Crowberry (Empetrum): A Chief Arctic Traditional Indigenous Fruit in Need of Economic and Ecological Management

The genus Empetrum (Ericaceae) is controversially classified taxonomically. It is conservatively treated as comprising one variable widespread circumboreal/circumarctic species, E. nigrum, usually known as black crowberry (although there are other fruit colors), and a comparatively localized circumantarctic species, E. rubrum, called red crowberry. For millennia in the Northern Hemisphere crowberries have been a valuable source of berries for Indigenous Peoples, and indeed Empetrum is one of the most important berry crops of the Arctic. It has recently begun to be marketed as a commercial processed fruit crop, with increasing evidence of possessing phenolic compounds of high value for nutrition and medicine. Ecologically, Empetrum is a keystone species, sustaining numerous birds and mammals, and dominating many tundra and heathland ecosystems through allelopathic toxins that exclude competitive plants. With climate change expected to greatly alter the northern world in the near future, there is considerable concern about the welfare of Empetrum.


Introduction
The Arctic region is often defined as the area north of the Arctic Circle (66°33' N), or alternatively the area north of the northernmost tree line. Local climates, especially in coastal regions, allows limited production of conventional crops in a few restricted regions, but in most of the Arctic the predominant food plants available for human consumption are wild dwarf shrubs producing edible fruits. Of these, Empetrum (crowberry) is a widely harvested wild plant of the harsher regions. Porsild (1953) remarked "Crowberry… is easily the most important fruit of the arctic regions," a contention that is at least suggestive of its considerable value. Nestby et al. (2019) noted "Throughout history, wild berries have played an important role in the boreal, arctic and alpine areas in the northern hemisphere. In European history, the use of wild berries by humans living in northern Europe dates back about 750,000 years." In relatively mesic areas of the northern hemisphere, there are hundreds of harvested wild berry species, as well as domesticates that are competitively superior to wild fruits and likely to remain so. Nevertheless, the fact that Empetrum is so dominant ecologically, so widely distributed, and so widely consumed in much of the northern world makes this fruit of special interest.
Several current factors combine to make an improved understanding of the crowberry timely. First, climate change is disproportionately heavily affecting the Arctic, and is predicted to warm much of the circumboreal world, destabilizing and harming natural northern ecosystems, of which the crowberry is a critical constituent. Second, urbanization and raw material development are expected to greatly increase (Laruelle, 2019), also threatening natural ecosystems. Third, the need to import food to feed increasing northern populations, to say nothing about the quite inadequate food supply of northern indigenous peoples, will increase pressure to develop high latitude agriculture, and given that the crowberry is already a dominant wild food plant of the coldest regions, its sustainable management is of considerable practical importance. Finally, and by no means the least consideration, indigenous peoples of northern regions currently are the principal consumers of the crowberry and have deep insight into its usages, and in the light of scarce income issues, fairness demands that they receive appropriate priority for local development of this unique resource.
Because it is extremely widespread, studies of crowberry have been quite scattered. Because it is mostly a plant of relatively unpopulated northern regions and is not competitive with commercial fruits, it has not received nearly the examination that temperate and tropical food plants have been afforded. Now that the crowberry has been identified as a premier candidate for development and management, it is in order to review what is known and what are the research priorities.
As presented in the following, the genus Empetrum (at least in the Northern Hemisphere) is highly variable and different classifications have led to confusion. For simplicity, and following a common practice, we consider all Northern Hemisphere natural populations to be assignable to E. nigrum L., and all Southern Hemisphere populations to be E. rubrum Vahl ex Willd. Murray et al. (2009Murray et al. ( , 2020, the most authoritative treatment of North American Empetrum, also recognize E. eamesii submerging Empetraceae, Epacridaceae, Monotropaceae and Pyrolaceae in the Ericaceae. Comparisons… provide ample evidence to justify retaining the segregate ericalean families for practical purposes." In opposition, Soltis et al. (2017) commented "Both molecular and morphological studies have provided compelling evidence for a broadly defined Ericaceae that includes Pyrolaceae, Monotropaceae, Epacridaceae, and Empetraceae."

The species controversies
The classification of the genus Empetrum is problematical, the number of species recognized ranging from two to 18, depending on the author (Jacobsen, 2005). The two comprehensive taxonomic monographs (Good, 1927;Vassiljev, 1961) were prepared before considerable modern systematic work was carried out, and are in need of revision. Vassiljev (1961) split the genus into 18 species, and his system was entirely or partly adopted in several Russian treatments (e.g., Tzvelev, 1980 for the Russian Arctic; Tzvelev, 1991 for the Russian Far East). Kuvaev et al. (1996) accepted Vassiljev's main northern Russian and Siberian taxa but recombined them as subspecies of E. nigrum. Baikov (1996) did not apply Vassiljev's system for the Flora Sibiri. Elven (2011) noted that Vassiljev's system has not been adopted outside Russia. In contrast, Hultén (1971) suggested that the entire genus could be considered to be a single, variable species. Mirré (2004), which represents an especially insightful analysis of Empetrum, concluded that Northern Hemisphere plants and Southern Hemisphere plants are distinctive lineages meriting separate species recognition, but "No single morphological character unambiguously distinguished among population groups within the two lineages." We follow this acceptance of just two species (Fig. 1). However, Mirré (2004) noted that while molecular differences distinguish E. nigrum and E. rubrum, morphological distinctions aside from fruit color have not been reliably documented (although geography makes identification straightforward). Our review of the literature has also not revealed reliable morphological differences. Hagerup (1927) divided Northern Hemisphere plants into two species on the basis of a combination of ploidy and sex: E. hermaphroditum Lange ex Hagerup (monoecious tetraploids) and E. nigrum L. (dioecious diploids). Löve and Löve (1959) supported this division. At the infraspecific level, these taxa have been recognized as E. nigrum subsp. hermaphroditum (Hagerup) Böcher (or E. nigrum var. hermaphroditum (Hagerup) T. J. Sørensen) and E. nigrum subsp. nigrum. The authoritative taxonomic treatment in the U.S. Germplasm Resources Information Network (https://www.ars-grin.gov/) and the corresponding print edition (Wiersema & Leon, 2013) recognize the two taxa as subspecies, but without comment. Elven (2011) criticised this taxonomic division on the basis that tetraploids seem to have arisen several times from different combinations of diploids and so cannot be assigned to a single lineage or taxon. Moreover, Elven noted that the name E. hermaphroditum is nomenclaturally based on tetraploid Greenland plants, but these differ in molecular markers from the tetraploids in Europe and northwestern North America, and so the taxon is unaceptably polyphyletic. Both putative taxa are very variable, overlap considerably morphologically, co-occur, and hybridize (Li et al., 2002;Suda, 2002;Suda et al., 2004).
In North America, two additional species are often recognized: the diploid, northeastern American E. eamesii Fernald & Wiegand with translucent pink to red fruits and the tetraploid northeastern American E. atropurpureum Fernald & Wiegand with opaque purple fruits, interpreted as an allotetraploid from E. eamesii and diploid E. nigrum (Elven, 2011). We regard these taxa as requiring confirmation, but employ the names in quotation marks as labels for the North American variants lacking black fruits.
In some Asian publications (e.g. Tianlu & Anderberg, 2005;Park & Lee, 2013), authors recognize plants of Asia as E. nigrum var. japonicum K. Koch ("E. nigrum subsp. japonicum Hultén"). Korean plants have been delimited as E. nigrum subsp. asiaticum (Nakai ex H. Ito) Kuvaev. Without a comprehensive recent treatment, the distinctiveness of Asian plants remains to be demonstrated. We judge the 21 st century systematic publications recognizing Empetrum species other than E. nigrum and E. rubrum as valuable works of high quality, but in view of obvious extensive and overlapping variation, we think that sampling has been insufficient to warrant species status. As noted in this section, species delimitation has often been based on combinations of fruit color, ploidal level and breeding system, and so information on the variation of these features is warranted. This is provided in the following.

Taxonomy and fruit color
Plants of the Southern Hemisphere (primarily southern South America) are red-fruited (Fig. 2), and appear to all be diploid. They are usually dioecious, but monoecious and polygamous plants also occur (Smith, 1973). They have been recognized as E. rubrum. On the basis of morphology Anderberg (1994) reported that E. rubrum was distinctive. Fig. 1 The two widely accepted species of Empetrum (public domain images). a Empetrum nigrum from Thomé (1885). 1: male flower. 2: stamen. 3: female flower. 4: perfect flower. 5: long section of perfect flower. 6: seed. 7: fruit. 8: long section of fruit. 9: flowering branch. 10: fruiting branch b Empetrum rubrum from Vallentin and Cotton (1921). 1, 2: flowering male branches. 3: fruiting branch On the basis of molecular and morphological studies Mirré (2004) found good support for the recognition of the Southern Hemisphere plants as a species separate from the Northern Hemisphere plants, although Li et al. (2002) did not. As discussed later, The Southern Hemisphere plants likely originated by long-distance dispersal from the Northern Hemisphere in pre-historic times.
Plants of the Northern Hemisphere, the vast majority of which are black-fruited (Fig.  3), may be collectively assigned to E. nigrum L. North American populations with fruits that are pink, red, or purple have, debatably, been separated as different species (Murray et al., 2009). Herbarium collections of North American red-and purple-fruited plants may be viewed online, for example, at: Consortium of Northeastern Herbaria (http://portal.neherbaria.org/portal/imagelib/search.php?submitaction=search&taxa= 846807), which shows many U.S. collections. The digital flora of Newfoundland and Labrador (http://www.digitalnaturalhistory.com/flora_empetraceae_index.htm) particularly well illustrates the variety of fruit colors that exist. The name E. eamesii has been employed to designate plants with pink or red berries in southeastern maritime Canada ( Fig. 4; see the distribution in Fig. 11). The name E. atropurpureum has been employed for plants with red or purple berries, in Southeastern Canada and Northeastern U.S.A. (Fig. 5; see the distribution in Fig. 11). These taxa, often called purple, pink, or red crowberry (depending on their fruit color), or rock crowberry (a name widely applied to Empetrum), were proposed and described in detail by Fernald and Wiegand (1913). The presence of red, pink, and/or purple fruits in a fairly narrow geographic range of eastern North America could be explained in various ways. Possibly there has been selection pressure by locally distributed animals. Possibly a local historical catastrophe resulted in a small mutant founder population with genes for fruit color, and it established local distribution. The difficulty in accepting these as species rests with the lack of demonstration that these fruit colors have been convincingly shown to be correlated with other discriminating characters, so that philosophically they are segregated merely as one-character taxa (perhaps deserving only the status of formae). Many authorities simply assign E. eamesii and E. atropurpureum to synonymy of E. nigrum (e.g. USDA Forest Service, 2002; Global Biodiversity Information Facility 2020).

