Primario

Many people, including some scientists, in Western countries tend to think first of conifers as resin producers among the plants living today because of their prominence in temperate zone forests, with which they are most famil-iar. At least in the northern hemisphere, the odor of the volatile terpenes in conifers (figure on Part I page) evoke the idea of resin for many people, for example, the smell of a conifer forest or a Christmas tree. Conifers and their progenitors are also the plants that left the earliest fossil record of resin (Chapter 4) and today occur in 80% of the world’s kinds of habitats.

Although five of the seven conifer families synthesize resinous terpenoids, only members of Pinaceae and Araucariaceae produce copious amounts. As a result, these taxa have been most studied, either for utilization of the resin or because of the resin’s protection of valuable timber (Chapters 5, 7–10).

Resin from some species of Cupressaceae s.l. and a few of Podocarpaceae, however, have been used by humans or have been analyzed in chemosystem-atic or chemical ecological research and are discussed where appropriate.

Classification

Conifers are the only gymnosperms that produce resin as defined here, although cycads produce mucilage and Ginkgo biloba produces terpenes that sometimes are referred to as resin. Conifers display such diverse characteris-tics that it is difficult to define them by a single feature, such as the flower for angiosperms (Miller 1999). The female cone (hence, the name conifer) is con-sidered the primary character in defining the families, but not all taxa have a woody or leathery multiseeded cone, often considered by nonbotanists as characteristic of conifers. Some species are multiseeded but their cones have more or less juicy scales and appear berry-like (e.g., junipers, Juniperus), or others have cones that are greatly reduced, with highly modified, juicy, brightly colored scales and just one seed (e.g., yews, Taxus). Furthermore,

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evolutionary relationships of conifers have remained controversial despite much work on their morphology, anatomy, embryology, cytology, phyto-chemistry, and paleobotany. This controversy has ranged from questions about the origin of conifers to their ordinal and familial relationships.

Since the seminal research of Florin (1951) on Paleozoic fossils, conifers have been associated with the fossil genus Cordaites (Chapter 4). Some re-searchers, however, have considered Cordaites and conifers to be in separate evolutionary lines. According to Doyle (1998), modern conifers are linked with Cordaites and ginkgos in analyses that include all extant groups of coni-fers. The earliest fossils attributable directly to conifers occur in the late Car-boniferous (about 310 Ma), and conifers were diverse and floristically impor-tant by the end of the Paleozoic era (290 Ma). In a study reexamining the phylogenetic relationships of fossil and living conifers, Miller (1999) pointed out that since the 1950s, modern conifer families were thought to have evolved from late Paleozoic ancestors via early Mesozoic transition conifers.

In the 1990s, however, expanding knowledge of Paleozoic conifers led to the view that modern conifers diverged directly from Paleozoic families, partic-ularly the Majonicaceae. The exception is the yew family (Taxaceae), derived from a different ancestral family than other modern conifers, a finding that supports the often held idea of placing Taxaceae in its own order, Taxales.

In contrast to paleobotanical support for two orders, Taxales and Coni-ferales, morphological and molecular cladistic analyses support the mono-phyly of conifers, that is, that conifer taxa are all descended from one ancestral population (e.g., Chaw et al. 1997, Stefanoviac et al. 1998). In this interpre-tation, Taxaceae are included in the Coniferales. Stefanoviac et al. (1998) thought that Taxaceae are closely related to the Cephalotaxaceae, which have sometimes been considered to be members of the Taxodiaceae, the redwoods and their relatives. The analysis by Stefanoviac and coworkers, as well as other morphological and molecular studies, support the merger of Taxodia-ceae into CupressaTaxodia-ceae although there are some strong opponents to this merger (e.g., Page 1990). In Plant Resins, Taxodiaceae are included in Cu-pressaceae and the combined group is referred to as CuCu-pressaceae sensu lato (s.l.). In some cases where the Taxodiaceae are not included in the group, the Cupressaceae are denoted as sensu stricto (s.s.). Stefanoviac and coworkers have put the so-called umbrella pine (Sciadopitys) into its own family, Scia-dopityaceae; they connected Araucariaceae to Podocarpaceae, thereby

