Torreya taxifolia

Torreya taxifolia
A young Torreya taxifolia
Conservation status
Critically Endangered  (IUCN 3.1)
Scientific classification
Kingdom:	Plantae
Clade:	Tracheophytes
Clade:	Gymnospermae
Division:	Pinophyta
Class:	Pinopsida
Order:	Cupressales
Family:	Taxaceae
Genus:	Torreya
Species:	T. taxifolia
Binomial name
Torreya taxifolia Arn.
Native range
Synonyms
Caryotaxus taxifolia (Arn.) Henkel & W.Hochst. Foetataxus taxifolia (Arn.) K.Koch Tumion taxifolium (Arn.) Greene Torreya montana Hort. Foetataxus montana J.Nelson, nom. illegit.

Torreya taxifolia, commonly known as Florida torreya or stinking-cedar, but also sometimes as Florida nutmeg or gopher wood, is an endangered subcanopy tree of the yew family, Taxaceae. It is native to only a small glacial refugium in the southeastern United States, at the state border region of northern Florida and southwestern Georgia.

T. taxifolia became one of the first federally listed endangered plant species in the United States in 1984. The IUCN has listed the species as critically endangered since 1998. It is considered "the rarest conifer in North America."

The Center for Plant Conservation describes Florida torreya as "one of the rarest conifers in the world," reporting that in the mid-Twentieth Century it suffered a catastrophic decline, as all reproductive age trees died. Approximately 0.3% of the original population remains, mostly as resprouting stems. The continuing threats are "changes in hydrology, forest structure, heavy browsing by deer, loss of reproduction capability, as well as dieback from fungal disease." The dieback was alarming not only for its speed and severity. Prior to its decline, "T. taxifolia was estimated to be the seventh most abundant tree species within the Apalachicola Bluffs region (Harper 1914)."

In its most recent (2020) update to the Florida torreya recovery plan, the United States Fish and Wildlife Service concluded that the naturally occurring population was continuing to decrease, with little to no reproduction observed and no recruitment in its wild habitat along ravine slopes on the eastern bank of the Apalachicola River. The remaining trees were still impacted by "disease, herbivory, and deer rub, along with other confounding factors." The agency reported that the ongoing decline of torreya numbers and health was exacerbated in 2018 when the entire native range of the species took a direct hit from the Category 5 Hurricane Michael. The agency reported an estimated 80–90% loss of canopy tree cover, causing direct kills of some torreya while exposing others to injurious levels of sunlight and heat.

Management of Torreya taxifolia as an endangered species has engendered controversy because a group of citizens, calling themselves Torreya Guardians, launched their own recovery program in 2005 by exploiting a legal exception for plants in the US Endangered Species Act. They began experimental plantings in the Appalachian Mountains and northward by obtaining donations of seeds from the owners of horticultural plantings in North Carolina. Media and academic publications have both reported on the unusual character and progress of this citizen form of species recovery.

Species discovery

In 1821 colonial control of the Florida Territory shifted from Spain to the United States. Plantation owners and their slaves began to move into the territory, exacerbating conflicts with the native peoples and the existing population of runaway slaves. One such plantation owner was the patriarch of the Croom family, who in 1826 purchased land around the town of Tallahassee. When he died in 1829, his two sons inherited and invested further in the region, buying up or leasing other plantations.

Plaque on the tree's discovery by Hardy Bryan Croom (Torreya State Park, Florida)

One of the two sons was Hardy Bryan Croom. Croom had studied law and became a state senator in North Carolina in his early thirties, but he also devoted time to exploring the sciences. Among other scientific interests, he described himself as fond of botany. He assembled a small personal herbarium and authored a monograph on the carnivorous plant genus Sarracenia.

While exploring along the east side of the Apalachicola River, Croom noted that the flora was quite different from elsewhere in the Tallahassee region. Beginning in 1833 he sent dried specimens to herbaria in the north, including that of another glacial relict woody plant found in the same, limited area. That plant is now known as Florida yew, Taxus floridana, and it is also critically endangered. In 1834 Croom initiated correspondence with the botanist John Torrey. Torrey carried forward studies of the species that would eventually carry his name after the tragic death at sea not only of Croom but also of his wife and children. Their shipwreck occurred during a hurricane in 1837, off the coast of North Carolina.

Taxonomy and naming

In 1838 this novel species was described by George Arnott Walker-Arnott from specimens sent to John Torrey and collected in Florida by Hardy Bryan Croom.

Arnott commemorated Torrey in the generic epithet. The etymology of the specific epithet is from Latin taxus, meaning 'yew', and folium, meaning 'leaf': i.e., 'yew-leaved'. Other species of Torreya have longer, less yew-like leaves, but this is not the reason that it was given this name, as the other species were described after this one.

The University of North Carolina Herbarium has a single specimen, originally from the Jesup Herbarium of Dartmouth College, sent by Croom in 1833 from the "Apalache River" (now, Apalachicola River). Curiously, it was first labelled as "Taxus montana Willd.", a South American tree, which was then later changed to Podocarpus taxifolia from southern New Zealand, and finally relabelled as Torreya taxifolia.