Taxonomy and sex
As some readers may be unfamiliar with technical reproductive terms, those that are often applied to Emptrum are defined in Table 1. The flowers may be perfect or unisexual (staminate or pistillate, i.e. male or female). The plants may be monoecious (with perfect flowers), polygamous (with mixed unisexual and bisexual flowers), or dioecious (with some plants having male flowers only, others having female flowers only). As noted above, dioecious and monoecious populations have been taxonomically separated at some rank. Hower, plants (especially in North America) are often polygamous, making floral sex a difficult character to apply. Webb (1972) indicated that the two alleged taxa have somewhat different distributions and morphology in Europe. However, there is not a clear correlation of sex with either geography or ploidy. For North America, Murray et al. (2009) reported that the two putative taxa are somewhat allopatric, but while diploids tend to be dioecious and tetraploids tend to be monoecious in some locations, ploidy simply is insufficient to define two separate groups in other locations. Whether the plants are dioecious, monoecious, or

Taxonomy and ploidy
Plants of Empetrum have been found to be diploid (2x = 2n = 26), tetraploid (4x = 2n = 52), and (occasionally) triploid (3x = 2n = 39). Sometimes two or three of these chromosome complements have been recorded in the same population (Suda, 2002;Mirré, 2004). Ploidy has been employed as a supporting character for taxonomic recognition. A minority of Empetrum have fruits that are not black. Only diploid counts have been found for Southern Hemisphere plants (E. rubrum). With reference to northern plants with pink, purple or red fruits, Murray et al. (2009) recognized "E. eamesii" as a diploid species, and "E. atropurpureum" as a possible allotetraploid derived from diploid "E. eamesii" and a diploid E. nigrum.
Most variation of Empetrum is in Northern Hemisphere black-fruited populations, which occur both as diploids and tetraploids. Diploid plants are common boreal plants in mainland (boreal-Arctic) Europe (Elven, 2011), and probably also in eastern north America (Aiken et al., 2007). They are known from Iceland and coastal areas of the North Pacific. Mirré (2004) noted that diploid plants usually are dioecious, while   (Elven, 2011). However, it appears that the tetraploid phase is not uniform, and may have multiple origins. Popp et al. (2011) concluded that the tetraploids in the mountains on the European mainland probably have a parental background different from the tetraploids in Greenland and elsewhere. Tetraploids usually are monoecious (and so often identified as E. nigrum subsp. hermaphroditum). An extensive study by Mirré (2004) based on AFLP markers, followed by a study by Popp et al. (2011) based on plastid and nuclear sequences, showed a very complicated structure with several intermingled diploid and tetraploid lineages, probably with a reticulate structure due to polyploidizations from several diploid combinations. Mirré (2004) stated "Tetraploidy and hermaphroditism appear to have originated in different time and space horizons, and, though fairly well correlated, should only be used in taxonomical delimitations when associated with other morphological characters." That is the use to date by taxonomists of ploidy level and separation of male and female floral features to delimit taxa (either at the species or infraspecific level) does not seem justified.
The relatively northern distribution of tetraploids compared to diploids in Empetrum reflects a general tendency in many Northern Hemisphere plant species with extensive distribution areas. As pointed out by Hijmans et al. (2007), "Polyploids are more common at higher latitudes… an important reason for the abundance of polyploids in arctic regions appears to be that they are more successful than diploids in colonizing after deglaciation." Bliss (1971), however, indicated that polyploidy is not necessarily more common at higher latitudes, but appears to be more common in stressful environments. For recent sophisticated discussions of the adaptive significance of polyploidy, see Soltis et al. (2014), Van de Peer et al. (2017), and Sessa (2019).

Roots
Young plants develop a strong primary root and a vertical shoot. The substantial primary root produced by Empetrum is eventually replaced by shallow roots originating from creeping lateral shoots outspreading from the central point of the original young plant. Some of the straggling or procumbent stems produce adventitious roots where they contact the ground, a form of natural layering (Fig. 6). A dense mat of finely branched roots is developed in the top 10 cm of the substratum. The shallow roots are susceptible to damage from trampling and fire, making the plants quite sensitive to both factors. As frequently occurs in species of the plant order Ericales, root hairs are absent, but an endotrophic mycorrhiza is present to aid with nutrient absorption (Matthews, 1992;Johnson & Gehring, 2007).

Stems
Older plants develop creeping lateral shoots resulting in an outspreading growth from a central point. The mature plant is a creeping, prostrate to semi-prostrate, mat-forming, much-branched, dwarf colonial shrub 5-50 cm in height (often no higher than 10 cm). The woody stems are 5-30(100) cm long, strongly branched, green (especially when young), and brown or reddish (often reddish when older or in colder times). Hairiness of the stems varies considerably (with whitish simple hairs and also sometimes glandtipped hairs), depending on population and age of plant, and is more dense on the distal parts. The bark is smooth and exfoliating. The branchlets are very slender. The centres of the shrub senesce as the outer stems grow outward laterally. Plants of crowberry as old as 140 years have been recorded (Good, 1927).
Site characteristics influence the morphology of Empetrum. In locations with high wind exposure, it is prostrate and branched; in wet places it may be sparsely branched; on dry substrates it tends to develop branching shoots and become bushy (Matthews, 1992).

Foliage
The leaves are evergreen, very small, coriaceous, sometimes reminiscent of the needles of spruce and fir trees (Fig. 7c). They are arranged alternate, subopposite or whorled (in a paper communicated by Charles Darwin, Airy 1877 commented on the variability of leaf arrangements on the same branch). The internodes are short. The leaves are crowded towards the stem apex, and either divergent or reflexed from the stem. They are 2-6(10) mm long, 0.5-1.5 mm wide, without evident petioles (the petioles are minute), with entire margins, and like many other plants in the Ericaceae, they have adaptations for conserving water: they are coriaceous (tough & leathery) and hairy below (which retards water loss from the stomates). The margins of the leaves are strongly revolute downward (so-called ericoid leaves; Fig. 7a, b). This creates a groove on the lower surface when the curved margins do not meet, or a tube when they do (another feature minimizing water loss from the lower leaf blade). The surfaces of the plant, particularly the inner surface of the rolled leaves, often bear gland-tipped hairs  (Muravnik & Shavarda, 2012; the margins may be glandular-ciliate). However, there is considerable variation among plants in stem and foliage pubescence.

Flowers
One or several branches bear flowers in the axils of the uppermost leaves. The solitary, inconspicuous, pinkish or purplish flowers are quite small, 1-2 mm long. The Empetraceae are commonly described as apetalous (e.g. Wood Jr. & Channell 1959). Nevertheless, the flowers of Empetrum have two whorls of free tepals, and below these are three tiny scaly often purplish bracts. The relatively small, lower tepals are usually greenish, and look like what most botanists would label as sepals. The uppermost set of tepals are larger, more delicate, and colored (whitish or purplish), and resemble what most botanists would call petals, but are nevertheless inappropriately called sepals in some texts. The flowers may be unisexual or bisexual. Male flowers usually have 3 stamens, perfect flowers have 2-6 stamens. The stamens are pinkish, with conspicously long filaments considerably exceeding the tepals. Female and perfect flowers have pistils composed of 6-9 segments (carpels) and a lobed stigma (6-9 lobes, one for each carpel). The styles, and often also the uppermost 3 tepals, fall off with maturity. The flowers lack evident fragrance (but this requires confirmation).  Bergen (1908). Note the glands on the abaxial leaf surfaces in a and b. c Views of the "bottoms" of leaves. The two lateral margins of the adaxial surface of the leaves are curved towards each other on the lower side, leaving only a line of opening to the inner part of the hollow cylinder that is formed. Photo by Krzysztof Ziarnek (CC BY SA 4.0)

Fruits
The sequence of development of the reproductive structures is illustrated in Fig. 8. The fruits (technically drupes) are 3-10 mm in diameter, globose, black, purplish-black, dark purple, or red when ripe, with sepals and sometimes also the petals (which often fall off), persisting at the base of the fruit. Fruit produced from bisexual flowers (but not female flowers) may also show desiccated stamens at the base. The flesh is reddishwhite.

World distribution
The genus Empetrum has an unusual pattern of distribution ( Fig. 10): circumpolar and widespread (circumarctic, circumboreal, transcontinental) in the Northern Hemisphere, and bipolar (in both the far northern and far southern regions of the world). Hultén and Fries (1987) is a particularly informative source of geographical information (map 1463 shows the putative distribution of the alleged taxon E. nigrum subsp. nigrum; map 1464 shows the putative distribution of the alleged taxa E. nigrum subsp. hermaphroditum, E. eamesii subsp. eamesii, and E. eamesii subsp atropurpureum). Other source of geographical information are: Löve (1960), Aiken et al. (2007), Small (2013), Kartesz (2015), Klinkenberg (2019), Global Biodiversity Information Facility (2020), Murray et al. (2020), and USDA Natural Resources Conservation Service (2020). Also useful are the informative albeit oversimplified maps in Donoghue (2011) and Popp et al. (2011). The Asian distribution of Empetrum is mapped in the following. Map 1463 in Hultén and Fries (1987) shows the putative distribution of the alleged taxa E. nigrum subsp. nigrum and E. nigrum subsp. japonicum. Empetrum nigrum var. japonicum has  (1868), remainder from Weiss (1789) been recorded on Kamchatka, Sakhalin Island, east Siberia, north-eastern China (Heilongjiang and Inner Mongolia provinces), Japan (central and northern Honshu, and Hokkaido), Mt. Baekdu and adjacent mountains in northern Korea, and Jeju Island (Min & Anderberg, 2005;Kim, 2007;Chung et al., 2013).  Hultén & Fries, 1987;Global Biodiversity Information Facility, 2020). This map shows approximate distribution, not fine detail

Northern Hemisphere distribution
In the Northern Hemispere, the distribution of Empetrum can be described as mid-arctic and sub-arctic. Mid-arctic includes the middle latitudes of the Arctic, while the subarctic includes the region immediately south of the true Arctic (much of Alaska, Canada, Iceland, northern Scandinavia, Siberia, the Shetland Islands, and parts of Scotland)mostly between 50°N and 70°N latitude.