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ing the two families with current southern hemispheric distribution and sug-gesting that they had a common ancestor. They also thought that the Pinaceae are the sister group to all other conifers, a view supported by others, includ-ing Chaw et al. (1997). Based on fossil cones, Miller (1999) changed his 1988 view that Araucariaceae and Pinaceae were sister groups in a basal clade to one in which Pinaceae branch from a basal position to all other conifer fam-ilies except Taxaceae.

Only the Pinaceae, Araucariaceae, Cupressaceae s.l., and Podocarpaceae unequivocally produce resin in secretory structures, although resin synthesis can be induced by injury without a secretory structure in some cases (Chap-ter 3). The Cephalotaxaceae have resin ducts but there is little evidence of their producing resin today, and Sciadopitys has not been recorded as produc-ing resin. Taxaceae produce terpene synthases similar to those of the Pinaceae (Chapter 1); there are no secretory structures, although Bierhorst (1971) con-sidered that they have been lost during evolution. Thus copious resin pro-ducers and little- or non-resin-producing families appear to be dispersed in the order Coniferales.

Pinaceae

Although essentially restricted to the northern hemisphere, the Pinaceae form the largest conifer family with approximately 200 species (about 35% of all conifers); 80–100 of the species, depending on one’s taxonomic perspective, are pines (Pinus; Richardson 1998). There are nine other genera; the next largest are the true firs (Abies) and spruces (Picea), with hemlocks (Tsuga) and larches (Larix) following. Douglas firs (Pseudotsuga), true cedars (Cedrus), golden larches (Pseudolarix), Cathaya, and Keteleeria each has only a few or one species (Appendix 1). The genera have been put into either three or four subfamilies over the years (e.g., Melchior and Werdermann 1954–64, Frankis 1989). Four subfamilies are most commonly recognized today. Phylogenetic studies, using molecular analyses based on chloroplast DNA and supported by fossil evidence, generally indicate that the Abietinoideae—Abies, Cedrus, Keteleeria, Pseudolarix, and Tsuga (including Nothotsuga)—are the basal group that appeared during the Jurassic. The Pinoideae (Pinus) and Piceoideae (Picea) follow during the early Cretaceous, and the Laricoideae (Larix, Pseudotsuga, and Cathaya) in the late Cretaceous (Labandeira et al. 2001).

Leaves of all Pinaceae contain terpenoid resin but in some genera resin

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may be produced only traumatically in the trunk of the tree (e.g., Cedrus, Pseudotsuga, Pseudolarix, and Tsuga). Wu and Hu (1997) thought the distri-bution of resin ducts in stems and leaves such a “striking morphological char-acter” that it should be used in evaluating relationships of genera in Pinaceae.

They thus divided the genera into three groups based on the presence or absence of resin ducts in the wood (Chapter 3). The importance of differ-ences in the kind of secretory structure and quantity of resin produced is elu-cidated in the contexts of the defensive properties of resin in Chapter 5, and human use in Chapters 7–10.

Paleobotanists such as Miller (1976, 1977) thought that the early evolu-tion of Pinaceae was centered on Pinus. Miller (pers. comm.) has concluded more recently, however, that there are three evolving lines within the Pinaceae and not a central pine group. Pinus today is not only the largest genus in the family but is particularly noted for its great ecological diversity and adapt-ability. Pines occupy a wide range of habitats from the arid plateaus of west-ern North America, the mountains of Mexico and Central America, to the tropical lowlands of the Caribbean. They also cover large areas across Eura-sia into the mountains and tropical lowlands of eastern AEura-sia (Mirov 1967, Richardson 1998). Furthermore, pines are the most widely planted exotic trees because of their adaptability and their large-scale use for timber, paper, and resin. Thus they are found out of their native range in South America, Africa, and Australasia.