Taxonomic and naming changes also occurred when European botanists analyzed herbarium samples. The species was moved to the junior synonym Caryotaxus taxifolia in 1865 by Johann Baptist Henkel and Wilhelm Christian Hochstetter in their monograph on the conifers of the world, Synopsis der Nadelhölzer. In 1873 Karl Heinrich Emil Koch moved the species to Foetataxus taxifolia. In 1891 Edward Lee Greene validated Constantine Samuel Rafinesque-Schmaltz's generic epithet Tumion and erroneously moved this species there as Tumion taxifolium.

Plate from Nuttall's The North American sylva, published 1849. It is captioned: "A branch of the male plant, natural size. a. Male amentum. b. Back view of one of the stamens magnified. c. Female ament and ovule, magnified. d. Section of the ripe seed. e. Germinating seed."

In Thomas Nuttall's entry about Torreya taxifolia in his book about American trees, which was published in 1849 although it had been for the most part completed in 1841, he relates that in the correspondence Torrey had sent him, mention had been made of specimens of another species of taxoid tree which had been sent to him by Croom from the same region. To this plant Nuttall "doubtfully attaches the name" Taxus montana, somewhat of a nomen nudum, because Nuttall never actually described the plant besides quoting a summary description from Torrey's letter to him. Nuttall is doubtful about the taxon, because according to him it seems "scarcely distinct" from T. brevifolia of the Pacific Northwest. Following the publication of this work, however, he was attributed as the author of this scientific name. By 1865 this name was misapplied to Torreya taxifolia under the name Torreya montana. Henkel and Hochstetter synonymised this taxon with T. taxifolia in their work mentioned above. According to the Index Kewensis this was in error; the name Taxus montana had actually already been given to a species, now Prumnopitys montana, described (validated, in fact) in 1806 by Carl Ludwig Willdenow from specimens collected by Alexander von Humboldt and Aimé Bonpland on their famous scientific exploration of the Americas, and Nuttall had in fact referred to Willdenow's species. John Nelson, in his more utilitarian as opposed to scientific 1866 horticultural handbook of firs and pines for growing in Britain, introduced the name Foetataxus montana to write about Torreya taxifolia, apparently unaware of the German publication the previous year. In fact, all these sources were wrong, for Nuttall states that he found a newer specimen of Croom's, of the same taxon, in the Herbarium of the Academy of Natural Sciences of Philadelphia labelled as Taxus floridana! Despite that the original synonymy with T. floridana, all these names are still maintained in the synonymy of Torreya taxifolia in some modern databases as of 2020.

Type species of genus Torreya

Torreya taxifolia compared with two Asian species and Florida yew

Torreya taxifolia is the type species of the genus Torreya, owing to the timing of its entering herbaria used in western science. The genus has far greater representation in east Asia and also in the mountains of California (Torreya californica) than in its relictual range in Florida.

Family level classification has been controversial, but with genetic analysis it is generally placed in the yew family, Taxaceae. Its closest relative within the yew family is genus Amentotaxus. Genus Cephalotaxus also used to be considered a close relative, but it is now classified within an entirely different family, Cupressaceae.

Vegetative structure among Torreya species is very similar, as seen in the image above. All samples were taken and photographed onsite at Cox Arboretum in Georgia (US). All were young saplings growing in similar light and soil conditions. Florida yew, Taxus floridana, is easily distinguished from Florida torreya by touch: while both genera have pointed leaf tips, the yew tip is soft while torreya is so hardened it easily punctures skin.

Common names

Torreya taxifolia new growth

Very ripe torreya seeds, 31 October 2013, Mt. Olive, NC

The United States government official page listing the endangered status of Torreya taxifolia shows only one common name, Florida torreya. The current (2020) version of the official recovery plan for the species lists three common names, in order: Florida torreya, Florida nutmeg, and stinking cedar. The current (1993) page for this species of the U.S. Department of Agriculture Fire Effects Information System, lists six common names, in this order: Florida torreya, Florida nutmeg, gopherwood, polecat wood, Savin, stinking cedar.

Internationally, the common names listed for Torreya taxifolia are, in order, Florida Nutmeg Tree, Florida Torreya, Gopherwood, and Stinking Cedar. This is in accordance with the latest (2010) update of the species page of The IUCN Red List of Threatened Species. The Integrated Taxonomic Information System lists two common names: Florida nutmeg and Florida torreya.

There is a long history of documented common names that are also paired with descriptions of the species features that may have given rise to such names. One of the first prominent botanists whose documentation of the species includes common names was Thomas Nuttall. Writing in the early 1840s, he proposed the name "yew-leaved torreya." He noted that locally the species was known as "stinking cedar." He ascribed this name to the "strong and peculiar odour" of the timber, especially when it is "bruised or burnt". He also mentioned that the seed, covered in an aril, is approximately the size of a nutmeg.

In 1865 the German botanists Johann Baptist Henkel and Wilhelm Christian Hochstetter noted that the Americans called the tree "stinking cedar" and "wild nutmeg". They explained that the name "nutmeg" is derived from the bone-hard shelled and acorn-sized seeds, which are covered in an aril somewhat similar to that of true nutmeg. They also described that when the leaves are crushed they exude a pungent and disagreeable odour, which is why the local Americans used the name "stinking cedar". They themselves called the plant "Torrey's Nuss-Eibe", which translates into English as "Torrey's nut-yew." According to the British gardening writer John Nelson in 1866, Torreya species in general were known as "stinking cedars" or "stinking nutmegs" by the locals. Recommending the name "mountain yew" for British use, Nelson was unaware that this Florida species grows almost at sea level — and thus nowhere near any mountains Of all species of its genus, Florida torreya is the only one whose historically native habitat is not in mountainous terrain.