Eurasian distribution
In Europe, the range extends south to the Pyrenees, the North Apennines, Macedonia, southern Bulgaria and the Caucasus. In Asia, Empetrum has been recorded in the Altai Mountains, China, and North Korea. In Pacific Asia the species occurs southward to the alpine regions of Japan, through the Kurile Islands, and across the Aleutian Islands to northwestern North America. Isolated southern mountain populations such as in Korea are often threatened by wildfire, change in water level, excessive growth of trees, recreation, invasive species, pollution, and global warming (Kim et al., 2005). In the Tomsk region, within the boreal coniferous forests of the West Siberian Plain, E. nigrum is protected as an endangered species (Semenova et al., 2017).

North American distribution
In North America, Empetrum occurs in Alaska, all of the provinces and territories of Canada, the three West coast states, and the northeastern states. On the Pacific coast it is found as far south as Del Norte County in northern California. In the eastern United States it has been recorded in the mountains of Maine and New Hampshire, in Michigan, Minnesota, and Vermont, and in isolated regions of New York. In some areas of its southern U.S. distribution, it is categorized as "sensitive," "threatened," "vulnerable," or "critically imperilled" (USDA Forest Service, 2002).
In North America, the greatest diversity of dwarf berry shrubs (including Empetrum) occurs in Low Arctic areas, and their highest berry productivity was identified to occur in subzone D of the map on page 35 by Bell and Brown (2018;available online).

North American distribution of red-, pink-, and purple-fruited plants
Distributions of the two putative eastern American taxa with non-black fruit are shown in Fig. 11. Murray et al. (2009Murray et al. ( , 2020 gave the distribution of their "E. eamesii" as Newfoundland, Labrador, Nova Scotia, Prince Edward Island, and Quebec; and the distribution of their "E. atropurpureum" as all of the above Canadian distribution and Maine, New Hampshire, New York, and Vermont. Löve (1960) indicated that "E. atropurpureum" was also in the Great Lakes (Lake Superior) region (Michigan and Minnesota). A University of Montreal photo of "E. atropurpureum" on the Magdalen Islands (Îles de la Madeleine, Quebec) is shown at https://calypso.bib. umontreal.ca/digital/collection/_madeleine/id/457/. The USDA Natural Resources Conservation Service, Plants profile for "E.

Southern Hemisphere distribution
As well as being circumboreal, the genus Empetrum is amphitropical, i.e. it has a disjunct distribution pattern with one part of the range north of the Equator, and the other part geographically well separated south of the Equator. The distribution of Empetrum is "bipolar" (a particular kind of amphitropical pattern), i.e. it occurs in the northernmost parts of the Northern Hemisphere and in the southernmost parts of South America. As noted above, there is good evidence to accept the southern plants as a distinct species, E. rubrum. Empetrum rubrum is restricted to the southern Andes regions of Chile and Argentina, Tierra del Fuego, Falkland Islands, and the Juan Fernandez and Tristan da Cunha groups of islands (Good, 1927;Moore et al., 1970;Mirré, 2004;Fig. 12). Global Biodiversity Information Facility (2020) also indicates presence in South Georgia and the South Sandwich Islands (Global Biodiversity Information Facility, 2020 cites hundreds of records of "E. rubrum," some of which are well outside the probable range; although cited they are not presented in Global Information Facility's map of Empetrum in apparent recognition that they are questionable.) The genetic relationships of the southern populations of Empetrum (i.e. E. rubrum) and the northern populations (E. nigrum s. lat.) have been examined in several publications. In early publications, some taxonomists interpreted the red berries of both South American Empetrum and some eastern North American populations as evidence Fig. 11 Distributions of the North American Empetrum taxa with non-black fruits, Empetrum eamesii and E. atropurpureum based on information in Löve (1960). Black-fruited plants should also be expected throughout the range of both. In much of the periphery of the range, Empetrum is rare and often endangered of close relationship. However, molecular evidence indicates that E. rubrum seems to have its closest connection with and to have been derived fairly recently from northwestern (Pacific) North American black-fruited E. nigrum s. lat. (Popp et al., 2011).
As noted by Mirré (2004), authors have proposed different explanations for bipolar distribution patterns in plants, including divergence from a common tropical ancestor, step-wise migration, long-distance dispersal, and vicariance. Continental drift or "vicariance biogeography" may provide an explanation for bipolar distributions (for example, an ancestral group may be split geographically by geological events). However, as Donoghue (2011) has pointed out, bipolar plant distributions have usually been shown to be too recent to be explained by ancient plant tectonics. The most plausible possibility is long-distance transport by some agent. Well-known long-distance distribution agents in plants include drift ice and driftwood (Johansen & Hytteborn, 2001) and wind (Jacobsen, 2005), but these are unlikely to have been responsible for bipolar distribution. Raven (1963) emphasized bird distribution as a likely cause of amphitropical plant patterns. For Empetrum bipolarity, "The best explanation for this distribution is that, sometime during the Mid-Pleistocene, a bird … ate the fruits of an E. nigrum plants and then flew to the southern tip of South America before depositing the seeds" (Donoghue, 2011). A convincing publication in support of this theory is Popp et al. (2011), who hypothesized that a single dispersal by a bird from Northwestern North America to southernmost South America, during the Mid-Pleistocene was responsible for establishing the southern populations. While it is speculative which birds could have been responsible for transporting E. nigrum in the past, based on  Popp et al., 2011;Global Biodiversity Information Facility, 2020) present bird migrations, possible vectors include the whimbrel (Numenius phaeopus subsp. hudsonicus) and the American golden plover (Pluvialis dominica), which have been reported to feed on Empetrum before migrating southward from their northern breeding grounds where E. nigrum occurs to the southern areas where E. rubrum also occurs (Johnson et al., 2020;Skeel & Mallory, 2020).

Sexual vs. vegetative reproduction
In the Northern Hemisphere, Empetrum occurs in Arctic, sub-Arctic, and alpine regions, stressful habitats in which plant species are predominantly perennial (Bliss, 1962;Billings & Mooney, 1968;Savile, 1972). Compared to annuals, perennials like Empetrum have the advantage of being able to survive for years without producing seeds, which is of particular importance when the environment is very demanding in some years. Remarkably, Díaz-Barradas et al. (2014) found that male plants of E. rubrum appear to be more resistant to stressful environments than female plants, possibly because producing seeds especially reduces energy reserves making female plants more susceptible.
Branches grow from the base of Empetrum as it matures. Most of these extend laterally, and where they contact the ground, shallow adventitious roots may develop (i.e., natural 'layering' occurs), spreading the plant laterally as a clone. Such vegetative reproduction has been claimed to be more important than sexual reproduction in Empetrum (Bell & Tallis, 1973). Tybirk et al. (2000) attribute much of the capacity of Empetrum to dominate ecosystems to the plant's ability to aggressively expand laterally, thereby excluding competitors simply by outgrowing them.
The issue of relative importance of sexual and vegetative reproduction in very cold environments has been examined in several studies. Bliss (1971) noted that "in arctic and alpine environments, seedlings are not common and it has been assumed that vegetative reproduction predominates." Despite this view that sexual reproduction is of minor importance, Angers-Blondin (2014) and Angers-Blondin and Boudreau (2017), have pointed out that recent research suggests that sexual reproduction in so-called clonal species could be much more frequent and widespread than once believed. There is evidence of significant sexual reproduction in many species of cold environments (Gabrielsen & Brochmann, 1998;Szmidt et al., 2002;Venn & Morgan, 2009;Boudreau et al., 2010;Douhovnikoff et al., 2010;de Witte et al., 2012). Szmidt et al., (2002) and Bienau et al. (2016) studied populations of Empetrum in Scandinavia and observed substantial sexual reproduction. Similarly, Angers-Blondin (2014) and Angers-Blondin and Boudreau (2017) found considerable sexual reproduction in a population of Empetrum on the eastern coast of Hudson Bay in subarctic Quebec, and speculated that seed reproduction was becoming more significant because of a warming climate. Bienau et al. (2016) showed that clonal reproduction increases with snow cover. The most likely cause of increased layering with increasing snow cover is greater and longer soil moisture leading to better chance that adventitious roots will successfully establish. This is fortuitous because plants covered by snow for much of the time have less opportunity to develop flowers, attract pollinators, and produce seeds.

Wind vs. insect pollination
There is uncertainty regarding the relative occurrence of wind and insect pollination in Empetrum. Several features of the flowers resemble those typically found in windpollinated plants, such as small flowers lacking in showy petals, well-exposed anthers, and large stigmas. Wind-pollinated pollen grains are relatively smalltypically 20-60μ in diameter according to Shukla et al. 1998. Erdtman (1986 found diploid tetrads were 28μ in diameter, tetraploid tetrads were 41μ in diameter, which is within the range of wind-pollinated pollen. However, Empetrum produces pollen in tetrads, an unusual feature for anemophilous plants, as the heavy tetrads would not be carried by wind as easily as single pollen grains. Knuth (1906Knuth ( -1909 observed that the flowers secrete nectar, which he interpreted as a lure to attract flies, but Aiken et al. (2007) stated nectaries are absent. Animal-pollinated flowers are often scented, but the literature is not clear on the degree of odor of Empetrum flowers. In the Ericaceae, many of the genera have spurs on the anthers, facilitating efficient deposition of pollen on visiting insects, but these are absent in Empetrum (Alsos et al., 2019), consistent with wind pollination.
According to Kevan (2009), pollination can be both by wind and by insects, including flies and bees (Colletes and Andrena). Bell and Tallis (1973) stated "Although the flowers are wind-pollinated, pollen is not dispersed to any great distance." Alsos et al. (2019) observed that "Pollination is assumed to be affected by wind but the purple colour attracts some insects (flies often observed on Empetrum flowers)." USDA Natural Resources Conservation Service (2006) suggested that wind pollination may be essential for good fruit production. Blondeau et al. (2018) stated that Empetrum is wind-pollinated. It appears that both wind and insect pollination occur with some frequency, but a reliable evaluation of the two modes is not yet available. Reviewing pollination in angiosperms, Culley et al. (2002) stated "Recent evidence suggests that ambophily (a combination of both wind and insect pollination) might be more common than was previously presumed."

