Introduction

Juniperus is one of most diverse genera of the conifers. Juniperus species are found from sea level (several, J. virginiana var. silicicola, J. taxifolia var. lutchuensis, J. procumbens) to above timberline (J. zanonii). Although limestone is the preferred substrate for many Juniperus species, other taxa grow on sand dunes, granite, and sandstone and range from deserts (J. californica, J. osteosperma) to bogs (J. communis var. charlottensis on Queen Charlotte Island, B.C.). In North America, Juniperus species have become weedy and invaded millions of acres of rangeland and abandoned farms (Adams et al., 1998).

Juniperus species have evolved a fleshy female cone in which the cone scales are fused. These are often called "fruits" or "berries". This reproductive structure is especially consumed by birds and small mammals (Phillips, 1910; McAtee, 1947; Holthuijzen and Sharik, 1985; Santos et al., 1999). In fact, the long distance dispersal by birds has resulted in Juniperus being established on Atlantic islands such as the Azores, Bermuda, the Caribbean and Canary Islands.

The genus Juniperus - Evergreen shrubs or trees. Branchlets terete, 4-6 angled, variously oriented, but not in flattened sprays (except in J. thurifera and occasionally in J. flaccida). Leaves in decussate (alternating) opposite pairs in 4 ranks or in alternating whorls of 3. Adult leaves either acicular (subulate) or closely appressed (scale like) to divergent tips (whip leaves); abaxial gland visible or not, elongate to hemispheric (J. ashei), sometimes exuding white crystalline deposit. Pollen cones with 3-7 pairs or trios of sporophylls, each sporophyll with 2-8 pollen sacs. Seed cones maturing in 1 or 2 years (to 3 yrs. in J. communis), globose to ovoid and berrylike, 3-20 mm (to 25 mm in J. drupacea), remaining closed, often glaucous; scales persistent, 1-5 pairs or whorls of three, peltate or valvate, tightly coalesced and fused together, thick and fleshy or fibrous to obscurely woody; some sweet (e.g. J. pinchotii, J. coahuilensis), many bitter and/or resinous. Seeds 1-3 per scale, round to faceted, wingless; cotyledons 2-6. Seed dispersal by frugivorous birds, that swallow the cones whole, digest the fleshy scales and pass the hard-shelled seeds undamaged through the gut; the bitter taste of many species may be related to discouraging mammalian predators of the seeds. 2n = 22 but reports of tetraploids (4n = 44) in J. chinensis and J. thurifera (Romo et al. (2012).

The phylogenetic position of Juniperus (and Cupressaceae) in the plant kingdom (Fig. 1.1) indicates Juniperus as a terminal clade and as one of the most advanced conifer genera (Rai et al., 2008).

A simplified Bayesian tree with genera collapsed shows (Fig. 1.2) the relationship for Juniperus to Cupressus and Hesperocyparis (adapted from Mao et al., 2010).

The phylogeny of Junipers is depicted in Figure 1.3. The three sections are in well supported clades. Juniperus phoenicea and J. turbinata stand loosely affiliated with sect. Sabina (Fig. 1.3). These taxa have small serrations on the leaf margins, but are denoted as 'pseudoserrate' (Fig. 1.3). It seems unlikely that serrate leaf margins in the eastern and western hemispheres is a homologous character, but has arisen independently as J. phoenicea - J. turbinata is not in the clade with the serrate, semi-arid junipers of the western hemisphere. It is interesting that J. erectopatens and J. microsperma form an unusual clade that does not nest into the J. chinensis clade (Fig. 1.3).