In the spring of 1875, Harvard botanist Asa Gray embarked on a trip to the panhandle of Florida, to "make a pious pilgrimage to the secluded native haunts of that rarest of trees, the Torreya taxifolia". The trees observed by Gray during that trip grew up to a meter in circumference and 20 meters tall. Pertaining to its common name, he wrote:

"The people of the district knew it by the name of 'Stinking Cedar' or 'Savine' — the unsavory adjective referring to a peculiar unpleasant smell which the wounded bark exhales. The timber is valued for fence-posts and the like, and is said to be as durable as red cedar. I may add that, in consequence of the stir we made about it, the people are learning to call it Torreya. They are proud of having a tree which, as they have rightly been told, grows nowhere else in the world."

Description

Technical description

Florida torreya will grow as a symmetrical cone-shaped conifer, with leafy branches remaining at ground level, if horticulturally planted and maintained in full sun. LEFT: October 2018 Fred Bess shows Connie Barlow, founder of Torreya Guardians, one of the two male trees he planted in his front yard in Cleveland, Ohio. RIGHT: Close-up of seeds in one of his two female trees.

Torreya taxifolia is an evergreen tree that may reach heights of 18 metres (59 ft) with an 80 centimetres (31 in) diameter trunk, although it typically grew to 9–12 metres (30–39 ft) tall and 30–50 centimetres (12–20 in) in diameter, and most stands today are composed of immature trees of less than 3 metres (9.8 ft) tall. The crown is open and conical in overall shape, with whorled branches. These branches are spreading to slightly drooping. The bark of two-year-old branches are coloured yellowish-green, yellowish-brown or grey. On mature trees the bark is only about 0.5 inches (1.3 cm) thick and is irregularly divided by shallow fissures.

The stiff, needle-like leaves are sharp to the touch and are arranged in two ranks on the branches. Images on this page show their dimensions; sizes vary depending on access to sunlight and the tree's overall health. The leaves are glossy green above and light green below, with a very slightly sunken grayish stripe of stomata on either side of the midrib on the underside, and slightly round in transverse profile on the topside. The leaves have an unpleasant, strongly pungent, resinous odor when crushed.

LEFT: October 2013 the ability of a Florida Torreya to bear both male and female cones on the same tree was documented at the home of A.J. Bullard in Mt. Olive, NC. RIGHT: Mature seeds are large and flesh-covered.

Genus Torreya is subdioecious, with separate male and female plants that may however include branches bearing cones of the opposite sex. The male (pollen) cones resemble those of a common yew, but are much larger and have imbricated scales (bracts) at their base. They are 5–7 mm long, grouped in lines along the underside of a shoot. The female cones when young are more angular than the male (as seen in the photo to the right). They are grouped two to five together near the tip of a branchlet. Tiny at first, they mature in about 18 months to a drupe-like structure with the single large nut-like seed (photo at right) surrounded by a fleshy covering called an aril, 2.5–3.5 centimetres (0.98–1.38 in) long including aril, about the size of a nutmeg. The aril is green but becomes streaked with purple as it matures, advancing to orange or fully purple in late fall. Unlike true yews, in which the aril forms a "cup" around the seed, in this plant the aril completely encloses the seed, leaving only a minute perforation at the end. When the aril is removed, the seed bears a striking resemblance to a large acorn.

Subcanopy growth adaptations

Florida torreya (LEFT, winter) adopts a leaning orientation in quest of sunlight under a deciduous canopy in northern Florida. Its close cousin, California torreya (RIGHT, summer), leans in the extreme beneath an evergreen canopy of Coast redwood and Douglas-fir in its native range.

Species within the Torreya genus are all adapted to establish and grow slowly as subcanopy woody plants in forest habitats of moderate to dense shade. In this way, their leaf structure and growth habit resemble species of yew, genus Taxus, which is a close relative.

Stems will lean in very shady conditions, in quest of patches of sunlight. Extremely leaning stems within a shady subcanopy gather moss as they age. An old leaning stem that fails to access sunlight will perish, but not before the long-lived root crown has given rise to one or more younger stems searching for sunlight in different directions.

Four years after a seed was planted in a deciduous forest in North Carolina, this seedling (LEFT) had not yet been damaged by rodent or deer herbivory. In contrast, a seedling of similar age (MIDDLE) had become multi-stemmed owing to herbivory in a forest in Alabama. But even when this species encounters sunlight, it still produces additional basal stems occasionally, as in this old horticultural planting in North Carolina (RIGHT).

Basal sprouting new stems from the root crown is thus another vital adaptation for long-term persistence in a subcanopy ecological niche. Basal sprouting will occur if young seedlings are browsed by herbivores. It also occurs in saplings when a multi-stemmed growth form enables a wider quest for patches of sunlight. But even in healthy, mature trees, new basal growth is present as a hedge against damage to the main stem. (References in the image caption.)