Self vs. cross pollination
Dioecious Empetrum (which are mostly diploid) are necessarily outcrossing (except for occasional polygamous plants). The degree of selfing in monoecious Empetrum (mostly tetraploids, commonly labelled "E. hermaphroditum") is at issue. At least in theory pollen from a monoecious plant could fertilize (i.e. selffertilize) ovules on the same plant. Wind-and insect-pollination have been observed, indicating that inter-plant crossing occurs, but the extent of selfing is unclear. Pollinators are relatively limited in arctic and alpine regions (Fulkerson et al., 2012), so dependence on them is likely to be limited, at least in many species adapted to these regions.
The existence of diploid and tetraploid populations leads to the possibility of hybridization between the ploidy levels. Generally pollen from diploids cannot fertilize tetraploid plants, and vice-versa (rare unreduced diploid pollen may fertilize tetraploid plants). Occasional triploid plants indicate that crossing between diploids and tetraploids does occur, and these triploids may (rarely) provide a bridge to transfer genes between diploids and tetraploids (Suda, 2002).
Selfing can lead to inbreeding depression in some species that can be both cross-and self-pollinated, but the resulting genetic homogenization may be evolutionarily adaptive in some circumstances (Barrett, 2003). Tikhmenev (1984) found that "E. nigrum" (obviously monoecious tetraploid plants) had an autodeposition efficiency of 0.9, i.e. plants protected from pollen achieved 90% of seed production compared to plants not protected from pollen. This indicates that the sample examined was mostly selfing. In strong opposition, USDA Natural Resources Conservation Service (2006) stated "Self pollination is considered impossible or so slight that fruit yield is significantly reduced if cross pollination does not occur." It may be that genetic and environmental factors conducive to the degree of selfing vary considerably, and such considerations explain these contradictory claims.

Seed viability & seedling survival
Although as pointed out previously vegetative reproduction is extremely strong in Empetrum, the species nevertheless sometimes produces considerable seeds. Vieno et al. (1993) found up to 588 viable seeds per m 2 under Empetrum plants in Finland. Komulainen et al. (1994) counted up to 150 viable seeds per m 2 under Empetrum in northern Russia.
Students of seed biology of Empetrum, ranging back to Hagerup (1946) have commented on their dormancy. In his field studies, Hagerup (1946) observed that seeds germinate sporadically, often only after 4 years of deposition in the soil. Hagerup pointed out that most germination in Scandinavia occurs in the spring. (As noted below, Bell & Tallis, 1973 observed germination throughout the winter in the British Isles.)  intensively examined germination of seeds from five sites in Sweden. They first observed that 62% of seeds were filled (i.e. at least 38% were inviable). They subsequently observed that only 2-5% of freshly matured seeds collected in September and October germinated, indicating that the seeds are naturally dormant. Application of gibberellic acid promoted germination of 77-87% of the intact seed samples, and it was concluded that at least most of the dormancy in Empetrum is physiological (and not, for example, due to impermeability preventing water intake). They examined the effects of cold (near 0°C) and warm (up to 30°C) stratification with various combinations of illumination (light or dark), and concluded that the seeds are naturally adapted to first require relatively warm stratification (i.e. autumn temperatures) followed by cold (i.e. winter) stratification. The experimental temperature regimes examined were 15/6°C, 20/10°C, and 25/15°C. They found that 12 weeks of relative warm followed by 20 weeks of relative cold, under illumination, resulted in over 90% germination in some of the collections. Long periods of cold stratification (20 or 32 weeks) resulted in 22-38% germination, while a long period of warm stratification (16 weeks) resulted in 10% germination. Komulainen et al. (1994) also observed that gibberellic acid was necessary to faciliate germination of seeds collected from nature. Seeds that we obtained from several germplasm banks and planted without gibberellic acid treatment germinated very poorly and slowly, and the seedlings grew very slowly.
In coastal Nova Scotia, Hill et al. (2012) observed (consistent with  that recently produced seeds were mostly dormant and the germination that did occur was very slow (compared to more rapid germination after overwintering).
Moreover, Hill et al. (2012) observed that after overwintering, about 50% of the seeds that overwintered in scat germinated, but about 33% of the seeds that overwintered in berries germinated. The clear suggestion here is that seeds passing through animal digestive systems germinate better. Hill et al. observed that seedlings essentially did not establish in crowberry mat (continuous vegetative cover).
Angers-Blondin and Boudreau (2017), also consistent with , stated that most crowberry seeds "possess physiological dormancy that requires warm (late summer) and cold (winter stratification)." These authors also noted that seedling survival for crowberry varies considerably with habitat, annual mortality ranging from less than 10% to more than 90%. Bell and Tallis (1973), for the British Isles (where temperatures only occasionally fall below 0°C), noted (in conformity with the observation above of Angers-Blondin & Boudreau, 2017) that cold stratification is required to break dormancy. They concluded that low temperatures over the winter are necessary for breaking dormancy under natural conditions. Bell and Tallis (1973) stated that optimum germination temperature is 25-30°C, but this is based on plants in England, and the optimum temperatures for northern plants may be different. Bell and Tallis (1973) also reported that crowberry seedlings are widespread overwinter but seedling survival declines rapidly during the winter.

Seed dispersal
Empetrum seeds are dispersed by mammals and birds (Bell & Tallis, 1973;Johnson, 1975). In the section on herbivory presented later, the varied animals that consume the seeds are noted. Grouse are the main agents of dispersal in upland areas of Britain, but numerous other birds species are also responsible (Bell & Tallis, 1973). As noted in the discussion of bipolar distribution, birds were responsible for transporting seeds from the Northern Hemisphere to the Southern Hemisphere, and presumably also for bringing seeds to isolated islands.
Endozoochory is the distribution of seeds by passing through the digestive systems of animals. Seeds adapted to such dispersal need to survive the mechanical and/or chemical forces encountered, and indeed may benefit from effects on the seed coat such as scarification, which may stimulate germination after excretion (Kleyheeg et al., 2018). As pointed out above, Hill et al. (2012) observed that seeds that had passed through the guts of animals germinated better.
The seeds of Empetrum are pyrenes. Pyrenes are seeds with a hard, bony layer, generally of endocarp origin (Fig. 8). (The word pyrene is also used to describe a drupe-like fruit with several small stony pits. A true drupe has a single pit, composed of a single seed surrounded by a stony endocarp.) The bony layer surrounding pyrenes seems an obvious adaptation to resisting mechanical damage associated with transmission through a gut, especially for surviving the abrasion experienced by passing through the gizzard of birds. Janzen (1982) predicted that plant species adapted to seed dispersal through digestive systems should have small, round, seeds, which is descriptive of the seeds of crowberry (Fig. 9).
Seeds passing through animal digestive systems are deposited in the animal's excrement (Fig. 13). Seedlings developing in dung have the advantage of being supplied with a supply of nutrients, especially nitrogen, which is a critical limiting element in northern habitats. Hagerup (1946) commented that on Danish moors, crowberry seeds in excrement of various animals can be widely observed.

Seed germplasm resources
The classification of Empetrum obviously requires study, but regardless of how the complex is recognized, the availability of considerable genetic variation in nature means that there are diverse resources available for collection, characterization, and long-term storage in nature. However, to facilitate scientific research and to serve as germplasm for creating cultivars, long-term seedbank collections are essential. A few public genebanks have Empetrum seeds. Also, a few commercial online sellers offer seeds of Empetrum.

Abiotic environmental factors
Landforms Crowberry plants are often near large bodies of water, as well as in the terrestrial interiors of continental areas. In North America, crowberry is associated with rockfields, coastal bluffs, sea cliffs, tundra, bogs, moorlands, and muskeg (Matthews, 1992;Small, 2013). Bell and Tallis (1973)

Substrates
Empetrum thrives in well-drained sandy soils (including sand dunes; Fig. 14), wet peat soils, mineral soils, bogs, and rocky terrain (Fig. 15), and is also found on glacial till and alluvial deposits (Douglas, 1974;Soper and Heimburger, 1982). In Canada, it is found on acidic rocks, gravel, peat, and tundra (USDA Forest Service, 2002). Crowberry can establish on mineral soils and stagnant surfaces rich in nutrients (Damman, 1977). The species tolerates a soil pH range of 2.5 to at least 7.7 (Bell & Tallis, 1973). It strongly avoids basic soils (Good, 1927;Bell & Tallis 1973), but rarely occurs on limestone pavement (Bell & Tallis, 1973). There are many parts of the Arctic where crowberry does not occur or is rare, particularly because the substrate is calcareous. In Britain crowberry has been recorded on impure shell sand with low nitrate and phosphate concentrations (Bell & Tallis, 1973). In mountain tundra, Empetrum can be found on sub-salt woodlands or sub-salt mining and mountain belts of the Northern Urals (Knyazev et al., 2019). Collantes et al. (1989) studied E. rubrum in the northern Tierra del Fuego, and observed that its density increased with the C/N ratio and aluminum content in the soil, and decreased with pH, calcium content and base saturation. Similarly Valle et al. (2015) found that growth of E. rubrum decreased with low pH, high aluminum activity and low amounts of non-acid cations in the soil.
Empetrum is an indicator of nitrogen-poor soils (Klinka et al., 1989), but is also found on nutrient-enriched sites (Matthews, 1992). It is generally associated with mycorrhizae (Bell & Tallis, 1973). The foliage is rich in phenolics, resulting in slow decomposition, producing an organic top soil. Plants like Empetrum with ericoid mycorrhiza are especially adept at extracting nutrients from this infertile substrate (Tybirk et al., 2000). Empetrum occurs in a wide range of soil moisture conditions, often on well drained wet sites, but is intolerant of prolonged water logging (Bell & Tallis, 1973. Indeed, excess water is considered a threat to the plant's survival (USDA Forest Service, 2002).

