et al. 1993), parent birds should also be resistant to chick begging, so potentially, the evolution of parent–offspring communication could be constrained. Nevertheless, Little Auk parents do communicate with their chicks acoustically (Kidawa et al. 2017), and potentially in other ways, too. The contrasting expectation and results create an intriguing background for examining the issue of parent–offspring communication.

Predator–prey interaction

The Little Auk is a very attractive subject for predator–prey interaction studies, which are usually extremely difficult to perform owing to the complexity of predator and prey behaviour and the minimal likelihood of observing such episodes. Such studies in Arctic conditions may be highly effective because of the easy accessibility and observation of an unlimited number of sequences of events. The most important predators of Little Auks are the Arctic Fox Vulpes lagopus and Glaucous Gull Larus hyperboreus (Stempniewicz 1995). Predators have adopted various techniques for hunting Little Auks efficiently (Stempniewicz 1983, 1993; Jakubas and Wojczulanis-Jakubas 2010). Anti-predatory adaptations in Little Auks function at the individual, population and species levels. As a result, predatory pressure from Glaucous Gulls is strictly limited by time mechanisms. They include the synchronization of all stages of the breeding period, most strongly expressed at fledging when the chick is easy prey. Departure from the nest is condensed into a few days and several hours a day, resulting in a swamping effect, which, together with the protective behaviour of the father, substantially minimizes losses (Stempniewicz 1995; Wojczulanis et al. 2005).

Foraging ecology

The Little Auk is one of the few pelagic seabirds (apart from Procellariiformes and Sphenisciformes), and so far the only alcid species, reported to exhibit a bi-modal foraging strategy during the chick-rearing period, i.e. alternating long foraging trips (both in terms of time and distance) with a series of short ones (Steen et al. 2007; Welcker et al. 2009a; Wojczulanis-Jakubas et al. 2010a; Jakubas et al. 2012). Diving behaviour generally differs between the long and short foraging trips with the magnitude of the disparity in diving characteristics depending on local foraging conditions (Karnovsky et al. 2011; Brown et al. 2012). This dual foraging strategy is interesting in the context of parental investment, as it is assumed to have evolved to reconcile the conflicting interests of parents and offspring (Jakubas et al. 2014). A study of body mass changes in Little Auk adults returning to their nests from foraging flights revealed that during short trips, the birds collect food for the chicks whereas the long trips are dedicated mainly to self-maintenance (Welcker et al. 2012). Moreover, with the two parents feeding the chick and both exhibiting the dual foraging strategy, the Little Auk is a perfect model species for examining parental coordination of the feeding performance. Studies show that parenting males and females avoid overlapping their long foraging trips, i.e. coordinate their foraging flights, thereby ensuring regular provisioning of the chick (Wojczulanis-Jakubas et al. 2018a; Grissot et al. 2019).

Ecosystem engineering

Apart from the effects of high numbers of individuals breeding in particular colonies, Little Auks profoundly alter terrestrial Arctic ecosystems by supplying marine-derived nutrients (MDN) (Skrzypek et al. 2015; Zwolicki et al. 2016a, b; González-Bergonzoni et al. 2017). Such nitrogen-rich ‘oases’ underlying Little Auk colonies massively enhance primary production, resulting in a higher richness of plant cover, which attracts herbivores, including geese, Reindeer Rangifer tarandus, Muskoxen Ovibus moschatus and some invertebrates (Stempniewicz et al. 2007; Mosbech et al. 2018). The large Little Auk colonies around the North Water Polynya in Greenland have profoundly altered the adjacent freshwater and terrestrial ecosystems. It has been estimated that MDN fuels more than 85% of terrestrial and aquatic biomass in bird influenced systems [this subsidy is much higher than that reported for migrating Pacific salmon species—23–25% of the biomass in aquatic organisms and terrestrial vegetation (González-Bergonzoni et al. 2017)]. A study performed in the large Little Auk colony on Spitsbergen found that the birds, respectively, supply the colony and the tundra beneath with 60 and 25 tons per km² of excreta (dry mass) annually (Stempniewicz 1990), and that the percentage of the total tundra nitrogen pool provided by birds ranged from 0 to 21% in patterned-ground tundra to 100% in ornithocoprophilous tundra (Skrzypek et al. 2015). Large colonies of Little Auks are usually located on gently sloping mountains, as a rule a few kilometres from the seashore, whereas colonies of piscivorous seabirds are situated on rocky coastal cliffs. The impact of the latter group on terrestrial ecosystems is therefore much smaller compared to Little Auks because the guano deposited on the seabird cliffs is rapidly washed out to sea (Stempniewicz et al. 2007). These results clearly indicate that the Little Auk acts as an ecosystem engineer, transforming terrestrial ecosystems right across its breeding range. Hence, ongoing climate change, causing a deterioration of Little Auk feeding conditions, may force them to leave their current breeding areas, which will have broad implications for both the marine and terrestrial Arctic ecosystems (Stempniewicz et al. 2007).

Concluding remarks

Given their characteristics (highly visible, easy to observe and capture in their colonies, allowing measurements of a wide variety of variables), seabirds have frequently been identified as useful indicators of the health and status of marine ecosystems, since they act as sentinels or bio-monitors of ecosystem change (e.g. contaminant load indicates pollution) and/or as quantitative indicators of specific ecosystem components, such as prey abundance (Piatt et al. 2007). In this context, the Little Auk, with all its life-history traits, breeding exclusively in the High Arctic, which is warming up more rapidly than any other region on Earth, has the potential for being both a qualitative and a quantitative ecological indicator of global changes, and a model species for other seabirds. It also fulfils many criteria applied to the selection of organisms for biological research (Dietrich et al. 2020): easy physical access (large breeding colonies are relatively easy to get to), phenomenal access (i.e. relevant to specific research questions concerning particular aspects of interest, e.g. the transition from bi-parental to uni-parental care), viability (a long-lived bird) and previous studies (knowledge about the species is already available). As in the case of each monitoring or model species, there are specific pros and cons for using the Little Auk in various studies (Tables 1 and 2). Some features of the species (a single-egg clutch/one chick, zooplanktivorous diet, High Arctic breeding range) are hard to extrapolate to other systems, but these features also greatly simplify research on questions that remain challenging in more complex systems, as well as offering an exceptional perspective, rarely considered in ecological studies. There are still many important issues to be investigated with the Little Auk as the model species. They include the mechanisms by which attractive foraging areas are detected, the threshold of environmental conditions above which birds are no longer able to compensate for suboptimal foraging conditions, the physiological consequences of rising air temperatures during the breeding season in High Arctic species, the reasons for the transition from bi-parental to uniparental care and the mechanisms by which parents coordinate their efforts/duties. The results of studies focussed on these issues have the potential to be extrapolated to other groups of organisms.

Table 1 Research questions that can be investigated with the Little Auk as a model species

Table 2 Pros and cons of the Little Auk as a model species with regard to its specific features