Despite fragmentation of large pine forests during the past few hundred years through land clearance and pest introduction, pines continue to be con-spicuous components of forests in many parts of the northern hemisphere.

For example, Pinus sylvestris (Plate 1), known as Scots or Scotch pine in Eng-land and common pine on the European continent, is a complex of many intergrading varieties or subspecies with a range encompassing more than 10,800 km²(Nikolov and Helmisaari 1992), the widest distribution of any pine. It spans a wide range of environments from the Scottish highlands along the Atlantic to the Pacific coast of eastern Siberia to northwestern Asia, occur-ring with most of the boreal tree species of Europe and Asia; it also has scat-tered populations throughout the Mediterranean region (Mirov 1967). The resin has been used by Europeans throughout history (Chapter 7).

Ponderosa pine (Pinus ponderosa) is the widest ranging pine in North America. A drought-tolerant species, it persists in dry environments. Two

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varieties are recognized, partly related to the difference in the drought seasons in California and the Pacific Northwest versus those in the southwestern United States. In the driest environments, ponderosa pine forms savannas, but in more mesic environments it occurs in mixed stands with various other conifers. For example, it commonly occurs with Douglas fir (Pseudotsuga menziesii) in the Rocky Mountains and with Abies grandis, Calocedrus decurrens, and Pinus lambertiana in the Sierra Nevada. Ponderosa pine and Douglas fir are the two most important western North American timber trees, and their resins have been intensively studied for the protection they provide to valuable timber (Chapter 5).

Lodgepole pine (Pinus contorta) is another pine widely distributed across western North America, with four varieties. Some varieties have cones that are more serotinous (closed, often aided by the gluing effect of resin, until opening because of high temperatures such as those caused by fire) than oth-ers. This characteristic is partly responsible for the various ecological roles played by lodgepole pines in diverse ecosystems. In the Rocky Mountains, P.

contorta var. latifolia is primarily a pioneer or early forest successional tree in the Picea engelmannii–Abies lasiocarpa forest zone (Plate 3), where infre-quent but high-intensity fires occur. Those trees with serotinous cones have little or no seed dispersal in the absence of fire but typically generate dense, even-aged stands following fire. There are other areas, however, where lodge-pole pine is the only tree species that can reproduce with or without fire, and it can become dominant in both early and late forest succession. Most of the late-succession or mature forest stands have lodgepole pines with nonseroti-nous cones, allowing regeneration after disturbances other than fire. The suc-cessional status of resin-producing conifers such as Pinus contorta var. lati-folia has been shown to be related to the characteristics of the resin defense and long-term health of the forest (Chapter 5).

Pines of the coastal plain of southeastern North America (e.g., Pinus elliottii, Figure 7-2; P. palustris; and P. taeda), occurring in widespread savan-nas, and those around the rim of the Mediterranean Basin (e.g., P. halepensis) have been some of the most heavily used for resin. Today, however, pines native to the Asian tropics (e.g., P. kesiya, P. massoniana, and P. merkusii) are among the most productive for the naval stores industry (Chapter 7). Numer-ous pines also cover midelevations of mountains in Mexico (e.g., P. mon-tezumae, a variable complex of subspecies; Figure 7-6) into Central America

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Figure 2-1. Abies balsamea, balsam fir, an important balsam-producing tree of North American boreal forests (see also Plate 2).

(e.g., P. oocarpa) and much of the Caribbean (e.g., the P. caribaea complex).

These pines have a long history of human use.

In many cases, species of different genera of Pinaceae either codominate or are prominent components over vast expanses of boreal and high-elevation forests in mountains. It is assumed that resins probably provide defensive properties for these important forest trees, some of which have been heavily used by humans (Chapter 5). Examples include the boreal spruce-fir forests across North America (with Picea glauca and Abies balsamea, Plate 2 and Figure 2-1), the subalpine spruce-fir zone in the Rocky Mountains (domi-nated by P. engelmannii and A. lasiocarpa; Plate 3), and the ponderosa pine–

Douglas fir zone in the Rocky Mountains. In the Sierra Nevada, Douglas fir occurs in a zone with Pinus jeffreyi (Plate 4), a close relative of P. ponderosa.