Heavy metal pollution
Anthropogenic pollution is increasing throughout the circumboreal north as a result of mining, urbanization (especially the establishments of dumps and the generation of liquid sewage), and transportation (including shipping and the expanded use of motorized vehicles). Empetrum is considered to be one of the most tolerant species near coppernickel smelters in the Northern Hemisphere (Helmisaari et al., 1995;Reimann et al., 1999;Reimann et al., 2001;Uhlig et al., 2001). It is capable of accumulating high concentrations of copper and nickel as evidenced by greenhouse experiments employing crowberry cuttings (Monni et al., 2000). Nevertheless the foliage appears particularly resistant to absorbing contaminants (Monni et al., 2001b;Lyanguzova, 2017). The tolerance of crowberry to nickel and copper is due to its ability to restrict accumulation of metals in its younger, growing parts (Helmisaari et al., 1995;Monni et al., 2000;Uhlig et al., 2001). Despite considerable tolerance, emission of heavy metal pollution has negative effects on E. nigrum (Monni et al., 2001a), and death of the plant has been observed due to agerelated damage of the main stem, resulting from soil toxicity near smelters (Zverev et al., 2008). Reiman et al. (2001) observed that manganese and phosphorus were significantly depleted in crowberry tissues, near Monchegorsk nickel refinery and smelter, probably a reflection of the decreased substrate suitability.

Fire
Empetrum is susceptible to fire, which is one of the factors that can significantly limit its success. Minor fires top-kill the plants, which will slow growth (Bell & Tallis, 1973;Wein, 1974;Viereck & Schandelmeier, 1980;USDA Forest Service, 2002). Moderate to severe fires kills underground parts close to the soil surface, which may slow recovery (Bell & Tallis, 1973;Racine, 1979;Viereck et al., 1992). Severe fires can entirely kill the underground portions and populations may not regenerate for many years (Tybirk et al., 2000). With climate warming, fires are expected to increase in forest-tundra and low Arctic regions where Empetrum occurs (Wottom et al., 2010).

Climate adaptation
In the Northern Hemisphere, Empetrum occurs in temperate to arctic climates, but is particularly adapted to short-season very cold climates, particularly subarctic and alpine sites. In the Southern Hemisphere, it is usually sub-Antarctic in continental regions of South America, but is also often found (as in the Northern Hemisphere) in more mesic coastal locations, particularly on South Atlantic islands. As is well-known, plants of extreme regions often need to be adapted not only to temperature per se but also to associated difficulties in acquiring and retaining water and nutrients. Perennial foliage (i.e. leaves that are evergreen, as in Empetrum) has been shown to be adaptive in stressful habitats such as arctic tundra (Aerts, 1995). While Empetrum survives well in subarctic and cool-temperate climates, appropriate habitat requirements need to be met. In most of Europe, Empetrum is restricted to subalpine and subarctic biomes and the species is essentially boreal-Arctic in its climatic preferences (Bell & Tallis, 1973;Buizer et al., 2012). It often inhabits sites exposed to fog, wind, and salt aerosols (Bell & Tallis, 1973) (Bell & Tallis, 1973).

. Empetrum grows best in open locations and is intolerant of shade, although it coexists with forest species in open woodlands
The occurrence of Empetrum is promoted by snow cover that provides a drought and frost barrier during the winter (Tybirk et al., 2000;Fig. 16). However, Empetrum is intolerant of snow-cover prolonged into the spring (Bienau et al., 2014;Bienau Fig. 16 Branches of Empetrum nigrum protruding from snow in northern Russia. A minimum amount of snow cover facilitates overwintering but too much kills the plants. Photo by Gennady Alexandrov (CC BY 2.0) et al., 2016). In alpine areas of northern Scandinavia, Empetrum is prevalently found on windy peaks with scarce and short-term snow cover (Tews, 2005). Olofsson et al. (2011) observed that a host-specific parasitic fungus, Arwidssonia empetri, killed the majority of the shoots of Empetrum after 6 years of increased snow cover in Sweden. Shvartsman and Bolotov (2005) pointed out that in some Russian regions, such as the southeast of the Kola Peninsula and the White Sea coast, the extensive development of crowberry tundras is due to low temperatures in the growing season and well-drained and poor soils of the Holocene marine terraces. Factors influencing this are the cooling effect of the White Sea in summer (Drozdov et al., 1989) and cold northwesterly winds, both producing cooling and desiccating effects (Kulyugina, 2004). Eyre (1968) concluded that wind speed is the most important factor controlling natural heathlands in Great Britain. In unstable habitats where the substrate is continually being removed by wind, Empetrum can form hummocks by accumulating sandy material (Tews, 2005). Crowberry populations occur from sea level to alpine areas (Matthews, 1992). McVean (1964) noted that E. nigrum occurs at altitudes higher than 650 m on exposed habitats of Scotland, Scandinavia and Iceland. Empetrum also appears further south in the high Alps (1200-1400 m; Polunin & Walters, 1985). At sea level, Empetrum tundra occurs in the arctic region north of 60°N, on the coasts of Greenland and northern Russia (Daniëls, 1994;Koroleva, 1994). Collantes et al. (1999) attributed the presence of Empetrum heathlands in Tierra del Fuego (52°S) at sea-level to the colder southoceanic climate related to the cold Falklands/Malvinas current and the high wind speeds.

Climate change prospects
Distribution changes of plant species caused by global warming in Arctic and subarctic regions, particularly due to rising temperatures and drying, have been recorded (Henry et al., 2012;Gérin-Lajoie et al., 2016). As temperatures increase, a general northward migration of species is expected (Lenoir et al., 2008;Steinbauer et al., 2018). Indeed, Parmesan (2006) observed the range margins of 1598 Northern Hemisphere species moved on average 6.1 km northward per decade or 6.1 m upward per decade. Although as noted below the effects of climate change on Empetrum are difficult to predict, such tundra species are often forecast to lose ground (Elmendorf et al., 2015). Buizer et al. (2012) observed a northward movement of Empetrum in Norway, particularly in the high Artic Svalbard region. During the past several decades, Empetrum occurrences in the southern limit of its European range (Great Britain, Ireland, Germany, and the Netherlands) have decreased (Buizer et al., 2012). These authors noted that global warming may affect the geographical distribution of Empetrum by influencing length of growing season, which can in turn affect the dates of leafing, flowering, and fruiting. However, Bokhorst et al. (2017) examined E. rubrum, one of the dominant shrub species in the Falkland Islands, over a 12 year period, and observed that its coverage did not change significantly. Buizer (2013), based on experimental studies in the Netherlands and the island of Spitzbergen, observed that warmer conditions affected the growth of Empetrum, sometimes improving fruit size, sometimes not, indicating that predicting future trends is difficult. Tevendale (2018) also cautioned that there are uncertainties in predicting the outcome of climate change in tundra communities where Empetrum is present.
Climate change in the Arctic is expected to produce longer growing seasons, warmer soil temperatures, improved nutrient availability, and increased solar radiation, which in the absence of competition would be expected to benefit the growth of Empetrum. As would be predicted, experimental studies have in fact demonstrated that the productivity of Empetrum increases with such conditions (Shevtsova et al., 1997;Wada et al., 2002;Buizer et al., 2012;Kaarlejärvi et al. 2012). However, the timing of warming can be critical: Bokhorst et al. (2009) found that unexpected winter warming can be extremely detrimental to Empetrum. Climate change may affect the variability of weather events, and so this consideration may be quite harmful to some species.
While growth conditions are likely to improve for Empetrum with climate change, at least in some regions, they are also certain to alter its performance in competition with other plants. In particular, deciduous shrubs may have a substantial advantage over evergreen shrubs like Empetrum (Chapin III et al., 1996). The schlerophyllous leaves of evergreens are naturally adapted to occupation of the cold Arctic (Aerts, 1995), because the foliage holds onto nutrients that are difficult to acquire from the frozen soils and leaves do not have to be developed every spring in a season that is very short. (Empetrum leaves typically remain on the plant for about 4 years.) However, the slow photosynthesis of evergreen leaves puts them at a disadvantage compared with deciduous shrubs in a less stressful environment. In some regions a moderating climate will also likely favor taller shrubs, to the detriment of the prostrate semi-dwarf Empetrum (Lavallée, 2013;Angers-Blondin, 2014;Spiech, 2014;Lussier, 2017). Nevertheless, evergreen shrubs like Empetrum will likely continue to dominate relatively cool sites with poor soils, where they have natural advantages.
Phenolic content of Empetrum appears to be modifiable by environmental conditions (Lavola et al., 2017). Väisänen et al. (2013) conducted studies to assess the interacting effects on phenolic development in Empetrum by global warming (represented by experimentally heated plants) and grazing by reindeer (artificially confined in plots). Under light grazing, warming altered the relative amounts of phenolics. As noted later, phenolics are ecologically important to the survival of Empetrum. Thus the effects of climate change on Empetrum may be expected to interact with other factors in complex ways.

Ecological communities
Plant species frequently occur together in communities because of their common adaptations to particular habitats. Empetrum associates well with other species occurring in alpine meadows, coastal bluffs, conifer forests, exposed sea cliffs, maritime heathlands, maritime grasslands, muskegs, open tundra (Fig. 17a), alpine tundra (Fig.  17b), rockfields, and sphagnum bogs. Many of the communities in which Empetrum occurs can be categorized as heaths, bogs, or grasslands (Bell & Tallis, 1973). However, crowberry sometimes forms dense mats of nearly monospecific vegetation (Tybirk et al., 2000). Empetrum often dominates ecosystems in woodlands and boreal sites, and in sub-artic, arctic, and alpine heathlands it is often co-dominant together with several ericaceous shrubs (Tybirk et al. (2000). Communities in which Empetrum occurs may be localized (such as in the Alps, where it occurs as a glacial relict) or widespread, as in much of the northern world, where it tends to occur in small to midsized patches on well-drained soils of plains and upland areas (Tews, 2005). Empetrum is frequently in assocations that are in open habitats, but also is an important constituent of the understory vegetation in the boreal forest. In North America, it is associated with coastal forests, moist coniferous forests, and sphagnum bogs (Matthews, 1992;Small, 2013).
Empetrum is a keystone species in many northern ecosystems, particularly subarctic tundra, where it is often quite aggresive, forming large, continuous, dense mats. It also occurs with some northern deciduous dwarf trees such as birch and willow. In more mesic southern habitats, it may dominate as an understory in open conifer woodlands. Empetrum frequently associates with other shrubs, particularly ericaceous species such as Vaccinium, Cassiope, and Pyrola, either in muskegs, bogs or open, moist tundra (Pollett, 1972;Douglas, 1974;Viereck et al., 1992;Aiken et al., 2007;Alberta Biodiversity Monitoring Institute, 2019). In Patagonia, Henríquez and Lusk (2005) found that Empetrum rubrum dominates in early succession in recently deglaciated valleys.