Distribution

Wild population

Map showing the counties and locations of populations of Florida Torreya along the Apalachicola River. The lone population in Jackson County is marked with an X, as it no longer exists.

Torreya taxifolia is restricted to limestone bluffs and ravines along the east bank of the Apalachicola River in the central part of the northern Florida Panhandle and immediately adjacent southernmost Georgia. There used to be one small colony west of the Apalachicola at Dog Pond in Jackson County, but it no longer exists.

This endemic tree grows along the Apalachicola River just south of the confluence of the Chattahoochee River and the Flint River, which drain the southern Blue Ridge Mountains, a subrange of the Appalachian Mountains. It occurs only in the Florida counties of Gadsden and Liberty and extends one mile into Decatur County, Georgia. The area in which it naturally occurs is 203 square kilometres (50,000 acres), stretching 35 kilometres (22 mi) along the Apalachicola River.

Alvan Wentworth Chapman, a leading botanist of his time in the southeastern states, wrote in 1885 that "Florida torreya" was found only in "widely separated clumps or groves" and appeared to be "exclusively confined" to the cliffs along the east shore of the river and to "the precipitous sides of the ravines" that dissected those cliffs. "It is never seen in the low ground along the river, nor on the elevated plateau east of it, nor, indeed, on level ground anywhere."

Prehistoric distribution

Torreya taxifolia is a member of an ancient genus at least 160 million years old. Fossil evidence indicates genus Torreya was widely distributed across the Northern Hemisphere beginning in the Jurassic period and as recently as the Pliocene. Like other globally disjunct genera of the Arcto-Tertiary Geoflora, Torreya was forced southward during the cooling of the Plio-Pleistocene epochs. In North America, the genus found refuge as numerous, but small and isolated, populations in California's coastal mountains and the west slope of the Sierras, which still constitute the native range of Torreya californica. Glacial advance was far greater on the eastern side of North America. But there, no mountains offered refuge as far south as the genus apparently needed to retreat. Hence, the only refuge that maintained Torreya through the coldest episodes of the Pleistocene yet also during the warming Holocene were ravines along the east shore of the Apalachicola River of northern Florida. Today, this location entails the entirety of the native range of Torreya taxifolia.

Each of the U.S. Fish and Wildlife Service official documents pertaining to Torreya taxifolia portrays this species as a glacial relict. The 1984 official listing of the species as endangered included this description:

"The Florida torreya and other endemics of the Apalachicola River system have received much attention from scientists and local residents. The relictual nature of this area accounts for the presence of many unique species (James, 1967). During recent glaciations, species migrated southward by way of the Apalachicola River system, which served as a refugium during cooling periods. The Apalachicola River is the only Deep River system that has its headwaters in the southern Appalachian Mountains. With the receding of the glaciers, cool moist conditions persisted on the bluffs and ravines of the Apalachicola River after climatic change rendered the surrounding area much drier and warmer."

The initial recovery plan in 1986 gave more details on the prehistory, stating, "Torreya is a genus of four or five species from Florida and Georgia, California, China, and Japan. The present geographic distribution of the genus is similar to the distributions of several other plant genera. The distributions, together with fossil evidence, suggest that these genera had wide distributions during the Tertiary Period that were subsequently reduced by climatic changes during the Quaternary (James 1961, Delcourt and Delcourt 1975)."

Peak glacial refuges and their famous relict trees, near river-system outlets in eastern North America. Critchfield Spruce went extinct before botanical explorers arrived. Florida torreya is critically endangered. The Franklin Tree (Franklinia alatamaha) went extinct in the wild soon after samples were collected and propagated in Philadelphia, PA.

The most recent (2020) recovery plan update states, "Based on fossil records, we can speculate that the geographical range of T. taxifolia included North Carolina and perhaps, it was forced south by glaciers, and when they retreated, it became isolated in small areas of the southeastern United States." This 2020 federal document describes the fossil history in this way: "Fossil records of Torreya are limited to seeds, leaves, and secondary wood of the Upper Cretaceous (Boeshore and Gray 1936, Chaney 1950). The records indicated that the distribution of the genus in past geological times was much wider than the present distribution. A fossil named T. antigua, which has some characteristics in common with T. taxifolia and T. californica, was described from the Mid-Cretaceous of North Carolina and was also collected from the near MacBride's Ford, Georgia (Boeshore and Gray 1936)."

Fossil pollen of genus Torreya and other genera within Taxaceae is generally deemed indistinguishable, one from another, and also from genera within families Taxodiaceae and Cupressaceae. Therefore, it is difficult to support past presence or absence of such genera in geographic locales where macrofossil plant material is rare or absent, even if substantial pollen (as in Quaternary bogs) is available. Nonetheless, because the Torreya genus entails sister species of a strongly disjunct distribution pattern of geographic ranges throughout the Northern Hemisphere, with macrofossil evidence at northerly latitudes during warm episodes of the Tertiary Period, it is clear that the eastern North American species of genus Torreya occupied more northerly habitats during many millions of years of history prior to the Quaternary glaciation.

The relictual character of the historically native range of this conifer species has been recognized for more than two centuries. The 1884 Annual Report of the Commissioner of Agriculture (USA) characterizes Torreya taxifolia (for which "Stinking Yew" and "Savin" are listed as common names): "No doubt the Torreya is a relic of a past epoch, when it may have had a wide range at the time when the elephant and mastodon were denizens of this country."