The genus Juniperus is comprised of approx. 75 species in 3 sections: sect Caryocedrus Endlicher, 1847, the type and only species, J. drupacea Labill., syn: genus Arceuthos Antoine, 1854 with large, blue, woody, 3-seeded cones, showing the fusing of 3 cone scales, with an Old World Mediterranean distribution (Fig. 1.3.1), see Adams, 2011, Adams and Schwarzbach, 2012a); sect Juniperus (syn: sect. Oxycedrus Spach, Ann. Sci. Nat. Ser. 2, 16: 288 (1841), 14 species, 12 only in the eastern hemisphere, one endemic to North America (Fig. 1.3.2) and one species, J. communis, being circumboreal, seed cones blue or red, often with 3 seeds (Adams and Schwarzbach, 2012a) and sect Sabina (Miller) Spach, Ann. Sci. Nat. Ser. 2, 16: 291 (1841), sect. Juniperus,. Sabina syn: genus Sabina Miller, 1754 (approx. 60 species), with species about equally divided between the eastern and western hemispheres, seed cones with 1 to 13 seeds, blue, red-copper, rose, or brown (Adams, 2011).

The leaf types in the three sections are shown in Figures 1.3.3.1, 1.3.3.2, and 1.3.3.3: Left: acicular leaf, the only kind of leaves in sections Caryocedrus and Juniperus. Notice the abscission layer (leaf drop) is on the stem (as in the Pinaceae). Center: decurrent leaf, found only in section Sabina. Right: scale-like leaves (adult foliage), present only in sect. Sabina on mature trees (after 3-5 years). The various types of leaves are shown diagrammatically in Figure 1.3.3.4. It should be noted that in section Sabina, some decurrent leaves are always present at the terminal branchlet tips when the foliage is growing fast. Decurrent leaves are the juvenile leaves in section Sabina. After a few years (3-5 years) most species in sect. Sabina, will begin to produce scale-like (adult) leaves (Fig. 1.3.3.3). However, some taxa, such as J. gracilior var. silicicola (Britton and P. Wilson) R. P. Adams, J. coxii A. B. Jacks, J. recurva Buch.-Ham. ex D.Don, J. fargesii (Rehder & Wils.) Kom., and J. morrisonicola Hayata (see Fig. 3.3.5) are frozen in the juvenile leaf state for life (neoteny).

Section Caryocedrus, consisting of one species, J. drupacea, is confined to the region from Greece to Turkey (Fig. 1.3.1) and is considered the most ancestral section of the genus (Adams and Schwarzbach, 2013b). Dioecious. Trees to 30 m or more. Leaves acicular (subulate, jointed at the base, Fig. 1.3), broad (2-3.5 mm wide); 10-25 mm long. Scale-leaves absent. Cones axillary on shoot, female cones 18 - 25 mm at maturity with 3 cone scales visible (see Fig. 1.3.3.1), three seeds fused together to make a drupe, female cones mature in 18 mos. to 2 years.

Section Caryocedrus has been treated as a separate genus (Arceuthos, Florin, 1963). But the inclusion of Caryocedrus into Juniperus has been confirmed with DNA sequence data (see Fig. 1.3). There is no support for the recognition of the genus Arceuthos using DNA sequence data. It is interesting that section Juniperus is separated by seed cone morphology and geography. All these species of sections Caryocedrus and Juniperus have acicular (subulate) leaves.

Section Sabina is divided into three major clades (Mao et al., 2010, Adams and Schwarzbach, 2013a):

1. Serrate-leaf junipers of North America (21 species, Adams and Schwarzbach, 2011, 2013d),

2. Turbinate-seed cones, single-seeded, entire-leaf junipers, eastern hemisphere (16 species, Adams and Schwarzbach, 2012b, 2013a, Zanoni and Adams, 1976, 1979) and

3. Multi-seeded, entire-leaf junipers, both eastern and western hemispheres (23 species, Adams and Schwarzbach, 2012c, 2013b).

Mao et al. (2010) used three Juniperus fossil dates: J. pauli (ca. ≥ 33.0 mya, cf. extant J. sabina and allies), J. creedensis (ca. ≥ 23.0 mya, cf. J. californica / J. osteosperma), and J. desatoyana (ca. ≥ 16.0 mya, cf. J. occidentalis / J. osteosperma). They postulated the serrate, semi-arid junipers migrated from the eastern to the western hemisphere via the North American Land Bridge (NALB) ca. 47 - 30.3 mya (Fig. 1.4).