Herbivory
In regard to Empetrum, Tybirk et al. (2000) stated "few animals are associated with the species and herbivory is generally low." As noted below, this is accurate for herbivory in general, but an appreciable range of species consume the berries, albeit most of the standing crop often survives uneaten.
The foliage of evergreen shrubs of the Ericaceae, such as Empetrum, frequently accumulates high concentrations of tannins and other phenolics, toxic tripterpenes, and other unpalatable components, and so herbivores generally avoid consuming the vegetative shoots of these shrubs (Christie et al., 2015). Accordingly, when the plants are not in fruit, vertebrate herbivores are substantially absent from heathlands with  Bell and Tallis (1973) reported that in Great Britain the vegetative parts of Empetrum are not grazed by deer or domesticated sheep but are eaten by ptarmigan and grouse. Mendoza et al. (2011) indicated that the dominant economic activity in the Magellanic steppe over the last century is sheep rearing for wool production. However, Collantes et al. (1999) andFernández Pepi et al. (2012) observed that sheep grazing has degraded these grasslands leading to a land dominated by E. rubrum and other acidophilic shrubs of little value for sheep production. In North America, caribou consume some woody plants, including Empetrum, in their varied diet, although crowberry is not considered a preferred forage (Matthews, 1992;Pamela, 2011). A survey among reindeer herders of northern Sweden suggested that reindeer fairly regularly graze Empetrum overwinter (Inga & Danell, 2012). Although the phenolics in the foliage strongly discourage insects, Empetrum is the food plant of several Lepidopteran species, such as Sympistis helioptera and Pygmaena fusca (Sepponen, 1970).
In general, grazing in mesic tundra heaths is known to increase the abundance of grasses at the expense of dwarf shrubs (Olofsson et al., 2001(Olofsson et al., , 2004. Grazing by large herbivores can have a marked influence on the growth of Empetrum, not so much from the loss of material but because the plant is very sensitive to trampling (Dalby, 1961;Tybirk et al., 2000). Physical disturbance during reindeer migration may prevent crowberry dominance in the vegetation under a heavy grazing regime (Väisänen et al., 2013). However, reindeer may benefit evegreen dwarf shrubs like Empetrum by preferentially grazing on deciduous shrubs (Vowles et al., 2017). Indeed, there is evidence that reindeer are, on the whole, significantly benefical to Empetrum (Bråthen et al., 2018).
Empetrum fruits are eaten by a wide diversity of birds (Fig. 18) and mammals. Perhaps most memorably, the extinct passenger pigeon (Ectopistes migratorius) was a consumer; as noted by Forbush et al. (1912) "In Labrador they gathered to feed on the wild berries, chief of which was the Empetrum nigrum, called curlewberry or gallowberry by the natives, but generally known as the crowberry." Migrating geese (Branta hutchinsii taverneri) were observed to eat 30-60% of the annual crowberry production on the Alaska Peninsula in the fall (Hupp et al., 2013). Empetrum and Vaccinium berries furnish Canada geese (Branta canadensis) much of the calories required for pre-migratory fat deposition and constitute over 40% of their diet in late summer (Sedinger & Raveling, 1984;Cadieux et al., 2005). Guitian et al. (1994) found that redwings (Turdus iliacus) on the coast of Iceland grazed heavily on crowberries. Matthews (1992) noted that the berries are especially important to grouse and ptarmigan. Nechaev and Nechaev (2018) recorded 60 species of birds feeding on Empetrum in the southern Russian Far East. In southern Yukon, Krebs et al. (2010) found that voles (particularly the red-backed vole, Myodes [Clethrionomys] rutilus), rely heavily on Empetrum berries as a main source of food in winter, and Callaghan and Emanuelsson (1985) stated that Empetrum is controlled by the grazing of voles (Microtus spp. and Clethrionomus rufocanus) and lemmings. Caribou (in North America) are not thought to significantly consume the berries (Boulanger-Lapointe, 2017) but reindeer (in Scandinavia) have been noted eating the fruit (Bråthen et al., 2007). Black bear occasionally consume crowberries in the Pelly River Valley, Yukon, Canada (MacHutchon, 1989). Boulanger-Lapointe (2017) examined berry seeds in feces in the region of Arviat Nunavut (on the western shore of Hudson Bay, about 200 km north of Churchill, Manitoba). Her study showed that the net annual production of berries in a 45.5 km 2 region surrounding the community was 400 g m -2 , with Empetrum accounting for the majority (90%) of the production. However, her analysis of the animal droppings for berry seeds indicated very low consumption of the total production by herbivores, particularly by snow geese and hares, which only ate about 2% of the available berries.
In conservation planting (i.e. establishing vegetation for the benefit of wildlife), Empetrum is of notable value to the diet of birds, including songbirds, waterfowl, grouse and ptarmigan (Huxley et al., 1992).
Perennial crops, particularly deciduous fruiting tree species, commonly exhibit cycles of high (mast years) and low fruit productivity. This is often interpreted as a "predator satiation" strategy to prevent frugivores from building up large populations that could seriously damage the survival of the trees, although weather conditions are also hypothesized as causes (Kelly & Sork, 2002). Such masting is known to occur in dwarf shrubs, including ericaceous species (Vander Kloet & Cabilio, 1996). Ericaceous shrubs appear to have their own internal cycle that is dependent upon the previous year's production (Krebs et al., 2009). Krebs et al. (2009) found that Empetrum berry counts in the boreal forest of the southwestern Yukon are heavily influenced by spring rainfall 2 years prior.

Allelopathy
Although the phenomenon of allelopathy can include beneficial influences, in reference to plants it usually designates the harmful effects of chemicals released into the Fig. 18 Birds on crowberry. a Whimbrel (Numenius phaeopus) feeding on Empetrum nigrum. Source: Alamy Limited. b Rock ptarmigan (Lagopus muta) adult male standing on Empetrum nigrum in May, Cairngorms National Park, Highlands, Scotland. Source: Alamy Limited. c Snow bunting (Plectrophenax nivalis) eating a crowberry in Flatrock, Newfoundland. Photo by Judith A Blakeley, reproduced with permission. d Goldencrowned sparrow (Zonotrichia atricapilla) on a crowberry stand. Photo (public domain) by Jacob W. Frank, U.S. National Park Service, Alaska Region environment by one plant on the germination, growth, survival, and/or reproduction of another (usually competitive) plant (Kamal, 2020). Such allelopathy is a form of interspecific chemical warfare, and it appears to be vitally important to the success of Empetrum.
As noted earlier, the leaves of Empetrum bear gland-tipped trichomes, and these synthesize a variety of chemicals (Muravnik & Shavarda, 2012). The most significant of these is batasin-III (3,3'-dihydroxy-5-methoxybibenzyl), a phenolic compound of the class dihydrostilbene produced by Empetrum and thought to be an allelochemical contributing to the success of Empetrum in dominating extensive ecosystems (Wardle et al., 1998;González et al., 2015). Batasin-III, which is water soluble, in addition to other secondary chemicals, is released from Empetrum's leaves and litter by rain, dew, and snowmelt (Odén et al., 1992;Nilsson et al., 1998;Gallet et al., 1999). The chemical has been shown to be allelopathic against seed germination of European aspen (Populus tremula L.) and Scots pine (Pinus silvestris L.) , and to harm seedling growth of Scots pine Nilsson et al., 1998;Nilsson, 1994). Also negatively affected are seed germination and seedling growth of several graminoid species (Bråthen et al., 2010). Batasin-III is easily washed away in mineral substrates, but is retained well in organic soils such as generated by Empetrum (González et al., 2015). Brännäs et al. (2004) found that batatasin-III washed from Empetrum into small streams can be lethal to aquatic fauna. The ability of Empetrum to employ batasin-III as a suppressant of other plants has been found to be reduced by disturbance and by deposition of excrement by animals (Bråthen et al., 2010).
The mechanisms of suppression of batasin-III and other secondary chemicals requires clarification. Wardle et al. (1998) found that these compounds form recalcitrant complexes with soil organic matter, reducing nitrogen availability to vascular plants (Wardle et al., 1998). Nilsson et al., 1993) observed that the chemicals have negative effect on mycorrhizal symbiosis of coniferous trees. Additionally, the humus under Empetrum becomes extremely unfavorable for microbial activity, drastically reducing decomposition rates and nutrient cycles to the detriment of plants unable to grow well under such conditions (Wardle & Lavelle, 1997;Nilsson & Wardle, 2005).

Traditional indigenous consumption of edible fruits of northern dwarf shrubs
Indigenous peoples all over the world and throughout history have exploited plants like Empetrum for various purposes, and depending on local abundance and ingenuity, the modern world has inherited a legacy of practical knowledge. Empetrum is mostly distributed from the boreal forest region through the Subarctic to the Arctic, and becomes progressively important northward for human food as fewer and fewer plant species are able to tolerate the harsher environment. In the Arctic, in addition to Empetrum (and particularly in North America), at least five other dwarf shrubs are especially significant sources of wild harvested fruit: Arctous alpina (L.) Nied. (torpedoberry, black bearberry, alpine bearberry); Arctous rubra (Rehder & E. H. Wilson) Nakai (red bearberry); Vaccinium uliginosum L. (bog bilberry, bog blueberry, northern bilberry, western blueberry); Vaccinium vitis-idaea L. (lingonberry, northern mountain cranberry); and Rubus chamaemorus L. (cloudberry, baked apple berry, bakeapple). All except R. chamaemorus (Rosaceae) are members of the Ericaceae, a family which clearly possesses exceptional adaptation to the cold short-season northern environment. In recent times in northern communities of Alaska, annual harvest of berries has been estimated to range from 6 L to 24 L/household per species (Murray et al., 2005). As stated by Porsild (1953), crowberry has been the most important wild fruit consumed by indigenous peoples of Arctic regions.