Ecology

Habitat

Resprouted torreya stem leaning outward from a bald cypress tree into a short needle palm at the bottom of a steephead ravine in Torreya State Park, February 2004.

Healthy original and offspring Torreya taxifolias at the Biltmore Estate, North Carolina in 2016

Torreya taxifolia occurs along limestone bluffs of the eastern shore of the Apalachicola River in a region with a warm and humid climate, occasionally influenced in winter by cold waves from the north that dip temperatures below the freezing point. It grows mostly in the shade of wooded ravines and steep, north-facing slopes under a canopy of Fagus grandifolia, Liriodendron tulipifera, Acer floridanum, Liquidambar styraciflua, Quercus alba, and occasionally pines (Pinus taeda, Pinus glabra). Often these woods are hung with vines (e.g. Smilax spp., Bignonia capreolata). Another rare conifer, Taxus floridana, occasionally grows with Torreya taxifolia. These ravines, known locally as "steepheads", have nearly permanent seeps.

The combination of subcanopy shade, a preference for north-facing slopes, and the nearly permanent seeps within the ravines suggest that Torreya taxifolia has already retrenched to the subhabitats within this glacial refugium that offer the coolest conditions during the extremes of summer heat.

Because the confined native range of Torreya taxifolia, which includes Torreya State Park, is a well known glacial refugium, the ecological conditions and plants that it associates with there do not provide the full picture of the habitat preferences of this species at this warming time of the Holocene. For this reason, the citizen advocacy group known as Torreya Guardians includes a page on their website titled "Historic Groves of Torreya Trees: Long-Term Experiments in Assisted Migration." "Naturalized groves" is the highest category listed, followed by "mature trees producing seeds" and "mature trees not producing seeds." As of 2022, 14 sites of historic groves are listed, described, mapped, and linked, along with six academic papers that describe the importance of such groves for assessing the viability of assisted migration as climate warms. The northern-most grove of horticulturally planted Torreya taxifolia that produces seeds is in Cleveland, Ohio.

Seed dispersal

Squirrels are abundant short-distance dispersers of the large seed of Torreya taxifolia today. But larger dispersers may have once carried seeds in their guts and deposited them in feces at longer distances from the parent tree.

View of the Apalachicola River from the highlands of the east shore in Torreya State Park, February 2004.

In her 2001 book, The Ghosts of Evolution, Connie Barlow suggested that T. taxifolia may be an evolutionary anachronism similar to the Osage orange (Maclura pomifera) and Kentucky coffeetree (Gymnocladus dioicus), which are thought to have been dispersed by now-extinct megafauna, such as the mastodon. Barlow suggested that the original seed disperser of Torreya might have been a now-extinct large tortoise. In the Winter 2004/2005 issue of Wild Earth magazine, an article by Barlow and Paul S. Martin titled "Bring Torreya taxifolia North — Now" offered another possible cause of dispersal problems as the glaciers retreated: extirpation of local squirrels by newly arrived Paleo-Indians inhabiting the riverside habitat and possibly also setting fires destructive of the species. Barlow's hypothesis later shifted to an intrinsic topographical barrier: perhaps "the large-seed of Torreya (which is sometimes capable of floating for several days) easily caught a fast and obstacle-free river ride southward from the Appalachian Mountains by way of the Chattahoochee River at the onset of cooling during the Pliocene or Pleistocene. But there was no river-flow way to return north during any of the interglacial warmings."

Uses

It has been too rare to harvest commercially since the 1950s, but it has a yellow-coloured, close-grained wood. The timber is lightweight, hard, strong and highly durable. In the 19th century, the tree was harvested for wood that was used as fence posts, shingles, cabinets, Christmas trees, firewood, and as a fuel for riverboats on the Apalachicola River. Fences made of this wood in the 1910s were still good in the 1970s. In the 1830s it was locally abundant enough for the trees to be harvested to be sawn into planks, which were much used in the construction of the village of Aspalaga Landing. In this era it was also recommended as making excellent posts for fencing, not being liable to attack by insects.

When the trunks are damaged, the trees yield a small quantity of pasty, viscous, blood-red turpentine, which can be dissolved in alcohol, but has a very powerful and unpleasant odour.

Cultivation

File:Torreya taxifolia norlina.jpg

LEFT: One of the original 1939 plantings of Florida Torreya at the Biltmore Estate near Asheville, NC. Photo March 2004. RIGHT: Paul Camire documented the 160 year-old tree in Norlina, NC and posted his report on the Torreya Guardians website.

It was first imported to grow in Europe in 1840. Large trees were to be found in Germany by the 1860s. It is tolerably hardy, but grows very slowly in Britain, and as such was only recommended for collectors.

It has occasionally been planted as a landscape tree around Tallahassee, and one such specimen in Lee, Florida has achieved 30 feet (9.1 m). Some large specimens are grown elsewhere in botanical gardens. There is a small introduced population on the Biltmore Estate in Asheville, North Carolina, where it was planted as an ornamental plant. The champion tree of the species is in a private garden in Norlina, North Carolina, having a height of 45 feet (14 m), a trunk diameter of 88 centimetres (35 in) dbh and a canopy width of 40 feet (12 m) in 1996. It has been said to endure winter temperatures of −31 °C (−24 °F) in North Carolina without much problem. The tree has also been naturalized in Louisiana at the Caroline Dormon Nature Preserve.