The fossil J. creedensis of the Creede geoflora (ca. ≥ 23.0 mya) bears a striking resemblance to present-day J. californica (Fig. 1.5). Because the present-day J. californica appears little changed from the fossil, J. creedensis, it may be that the serrate junipers in North America are much older than thought. It might be noted that Axelrod (1987) described a second juniper from the Creede geoflora as J. gracillensis that he thought was similar to extant J. flaccida, but Wolfe and Schorn (1990) have identified the specimen as Eleopoldia lipmanii (Rosaceae).

The Madrean-Tethyan vegetation belts in Eurasia and North America may have been continuous during the Eocene and Oligocene (Axelrod, 1975; Wen and Ickert-Bond, 2009), such that Juniperus section Sabina might have had a wider distribution (Fig. 1.6). So it is possible that the serrateleaf junipers may have existed in the Madrean-Tethyan vegetation belts in both Eurasia and North America during the same period (Fig. 1.6), and there may have been exchanges via the North Atlantic Land Bridge (NALB). Although the Madrean-Tethyan vegetation, depicted in Figure 1.6, predates the ages of any known juniper fossils, because only a few Juniperus fossils are known, older fossils likely exist.

It is unfortunate that the serrate-leaf species (J. phoenicea, J. turbinata) that are extant in the eastern hemisphere, have DNA so different that they are poorly grouped with any clade (Fig. 1.3). It is quite removed from the serrate junipers clade (Fig. 1.3). At present, it seems appropriate to consider J. phoenicea and J. turbinata as 'pseudoserrate' and of a different lineage than the serrate junipers of North America. If the serrate leaves of J. phoenicea/ J. turbinata are not homologous to the serrate leaves of junipers in North America, then we are left with no extant (or known fossils) of truly serrate junipers in the eastern hemisphere.

The migration of the smooth leaf members of sect. Sabina to the western hemisphere is thought to be more recent (17.6-5.5 mya, Mao et al., 2010) and those dates are younger than the fossil J. creedensis of the Creede geoflora (Axelrod, 1987). Since J. phoenicea/ J. turbinata do not appear to be true members of the serrate junipers and no serrate juniper fossils have been found in the eastern hemisphere, the serrate junipers may be endemic to the western hemisphere. Undoubtedly, additional fossils will be found some day to help resolve the question.

Mao et al. (2010) argues that the movement of sect. Sabina to the western hemisphere (17.6-5.5 mya) is too young for migration across the North Atlantic Land Bridge (NALB), but possible via the Bering Land Bridge (BLB). Because sect. Sabina species such as J. sabina and J. davurica are quite cold adapted; they (or an ancestor) could have migrated to produce the ancestors that gave rise to the current, cold climate, western hemisphere species such as J. horizontalis and J. scopulorum. Juniperus davurica is the northeastern-most species in northeast Asia (in sect. Sabina) and could have provided ancestral stock to migrate across the Bering Land Bridge (Fig. 1.7). Notice that J. davurica / J. sabina are in a sister clade to the smooth-leaf juniper of North America (Fig. 1.3), supporting the concept of migration from northeastern Asia via the BLB (Fig. 1.7.)

The North America communis group is equally linked (Fig. 1.11.2) between the Japan and Europe-Central Asia groups. Thus, the linkage map gives equal support to the Bering Land Bridge and North Atlantic island hopping model for the origin of J. communis in North America. The situation was previously more unclear when J. jackii was included in J. communis (J. c. var. jackii). However, J. jackii is clearly quite differentiated (20 MEs from J. mairei, Gansu, China; 21 MEs from J. c. var. megistocarpa, NA and Fig. 1.11.2), but the data is equivocal as to whether its origin is from the BLB or North Atlantic island-hopping model. Juniperus jackii grows on serpentine and volcanic basalt of quite recent origin in the Cascade Range of western Oregon/ northern California (but occasionally on granite in the Trinity Alps, CA).