Traditional indigenous consumption of crowberries
Empetrum berries were often a staple food for northern peoples, but were also consumed simply to slake thirst (Small, 2013). Kuhnlein and Turner (1991) reported that the fruits were eaten raw or cooked by several North American indigenous groups, including Ojibwa, Slave and other Déné, Chipewyan, Cree, Carrier, Haida and Tsimshian, as well as the Inuit of northern Canada, the Inupiaq, and other Eskimo peoples of Alaska. These berries were mixed with bear grease, cooked and mashed, and dried in the sun in cakes. The Inupiaq Eskimo, ate them or mixed them with cloudberries, Vaccinium or other fruits, Arctic dock (Rumex arcticus Trautv.), or with oil and sugar, with whipped fat, or fish livers. Mixed whole with greens and other berries and seal oil, they were stored in airtight container such as a sealskin poke (storage bag) (Heller, 1976;Jones, 2010). Another storage method consisted of "making a hole in the sand, pouring some fat in it, waiting for it to dry and once dried, fresh berries were placed on it and covered with a seal skin then buried for the winter supply" (Ootoova et al., 2011). Fresh berries were also mixed with dwarf fireweed (Chamerion latifolium (L.) Holub.), oil, and blood and consumed raw (Ootoova et al., 2011). Additional food uses by various indigenous communities are recorded by Moerman (1986Moerman ( , 1998. In modern times, crowberries continue to be harvested for food by indigenous people (Fig. 19). In the North American Arctic, berry collection continues to be important to indigenous communities, especially the Inuit, not just for food but also as a community-reinforcing cultural heritage that contributes to mental health (Desrosiers, 2017;Boulanger-Lapointe et al., 2019).
In subarctic areas, native people commonly used the natural refrigeration provided by the climate to preserve foods overwinter. Since crowberries ripen in August and Fig. 19 Indigenous women harvesting crowberries. Photos © Robert Fréchette, Avataq Cultural Institute, reproduced with permission remain on the plant through the winter, they were available fresh or frozen into the early spring, and could be collected through winter from under the snow. When harvested in the fall, they were frequently mixed with other berries or greens, and meat, fish, seal oil, blubber, or fat, for storage in the frozen ground until required. "Eskimo ice cream" (ahkootuk, akutaq, akutq) is a combination of fish or meat fat (commonly moose, reindeer, caribou, or seal oil) and berries (often crowberries).
Crowberries have been used in Arctic areas to prepare wine. Centuries ago in Norway the crowberry was named drunken berry or inebriating berry as it was used to make wine (Rätsch, 1998). Also long ago, Rink (1857) wrote that a sparkling white wine was produced by fermentation of crowberry juice in Greenland. Aiken et al. (2007) recorded that crowberries were used to make wine in Iqaluit.

Contemporary food applications
The berries of Empetrum are quite juicy or watery, acidic, and taste best after a frost (Schofield, 2003). They are often described as mild in flavor (at least after exposure to frost) in books for wild-food enthusiasts (e.g. Schofield, 2003). Less complimentary, Jurikova et al. (2016) stated "the fresh fruits are sometimes classified as inedible in botanical literature. This is due to the high content of tannins that are responsible for the raw fruits' taste. They are slightly acidic, bitter and astringent." USDA Natural Resources Conservation Service (2006) commented "Raw berries are small, mealy and often considered tasteless when eaten alone." Bitterness and astringency of crowberries are due particularly to eight flavonol glycosides and two flavonol aglycones (Laaksonen et al., 2011). The hard seeds are large enough (1.6-2.5 mm long) that some people would find their crunchiness annoying, but they can easily be strained away. "Crowberries have many small seeds and a tough skin, which makes them unsuitable for drying" (van Delden, 2011; nevertheless, commercially dried fruits are marketed). Crowberries are often collected from the wild for local household usage. Van Delden (2011) provides a guide for personal collecting, preparing, and storing. Indigenous people and wild food enthusiasts harvest large amounts. The fruits can be eaten raw or cooked as confections such as pies, muffins, pancake, jelly, tea, and juice (Fig 20). Because the berries are mild in taste, they are generally combined with more flavorful berries in recipes.
Crowberries are also collected by the beverage and food industries for incorporation into commercial products. They are employed commercially to prepare beer, wine, and liquor, usually as one of a mixture of flavoring agents (Fig. 21). The berries have been used as color enhancers in food products, particularly juices and wines (Rein, 2005). They are also employed commercially to nutritionally fortify other juices (Törrönen et al., 2012).

Nutritional value
Like most berries, crowberries have been found to be rich in vitamins and minerals (Kuhnlein & Turner, 1991;Lacramioara & Ciprian, 2016;Canadian Nutrient File, 2018). We do not cite chemical analyses because, as noted by Nestby et al. (2019), "values reported in different studies may not be directly comparable, because they are biased by the time of harvest, cultivar and local and regional conditions." Since such conditions can profoundly affect the phytochemical composition of fruits, the effects of climate change on the nutritional quality of wild berries is a concern (Kellogg et al., 2010).
In recent decades in affluent nations, there has been widespread concern about degeneration of health due to overabundant consumption of nutritionally questionable foods. A prominent resulting trend has been the growing popularity of "super-fruits" such as cranberries and blueberries, rich in phytochemicals thought to be protective against diseases. In particular, antioxidant phenolic constituents of such berries have acquired reputations as potentially effective against a wide variety of conditions, notably cardiovascular and neurogenerative diseases, obesity, diabetes, and even cancer. There is laboratory and clinical evidence validating many of the health claims  (Kellogg et al., 2011), but marketing campaigns have perhaps been more persuasive, as essentially the same phytochemicals can be obtained much more cheaply from various conventional fruits. "Market exoticism" is the phenomenon of appealing to consumers' sense that there are amazing previously unknown commodities with wonderful properties, and this tactic largely accounts for the recent success of açaí berries and goji berries. The possibility exists that even a fruit like crowberry that has been largely a marginal, subsistence food to date could be transformed into a new marketing success.
The subarctic and arctic region have few food plants, and most of these provide fairly low food energy for human use. In past times, when indigenous people, settlers, and explorers needed to live off the land, essential vitamins from plants would have contributed significantly to health and nutrition. In modern times, when overnutrition is the predominant health issue, re-adoption of traditional northern diets that included berries like Empetrum, offers the prospect of better health.
The Haida people believed that eating too many berries could cause haemorrhaging (Kuhnlein & Turner, 1991) or constipation (Ootoova et al., 2011;Aiken et al., 2007), but this may simply be reminiscent of the warning that children receive about overeating. Crowberries are rich in tannins (Jurikova et al., 2016), and possibly excessive consumption could lead to digestive problems.

Modern medicinal research
Berry fruits in general have health-promoting constituents (Nestby et al., 2019), and there are numerous chemical analyses of such compounds in Empetrum, including phenolic compounds (anthocyanins, flavonols, flavan-3-ols, phenolic acids, proanthocyanidins and ellagitannins) and abscisic acid derivatives, (Bukharov & Karneeva, 1970;Vasilets et al., 1988;Ogawa et al., 2008;Koskela et al., 2010;Park & Lee, 2013;Dudonné et al., 2016;Juríková et al., 2020). Also, numerous studies (usually with experimental animals) have been conducted in relation to specific physiological or disease conditions that may benefit from Empetrum constituents. Examples follow. Hach (1936) examined several northern berries for vitamin C content, but favored other species than crowberry for antiscorbutic use. An extract from Empetrum was discovered to protect cells against oxidation damage, to have anti-inflammatory and anticancer activity, and to benefit lipid metabolism (Kim et al., 2009;Jurikova et al., 2016). Park et al. (2012) suggested that Empetrum might be useful for the development of functional foods based on antioxidants which prevent stressrelated diseases like atherosclerosis. Hyun et al. (2018) suggested that crowberry fruits could serve as potential antioxidant and antidiabetic supplements. Bae et al. (2016) found that extracts of crowberry inhibited angiogenesis (formation of new blood vessels) indicating that the plant may have potential applications in the prevention and treatment of angiogenesis-dependent human diseases. Matsuura et al. (1995) characterize antibacterial and antifungal compounds in Empetrum. McCutcheon et al. (1997) reported that Empetrum extracts were antibiotic against the tuberculosis bacterium (Moerman, 1986 noted that indigenous peoples employed Empetrum as a treatment for tuberculosis). Empetrum contains high level of an anticonvulsive compound labelled empetrin, of potential significance for treating epilepsy (Saratikov et al., 1991;Ermilova et al., 2001;Muravnik & Shavarda, 2012). Kochkin et al. (2017) observed that laboratory rats treated with an extract of crowberry for an extended period adapt faster to stress caused by general hypothermia. Plaksen et al. (2019) demonstrated the effectiveness of juice and oil meal of Empetrum nigrum fruits in the prevention of osteoporosis. Crowberry extracts have significant potential as healthful ingredients for cosmetics (Roberts et al., 2019;Fig. 22).

Ornamental uses
Empetrum can be grown as an urban landscape ground cover and as an ornamental plant in rock gardens (Finn, 2008). As noted earlier, development from seeds is extremely slow, so most gardeners prefer to purchase established stock in containers. There has been selection of forms with ornamental value, and these are available in the c Crowberry night cream. Photo courtesy of Ecouna (Sweden). All photos reproduced with permission horticultural trade. Notable cultivars include 'Bernstein' and the yellow-foliaged 'Lucia' (Fig. 23).
Empetrum ornamental cultivars are selected clones, some of which develop few if any seeds, and so to propagate these efficiently there has been appreciable research carried out on how to reproduce them by cuttings. Propagation with softwood or hardwood cuttings is effective (Huxley et al., 1992;Sheat, 1948;Turner, 2012). Hagen (2002) achieved over 70% establishment of cuttings of Empetrum. Leafy stem cuttings taken in mid-summer root rapidly in peat, but plants will not regenerate from root cuttings or prostrate leafless stems (USDA Natural Resources Conservation Service, 2006).