Propagation

Cuttings of Torreya shoot-tips in its native range and extending northward into some horticultural plantings of Georgia often show fungal contamination. Experimental studies with weekly sprayed applications of a combination of systemic fungicides, such as thiophanate-methyl combined with zinc and Maneb or thiabendazole, were able to eliminate the fungi from stock plants after four weeks, although these preparations were not US government approved as of 1987. Tissue culture methods of propagation were being investigated as of 1987. In the 21st Century, there was growing awareness that Torreya's dependence on arbuscular mycorrhiza fungal partners in its roots required that any treatments for removing above-ground fungal pathogens must not impinge on the health of the below-ground fungal symbionts.

Conservation History

Extinction Threats

The focus of concern for the future of Torreya taxifolia has shifted through time. The exceptionally small scale of its native range, however, has always been a primary concern.

In the 19th century, the vulnerability of any plant inhabiting only a very small range was known and was noted expressly for this species. Through the late 1800s, however, there was no mention of population decline owing to disease. Rather, A. W. Chapman in 1885 pointed to human overharvesting "for posts, shingles, and other exposed constructions" of the extremely durable wood as the primary threat.

A decade earlier, both restricted range and human overuse had been named as primary threats by Harvard botanist Asa Gray in the report of his self-described "pilgrimage" to the species in the spring of 1875. Fresh seedlings and the species' propensity to regrow new stems from the same rootstock were noted by him as a hedge against extinction:

"Seedlings and young trees are not uncommon, and some old stumps were sprouting from the base, in the manner of Californian Redwood. So this species may be expected to endure, unless these bluffs should be wantonly deforested — against which their distance from the river and the steepness of the ground offer some protection. But any species of very restricted range may be said to hold its existence by a precarious tenure."

As a new century began, there was still no mention of Torreya taxifolia decline by any threat other than humanity. Its relictual character still evoked strong interest. In a 1904 conference contribution, University of Chicago botanist H.C. Cowles wrote,

"In these ravines, and especially on the northward-facing slopes, is to be found a mesophytic association of plants that is abundant far to the north, but which reaches its southern limit here.... It seems likely, then, that we should regard Torreya taxifolia as a northern mesophytic left stranded today only in Florida. It presumably is one of the plants that failed to follow up the last retreat of the Pleistocene ice, and is preserved here perhaps because of exceptionally favorable topographic conditions."

Sometime between 1938 and 1962 it became clear that not only harvesting was reducing the remaining torreya trees to thin, resprouting stems. There was strong evidence of one or more above-ground pathogens that killed virtually all replacement stems not long after they had emerged from still-healthy rootstock. In a 1967 paper titled, "Stem and Needle Blight of Florida Torreya," a team of Florida plant pathologists described a "fungus disease contributing to a progressive state of decline which threatens the existence of the species both in its natural habitat and wherever it is grown." The team, led by S.A. Alfieri, included in their report a concise history of the unresolved nature of disease discovery and the speed of its spread.

Alfieri et al. presented that the first person to notice that Torreya taxifolia trees were dying in their wild habitat was an extension service forester in northern Florida, Lewis T. Nieland. He made his observation in 1938, but he did not write a formal paper about it. In that same year, Herman Kurz made a detailed study of torreya ecology, yet he remarked that there was no danger of the species vanishing from its habitat, so long as the human taking of stems could be kept in check. In 1954 Kurz and Robert K. Godfrey surveyed the population and noticed no evidence of decline by any stem-killing pathogen.

Eight years later, Kurz and Godfrey surveyed the species again — and reversed their conclusion. Their 1962 report, published as a "Letter" in the journal Science, offered a dire prediction: "Its extinction is well-nigh an accomplished fact." What they saw instead of healthy groves were "skeleton trunks, a few of which have abortive sprouts at their bases." As to the identity of the pathogen, they suggested, "apparently a fungal disease of the stems. We know nothing more than that."

The Role of Pathogens in the Die-off

The 1967 article by S. A. Alfieri Jr. et al, as summarized in the previous section, became a turning point in conservation concern for Florida torreya. Henceforth, conservation initiatives focused on determining why disease had killed virtually all the older stems, the identities of the disease agent (or agents), and how to proceed with species rehabilitation.

Diseased branch of a wild Torreya taxifolia, Torreya State Park, Florida (2004).

Alfieri, with additional colleagues, continued studies of Torreya pathogens well into the 1980s. His 1987 pathology team identified a half-dozen "associated microorganisms," mostly fungi. The team reported that since 1962, "natural populations have drastically diminished for reasons not fully understood. No reproduction from seed is taking place and only stump sprouts can be found in native areas." The canker disease had also spread to plants cultivated outside the native range such as in the University of Florida campus in Gainesville and in the Alfred B. Maclay Gardens State Park in Tallahassee.