A diagrammatic representation of the possible migrations of J. communis (and J. jackii) is shown in Figure 1.8. The migration dates proposed by Mao et al. (2010) seem consistent with the recent habitat availability for J. jackii and support the observed lack of differentiation among morphological varieties of J. communis (Adams and Schwarzbach, 2012a).

Wen and Ickert-Bond (2009) summarized data from 17 studies concerning Madrean-Tethyan disjunctions. Their summaries are useful in the present discussion. They concluded (Fig. 1.9) that: 53% of the inter-continental migrations was by the North Atlantic Land Bridge; 40% was by long distance dispersal and 7% by the Bering Land Bridge (BLB). Their summary of the directional data indicated the origins as: 86% from eastern to western hemisphere; 7% from western to eastern hemisphere and for 7% the direction was uncertain (Fig. 1.9).

Section Juniperus (= section Oxycedrus of other treatments, type species J. communis L.). Trees or shrubs, Dioecious (male and female cones on different plants); Leaves acicular (subulate, Fig. 1.3.3.2) as in section Caryocedrus, with a basal abscission area, in whorls of three. Both seed and pollen cones axillary on shoot, on a very short 0.3-1 mm peduncle (appearing sessile); Mature seed cones, 6-15 mm, scales valvate in 1(-2) whorls of three, usually 3 - seeded, but seeds not fused together; mature in 2 (-3) years. Eleven species are recognized in this treatment.

Section Juniperus can be divided into 2 groups (Fig. 1.10): a northern (and far eastern) group associated with J. communis with blue or blue-black mature seed cones and one stomatal band on the adaxial leaf surface; and the J. oxycedrus allies of the Mediterranean region that have 2 stomatal bands and red, red-copper, reddish-brown to reddish-purple mature seed cones.

The phylogeny of Juniperus sect. Juniperus is shown figure 1.10. The varieties of J. communis are not well resolved, which indicates the closeness of this group.

The red colored seed cone species occur around the Mediterranean. The DNA sequence data (Adams and Schwarzbach, 2012a) support the recognition of several species: J. navicularis, J. brevifolia, J. deltoides, J. cedrus, J. maderensis, J. oxycedrus and J. macrocarpa in this group (Fig. 11.1).

Table 1.2. shows the support from DNA sequencing for various species and varieties in section Juniperus. It might be noted that not every case is concordant between DNA data, morphology, ecology and secondary plant chemistry. No doubt, the reality of species delimitation will be better understood in the future.

Juniperus communis is an interesting taxon in that it is the most weedy (invasive) species in sect. Juniperus. Its seed cones are especially juicy and attractive to birds. It is found in disturbed habitats as an invasive weed in Hungary and central Europe as well as in North America (as J. c. var. depressa). Juniperus communis and J. c. var. depressa form a boreal distribution in the higher latitudes around the northern hemispheres. Adams and Schwarzbach (2012a) examined the taxonomy of J. communis and found it to be very complex. The species is comprised of several morphological varieties that are closely linked and separated by only a few mutations (Fig. 1.11.2). Notice the Kamchatka group (Fig. 1.11.2) is closely linked (6 mutational events, MEs) to J. communis var. nipponica, Japan, thence to J. c. var. megistocarpa (NA, 5 MEs).

Section Sabina (type species J. sabina L.), Trees or shrubs, Dioecious or rarely monoecious species; Leaves not acicular (subulate) but decurrent (with a blade that may be appressed to the stem or free), and a sheath that clasps the stem. Leaves on juvenile plants (or the tips of rapidly growing shoots) are composed of only whip leaves (decurrent leaves with the tips free); occasionally, an adult tree may have only juvenile leaves. Some species have only juvenile leaves (J. carinata, J. coxii, J. morrisonicola, J. pingii, J. procumbens, J. recurva, J. gracilior var. saxicola, J. squamata). Leaves are without an abscission zone, decurrent (in pairs) or whorls of 3. Most species have only scale-like leaves on adult foliage (except at growing tips) as seen in figure 1.3.3.3.