Ground cover for land reclamation
Empetrum has potential for land reclamation (Kershaw & Kershaw, 1987). It has been observed naturally colonizing borrow pits (sites excavated for construction material) in the tundra regions of northwestern Canada, reflecting its adaptation to cold, short-season sites with infertile, frozen soils (Famous & Spencer, 1989). It also has spontaneously recovered in mined peatlands in North America, a situation requiring tolerance to quite infertile substrates (Famous & Spencer, 1989). The species has been used as ground cover in rough, bumpy low areas in interior Alaska, a habitat that a laterally spreading low shrub like Empetrum is adapted to utilize (Viereck & Little, 1972). Its interlocking roots can help stabilize steep and rocky slopes, and its dense leafy mats catch blowing soils in areas of high wind exposure (Matthews, 1992). However, Empetrum colonizes slowly and is not competitive in many circumstances, so that research would be necessary to establish appropriate circumstances for which it is suited.

Economic and agricultural potential
The need for development To date, agriculture in the northern world has been considered to be a marginal activity, difficult to justify economically, and so necessitating importation of considerable Fig. 23 Empetrum cultivars. a 'Bernstein', a cultivar that develops orange-red foliage. Photo credit: Baumschule Hachmann (Germany), reproduced with permission. b 'Lucia', a cultivar with yellow foliage growing at botanical garden Ban-de-Sapt, France. Photo credit: Christian Amet (CC BY SA 3.0) amounts of food, especially fruits and vegetables, from southern locations at considerable expense. Unfortunatelly, this has resulted in alarming food insecurity, poor diets, and health problems (Huet et al., 2012). Northern ecosystems are rapidly changing, along with the food needs of Arctic and sub-Arctic communities which have long depended on local wild harvested foods. Crowberry is a premier wild fruit resource in the Far North, and as such deserves serious consideration for future development as a crop. Kellogg et al. (2011) observed: "Economic development is a pressing issue for many North American indigenous tribes. Despite fluctuating levels of government support throughout the twentieth century, the socio-economic status of the indigenous people has stagnated, culminating in a state of chronic economic underdevelopment… High rates of poverty and unemployment have exacerbated social problems, including domestic violence, alcoholism and substance abuse, health issues and depression… efforts to create culturally congruent development projects (such as local floral commodities, crafts, ecotourism and indigenous wild food products) can bolster economic development within underdeveloped natural areas while simultaneously maintaining their value as wilderness and preserving biodiversity." Technological alternatives for the development of Crowberry are examined in the following.

Wildcrafting
Although most food plants today are cultivated, wild plants represent a sustainable resource that is generally underexploited (Shelef et al., 2017). Crowberry is harvested in considerable amounts from wild stands, and mostly consumed locally, but it is also sold commercially in northern climates, and used in some marketed blended juices (Small, 2013). In Finland, crowberry is the third largest wild berry crop after lingonberry (Vaccinium vitis-idaea L.) and bilberry (Vaccinium myrtillus L.) (Laaksonen et al., 2011). Nevertheless, crowberries are underutilized.
Wild northern berry shrubs constitute a massive potential food resource for both humans and wild animals, and as noted in this review, Empetrum is one of the most harvested plants. Curiously, however, it has been observed that much of the fruit production goes unharvestedeither by people or other animals. In Nordic forests, 90-95% of the wild berry crop remains and degenerates on the plants (Nestby et al., 2019). Boulanger-Lapointe (2017) pointed out that there is considerable availability of crowberries for exploitation throughout the Arctic, most of which is not collected. However, harvesting wild berries is, comparatively, a low-value activity, and is only worthwhile if the resource is near where people live and work, as transportation costs to distant sites would be prohibitive. For the Canadian Arctic, a particularly valuable guide to the relative abundance of crowberry near population sites is provided by Boulanger-Lapointe (2017; available online; see her Fig. 4.4). Arctic Flavours Association (2014) present a guide to responsible picking of wild berries in Finland. Stanek and Butcher (2007) and Gray (2011) are guides to Arctic berries of North America.
Indigenous people have relied on wild plants for centuries if not for millennia, and to this day often retain unique cultural ownership of these resources, regardless of whether the plants are on private or public lands. By contrast, many non-native harvesters and much of the business community are profit-oriented, and do not necessarily share the same concerns regarding ecological sustainability or social aspects. Commercialization can lead to overharvesting and degradation of the wild supply, and loss of control of management by native groups. Native tribes may be philosophically opposed to all commercial development on their lands, and might decline to participate in profitmaking ventures exploiting any wild resources. Kellogg et al. (2011) noted that "in Native American/Alaska Native lifestyles for generations… historical traditions typically dictate community ownership of the wild indigenous berries." In Arctic North America there is a tradition among some indigenous peoples of refusing to harvest berries such as Empetrum for sale as such practices interfere with traditional food sharing systems (Murray et al., 2005;Karst & Turner, 2011;Searles, 2016;Boulanger-Lapointe et al., 2019).
Professional wild berry collectors may pick the fruit with their bare hands, but often employ 'berry-picking hand rakes" or "berry pickers" (small hand-held harvesters, typically made of plastic; Fig. 24). Røthe et al. (2004) reported that berry hand rakes are more efficient, but can collect crowberries of uneven ripeness. However, Manninen and Peltola (2013) found a variety of small and large rakes efficiently collected crowberries without significantly damaging either the berries or the plants. The conventional orchard fruits are often harvested with specially designed machinery, but such technology seems unlikely to be available for wild fruits, which are traditionally harvested by hand. Such work does have the advantage of providing employment for regions that are remote from the more populated areas.
Semi-cultivation (management of wild resources) Kellogg et al. (2011) expressed doubt that agricultural attempts to improve productivity of Arctic berries have appreciable prospects. However, Nestby et al. (2019) reviewed the potential of four dwarf shrub Vaccinium species and Empetrum, and commented "Semi-cultivation in the natural habitat is probably the best solution for viable and sustainable commercial exploitation… these species are easily propagated by fresh Fig. 24 Hand rakes ("berry pickers"). a A 19 th century berry hand rake made specifically for harvesting crowberries. Source (public domain): Schübeler (1873). b Indigenous woman harvesting berries in Alaska employing a hand picker. Public domain photo, U.S. National Park Service. Credit: Maija Lukin cuttings, and they can grow on arable land, adapting soil conditions to fit their growing preferences. Such cultivation, to our knowledge has not yet been performed on a large economic scale." Crowberry has the potential of being environmentally managed in the same manner as the North American lowbush blueberry (Vaccinium angustifolium). Natural stands of this species are provided with fertilization, weeding, herbicides, irrigation, pollination, and pruning to increase productivity (Yarborough, 2004). Initial experiments in fertilizing natural stands (Hylgaard & Liddle, 1981;Monni et al., 2001b) or irrigating (Shevtsova et al., 1997) Empetrum did not produce significant improvements, although Shevtsova et al. (2005) reported a more positive reaction to fertilization. USDA Natural Resources Conservation Service (2006) provides general recommendation on managing wild berries, including Empetrum, in Alaska. Although semi-cultivation of a wild plant like Empetrum is very challenging, such development of local indigenous species has the potential to be carried out in ecologically sustainable ways (Balestrini et al., 2015;Hawkes et al., 2007;Provenza et al., 2015).

Domestication
English philosopher Francis Bacon (1561-1626) stated that "acorns were good until bread was found," which roughly translates to saying that wild plant foods cannot compete with domesticated crops in modern society. There are already more domesticated fruit species than any other class of food crop, making it difficult for additional entries to be added to the marketplace. Also, the wild supply of Empetrum is considerable, so that deliberately cultivating the plant to obtain the berries may seem unnecessary. However, this is misleading since most of the supply is not practically accessible. An additional limitation is that outside of the natural geographical range, it can be difficult to supply the soil and climate conditions that are appropriate, and other berry crops are already much more competitive (Small, 2013). Nevertheless, the potential exists for selection of clones with desireable agronomic characteristics, especially for fruit quality and productivity, but also for adaptation to local environments. There has already been selection of ornamental cultivars, so that there is some technology available to transform Empetrum into a domesticated fruit crop. As noted earlier, there is a dearth of collected germplasm for this exercise, but there is considerable genetic variation available in nature. Both the tetraploid monoecious forms (socalled subsp. hermaphroditum) and diploid dioecious forms (so-called subsp. nigrum) have potential applicationsplants of the former always have flowers and fruits, but some dioecious crops are deliberately raised with just enough male plants to fertilize the much more numerous planted female plants (e.g. in date plantations, only one male tree is required for every 50 female trees).
In suggesting the possibility of developing crowberry as a new domesticated crop, we note that high-input cultivation of the world's major crops, while indispensable for feeding the world, is associated with great damage to the environment, biodiversity, and human health. Both traditional and potential new crops need to be managed in more sustainable ways (Horrigan et al., 2002;Massy, 2017).
An additional issue pointed out by one of the reviewers of this paper is that should superior crowberry cultivars be created, these would likely be grown primarily at lower latitudes, where yields would inevitably be higher. The southern harvest would then be in potential competition with the higher latitude crop, depriving northern indigenous people from benefiting from their local wild resource. This possible development is illustrated by wild rice (Zizania species), which a half century ago was collected almost entirely from wild North American plants by indigenous people. Currently, 95% of the world supply comes from domesticated cultivars grown in California (Small, 2013).

Economic overview
The crowberry genus Empetrum is one of the world's most widespread species, but as an occupant primarily of the coldest and least populated regions of the planet, it has attracted limited economic attention. Aside from its importance as a keystone species regulating the success of many ecosystems, Empetrum offers the prospect of significantly increasing the food production of the northern world, where crops are extremely limited. Moreover, crowberries have exceptional content of phenolic compounds with potential for nutritional supplements and medicinal applications. With impending climate change representing both a threat and a benefit to the future development of Empetrum, it is important to address botanical and ecological issues that remain to be clarified. Insofar as the crowberry has been a specialty of Indigenous Peoples of the North, their unique knowledge and claim to its future development need to be respected.