An achievement in disease understanding was offered by the team in their 1987 paper: "the first documented report of pathogenicity." It was team member Nabih Elias El-Gholl who had made the initial discovery in 1985, now worked into a full report in this 1987 publication. The pathogen, Fusarium lateritium, is a kind of filamentous fungus that infected and killed torreya needles in laboratory experimentation. It has a global distribution and infects a variety of agricultural plants. Fusarium is a species-rich genus, and it is highlighted here because in 2011 its role in torreya pathology gained renewed attention as a lethal pathogen. At that time, the fungal agent would be documented as the cause of stem cankers, and it would be awarded a new species name, Fusarium torreyae.

The Role of Habitat Deterioration in the Die-off

Fungal pathogens associated with Torreya taxifolia, listed in the 1986 recovery plan, US Fish and Wildlife Service.

Following the 1984 listing of Torreya taxifolia as federally endangered, the first recovery plan (1986) included a list of numerous fungal species "associated with diseases" affecting this species. No pathogen was presented as the dominant or sole cause of the sudden and extreme die-off of virtually all the reproductively mature stems.

Fusarium genus was included in the list, though linked with "root rot" rather than needle necrosis as the disease symptom. The recovery plan, however, suggested that pathogens may be the "proximate causes," with "environmental factors" entailing the ultimate cause or causes:

"The occurrence of multiple fungi, some of them known to be soil inhabitants and opportunistic pathogens of several plant species, suggests that the fungal infections are merely symptoms of another underlying cause of decline" (page 6). "The decline of Torreya taxifolia in its native habitat may ultimately be due to environmental factors that stressed the trees, including alteration of its forest habitat, alteration of vegetation above the ravines it inhabits, alteration of water seepage into the ravines, or droughts. The proximate causes of the decline are an assortment of fungal infections, resulting in stem cankers, stem and leaf blight, and possibly other problems. The decline has affected all wild Florida torreya trees (Godfrey and Kurz 1962) and possibly all cultivated trees" (page 2).

The recovery plan put environmental deterioration into the context of the geological timescale of climate change:

"The basic limiting factor of Florida torreya is its restricted geographic range and habitat, rendering the species vulnerable to human disturbance of its habitat and to natural factors, such as climate change, which are likely to be felt by all of the populations.... The decline has been so great that few if any seed-bearing trees exist in the wild, making recovery of the populations through natural sexual reproduction impossible" (page 5). "It is possible that relatively minor human alterations of the habitat may seriously affect torreya; it is possible that the present-day physical environment of the Apalachicola bluffs and ravines is only marginally suitable to Florida torreya. The species may be restricted to the area because it failed to migrate northward at the end of the Pleistocene" (page 6).

Noting that torreya "appears to occupy sites where a steady supply of moisture is available from seepage, and where it is shady in the summer" (page 6), the plan then offered possible human factors that may have deteriorated those habitat conditions. "Alteration of the pine forests on uplands above the ravines" was one possible factor. Logging within the ravines was also noted. Ravine temperatures could have been affected by "construction of the Jim Woodruff Dam, completed in 1956."

The Jim Woodruff Dam was one human alteration in the landscape for which quantitative data was available and could be assessed. Mark Schwartz would be the scientist to make that evaluation. But first, he would join with Rob Nicholson of Harvard's Arnold Arboretum, to undertake the "first objective" of the federal recovery plan: to gather cuttings from the remaining wild specimens in the native range in order "to produce a genetically diverse collection of sexually mature, reasonably healthy trees in cultivation to preserve a representative gene pool to serve as stock for possible reintroduction into the native habitat" — which itself would begin only "when there is reason to believe that the trees would survive to maturity" (page 8).

With more than 2,000 branchlets cut from the wild and being rooted in facilities at Arnold Arboretum and other institutions, Mark Schwartz joined with Sharon M Hermann in the field to officially catalog "The Continuing Population Decline of Torreya taxifolia", which was published in 1993. In 1995 Schwartz and Hermann teamed with Cristoph S. Vogel in publishing the results of their field and lab work in assessing a number of environmental variables that could have stressed the torreya population enough to induce one or more pathogens to become lethal. The team posed and assessed a total of eight hypotheses for the decline: three possible "biotic agents" and five possible "abiotic triggers."

The "abiotic triggers" assessed were: (1) Water stress, (2) Microclimatic warming, (3) Regional warming, (4) Hydrologic change, and (5) Fire suppression. The team documented that both regional drought and dam construction were "coincident with the timing of the decline," but such triggers were not, in their view, commensurate with the scale of torreya die-off: "While we cannot rule out the possibility that moisture, temperature or soil nutrient stress contributed to inciting disease in T. taxifolia, the argument that one of these concurrent environmental changes single-handedly incited a decline is very weak." The team did acknowledge, in Table 2, that, "If T. taxifolia is limited by warm temperatures, a slight increase in temperature may render it susceptible to native pathogens. This species may be an early casualty of global warming."

Because the team focus and expertise was ecological rather than pathological, their assessment of the three hypotheses for "biotic agent" causes relied on existing pathological publications rather than new research of their own. Their assessment was negative as to: (1) Introduced pathogen, (2) Pathogen vectors (e.g., deer antler rubbing), and (3) Fungal pathogens as epiphenomenon (that is, initially virulent but becoming weak or absent). However, the team did acknowledge that "most catastrophic declines have involved exotic pathogen" and therefore an as-yet "unknown pathogen" could ultimately be determined as the cause.

The Stem Canker Fungus Identified

TOMORROW I WILL ADD THIS TOPIC WITH THE JOURNAL REFERENCES OF JASON SMITH ET AL.