Large areas in the arid southwestern United States and northern Mexico have a low open forest or woodland characterized by mixed species of pinyon pine (e.g., P. edulis and P. monophylla) and juniper (e.g., Juniperus monosperma and J. scopulorum, Plate 5). The resins from these trees have long been used by Native Americans (Chapter 10), and pinyon pines were once tapped for their resin on a small scale. Desert junipers also could be used as a basis for small cedarwood oil industries (Chapter 7).

The true cedars (Cedrus) consist of only three or four species that occur naturally in the western Mediterranean in North Africa to the western

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laya. Differences between the species are slight, and Melchior and Werder-mann (1954–64) considered their nearest relatives to be the deciduous larches (Larix). The name Cedrus is from kedros, used by the ancient Greeks to desig-nate a resinous tree. General use of this name by the Greeks may have led to trees other than Cedrus being called cedars, as discussed under Cupressa-ceae. The leaves of true cedars are resinous, and resin exudes from young cones (Plate 6). Resin that accumulates in the heartwood gives the wood its fragrant odor and is distilled as cedarwood oil (Chapter 7). Cedars of Leba-non (C. libani) are highly resistant to pests and also were the most massive trees known to the ancient Israelites, who used them to build the temple and palace of Solomon. Other ancient potentates exploited C. libani so inten-sively that only small remnant populations remain.

Larix, a cool northern hemisphere tree, is the most abundant deciduous conifer and occurs in some of the most extreme environments, above the northern and elevational limits of most conifer growth (Gower and Richards 1990). The American larch or tamarack (L. laricina), a tree of the cooler northern hemisphere, produces an economically valuable resin, as does the European larch (L. decidua), that is similar to Canada balsam from Abies balsamea (Chapter 8). Pseudolarix, with only one species, P. amabilis (Plate 7), is indigenous to a very limited area in the coastal mountains of eastern China. Considered to be closely related to Larix by Melchior and Werder-mann (1954–64), Pseudolarix is also deciduous. Before dropping, the leaves change to a rich golden yellow, hence its common name, golden larch. On the other hand, Frankis (1989) considered Pseudolarix more closely related to Abies and Cedrus than to Larix. Despite its restricted distribution today, Pseudolarix fossils indicate the genus was widely distributed in mid- to high latitudes of Asia, North America, and Europe during the Cretaceous and Ter-tiary (Le Page and Basinger 1995). Pseudolarix resin forms amber and may be related to the producer of Baltic amber because it is one of the rare conifers with resin that contains succinic acid (Chapter 4).

Members of the North American and Asiatic genus Tsuga are called hem-lock in North America and hemhem-lock-spruce in the British Isles. Despite the name, they are not relatives of the poison hemlock (Conium maculatum, Api-aceae, or Umbelliferae) used by the ancient Greeks to poison Socrates among others. Species of Tsuga are either small or large trees in northern coastal or subalpine forests. Hemlocks are considered by Melchior and Werdermann

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(1954–64) to be close kin of firs (Abies) and spruces (Picea) and often are confused with them. Hemlock leaves are resinous, but like Abies, Cedrus, and Pseudolarix, Tsuga only produces resin in the wood following injury (Chapter 3).

Since species of Pinaceae tend to occur in high density, dominating forests that cover vast areas, there are probably more individuals of these northern temperate zone dwellers than other producing trees; however, resin-producing angiosperm trees of the tropics have a far greater diversity of taxa.

Araucariaceae

Araucariaceae have been reported from the Triassic about 200 Ma (Chapter 4).