Status

A potted Florida Torreya at the US Botanic Gardens in Washington, D.C.

This was one of the first federally listed endangered plant species in the United States in 1984 (Federal Register 1/23/84). It is one of only two species of conifer protected under the Endangered Species Act. It was listed as "threatened" within the state of Florida by 1987 (Florida Statutes Section 581.185), again in 1994 by the Florida Game and Fresh Water Fish Commission, and in 1998 the status in Florida was changed to "endangered". In 2002 it was added to the list of "endangered" plants of Georgia. It has been a "critically endangered" species on the IUCN Red List since 1998, in 2000 this was said to be due to estimated 98% decline in mature individuals since the early 1950s.

Threats

According to one older theory logging of shade trees may stress individuals of this species, which does not like being suddenly exposed to full sunlight, conducing infection.

Another threat to the population is destruction by deer. Deer preferentially select young trees of this species to rub their new antlers on, sometimes killing them. Feral pigs may also uproot and destroy seedlings. Another possible cause of the historical decline may be changes in the environment due to fire suppression, and changes in water tables linked to the construction of dams. Specifically, many trees were killed when the land was flooded in the construction of the Jim Woodruff Dam impounding Lake Seminole.

According to one writer, the population of the species may have been impacted by postglacial global warming, as it may possibly be better adapted to the cooler climate found in Florida during the last ice age. It may not have been able to move north due to poor dispersal abilities. This is based on the fact that the introduced population on the Biltmore Estate in North Carolina appears to be doing fine, and is even reproducing naturally; squirrels plant the seeds in the flower beds and these germinate.

Actions

Fungicide treatment with Maneb has been shown to be remarkably effective, with plants showing renewed growth afterwards with little to no fungal infection. It has been applied since 1967, but as of 1987 it is not specifically labelled for use in Torreya.

A theory perhaps first put forward in 1990 by Greg Seamon, land manager at the Apalachicola Bluffs and Ravines Preserve (of The Nature Conservancy), was that Torreya taxifolia may be somehow suffering from the suppression of fire in the upland longleaf pine-wiregrass sandhill ecosystems. However, after regular fires were again instituted in the 1990s in the preserve, this appeared not to have an effect, with the species experiencing an increased three percent annual mortality at the turn of the century.

Two years after declaring the species an endangered species, in 1986, the U.S. Fish and Wildlife Service published a recovery plan. The chief tactic was to produce a genetically diverse collection of trees for reproduction and reintroduction into the wild. Other priorities were to protect the habitat of remaining populations, and to study the disease and methods of propagation.

Plants in general attract very little funding compared to vertebrates, this tree is no different. The US federal government spent only $1,500 on conservation of the species in 1993, placing it 884th out of 926 endangered species. Schwartz et al. stated that recovery is possible, but this will require a greater level of commitment and a dedicated increase in funding.

Small experiments by Schwartz and Hermann in the 1990s found that planting cuttings in the native habitat is possible. Schwartz et al. recommended population augmentation by planting volunteers isolated by more than 100m from extant stands to reduce chance of contamination.

The tree is well-represented in cultivation, and is widely planted for conservation purposes outside of its native range. Plants outside of its historic native distribution are undamaged by fungal disease and produce viable seed. In Tallahassee for example, not far from the native range, a number of large trees had been grown for almost a century in the Alfred B. Maclay Gardens without problems and had been successfully propagated here since the 1960s, although the trees in this park became infected by the canker disease by 1987. It is found in arboreta, botanical gardens and elsewhere throughout the world. In the Netherlands, for example, it is grown in the Arboretum Trompenburg, the Arboretum Oudenbosch, the Hortus Haren, the Hortus Botanicus Amsterdam and the Pinetum Blijdenstein.

In the United States the Center for Plant Conservation maintains the species in its National Collection of Endangered Plants; the Arnold Arboretum of Harvard University is the primary custodian of this species. The Atlanta Botanical Garden and the State Botanical Garden of Georgia are actively propagating the plant for conservation purposes. These are members of the Georgia Plant Conservation Alliance, which is protecting the species by growing seedlings and cuttings, and planting these both in situ and ex situ. Plants are also grown at the United States Botanic Garden.

In her 2001 newsletter article Barlow synthesized her suppositions to suggest that the only way to conserve the species was for humans to engage in assisted migration, transplanting across great distances. She noted that, in essence, humans are now the gardeners artificially preserving most isolated islands of "wilderness" amongst a sea of human development, if we like it or not. In this she was not unique, in 1994 Foote and Jones had already written that the survival of this species was likely dependent upon cultivation in gardens. The idea is that T. taxifolia for some reason was unable to migrate north from its "ice age pocket refuge" in northern Florida. This inspired the formation of a group, Torreya Guardians, which are attempting to rewild Torreya taxifolia trees in cooler mountain areas in the southern Appalachians in an attempt to aid the species. Some conservationists consider T. taxifolia as the lead candidate for assisted migration of forests in North America. This project has proved contentious.

Protected areas

The natural populations are largely protected within the Torreya State Park and at the Nature Conservancy's Apalachicola Bluffs and Ravines Preserve (first parcels purchased in 1982 to protect the ravines, before the species was officially listed as endangered).