In fact, possible araucarian wood (Araucarioxylon) is thought to be related to that of Dadoxylon, a cordaitalean tree abundant during the Carboniferous period, 300 Ma. Today, Araucariaceae are a small family with only three gen-era and about 40 species (Appendix 1). Araucaria (19 species) is the most diver-sified genus and is disjunctly distributed throughout the warm southern tem-perate zone. However, araucarian fossils have been discovered widely in both the northern and southern hemispheres. Beautifully preserved fossil cones of Araucaria have been identified from as long ago as the Triassic and Jurassic periods (Miller 1977, 1988; Stockey 1982). Although some Araucaria species today produce abundant resin, often associated with insect damage, Araucaria has not been studied from an ecological perspective. The resin has a complex composition, often admixed with gum. There is relatively little variability in the gum fraction of resin from different species of Araucaria (D. Anderson and Munro 1969); the terpenoid fraction, however, has received little study.

The taxonomy of Agathis remains confused, with about 20 species recog-nized (Whitmore 1980a, de Laubenfels 1989). The genus may have evolved from Araucaria in the late Jurassic (Miller 1977). It contains by far the most important resin-producing species of Araucariaceae, some of which produce copious quantities of resin (Thomas 1969, Whitmore 1980a). Agathis is the genus of conifers most nearly confined to the tropics; in fact, A. robusta in southern Queensland, Australia (Plate 8), and A. australis in northern New Zealand (Figures 2-2 and 2-3) are the only species of the genus that extend beyond the tropics into the subtropics. Within the tropics, Agathis occurs in a wide range of habitats, for example, those with dry seasons varying in length from one to a few months, lowlands on a diversity of soil types, and at

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elevations up to 2000–2500 m. Both the timber and resin are of sufficient commercial value that rapidly growing species have been considered for enrichment planting, particularly in Irian Jaya (or West New Guinea), Indonesia (Chapter 11). The very hard (highly polymerized) copal-type resin has an extensive fossil record; researchers have chemically identified Agathis-type resin from the Triassic, 200 Ma (Chapter 4).

Figure 2-2. Agathis australis, kauri. The broad ever-green leaves, globose female cones, and elongated male cones are characteristic of the genus.

Figure 2-3. Agathis australis, towering monarch and copal-producing tree of northern New Zealand. With permission of the Alexander Turnbull Library, National Library of New Zealand, Te Puna Ma¯tauranga o Aotearoa (timber industry, logging, reference 6266 1/1).

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Agathis australis is the most famous species in the genus, and its Maori vernacular, kauri, has become a common name for the genus in many Euro-pean languages. It is also commonly referred to as kauri pine, an obvious misnomer since it is not a pine. About 1850, kauri occurred over millions of hectares, but now only about 7000 hectares of virgin forest remain on the northern tip of New Zealand’s North Island (Whitmore 1977). Agathis aus-tralis is one of the world’s forest giants, and trees can form a canopy 40–50 m or more tall. The trees also have vast girth, more than 10 m being common, with clear boles of 10–12 m before the crowns spread (Figure 2-3). Trees self-prune their lower branches as they grow, leaving massive limbs sometimes a meter in diameter in the crowns of older trees. Although the big trees are thought to be 500–800 years old, with a few approaching 1000 years, their precise age is difficult to determine because the trees are often hollow. These giant trees contain a large volume of millable timber and produce enormous

Agathis australis is the most famous species in the genus, and its Maori vernacular, kauri, has become a common name for the genus in many Euro-pean languages. It is also commonly referred to as kauri pine, an obvious misnomer since it is not a pine. About 1850, kauri occurred over millions of hectares, but now only about 7000 hectares of virgin forest remain on the northern tip of New Zealand’s North Island (Whitmore 1977). Agathis aus-tralis is one of the world’s forest giants, and trees can form a canopy 40–50 m or more tall. The trees also have vast girth, more than 10 m being common, with clear boles of 10–12 m before the crowns spread (Figure 2-3). Trees self-prune their lower branches as they grow, leaving massive limbs sometimes a meter in diameter in the crowns of older trees. Although the big trees are thought to be 500–800 years old, with a few approaching 1000 years, their precise age is difficult to determine because the trees are often hollow. These giant trees contain a large volume of millable timber and produce enormous