Torreya taxifolia

In 1821 the United States had managed to conquer the Florida Territory from Spain after years of surreptitiously trying to usurp Spanish rule, and begun the process of ethnically cleansing the land of its previous inhabitants. Plantation owners and their slaves began to move south to colonise and exploit the new land. One among them was the patriarch of the wealthy Croom family, who in 1826 purchased land around the town of Tallahassee. When he died in 1829, his two sons inherited his holdings and resolved to invest further in the region, buying up or leasing numerous plantations and eventually becoming the largest landowners in the area. They had all of their slaves shipped from their North Carolina plantations to labour at clearing the land, cultivating maize and cotton, and building giant mansions for their slave-masters. One of the two sons was Hardy Bryan Croom, who besides having studied law, being state senator in North Carolina since his early thirties, and his duties running the family and managing his properties, devoted some time to exploring the sciences.[12][13][14][15] Among other scientific interests,[14] he describes himself as fond of botany, had assembled a small personal herbarium,[16] and posthumously authored a monograph on the carnivorous plant genus Sarracenia.[14]

East across the Apalache River from the first estate of his brother Bryan Croom in Gadsden, who had acquired it in 1826 and coined it 'Rocky Comfort',[14][15] (another source maintains Hardy Bryan Croom leased the property in 1832), he noted that the flora was quite unique compared to elsewhere in the Tallahassee region,[15] and sent specimens to the herbaria in the north from 1833,[12][17] and corresponded with the botanist John Torrey about the plants here from 1834 onwards.[16] Among the exsiccata he sent north in 1833 were samples of a type of yew,[12] which in his 1834 first letter of reply to an inquiring Torrey he describes as having "little doubt" was the Taxus baccata, the common yew of Europe. His description of the red berries appears to confuse this tree with another rare, local and hitherto undescribed species, T. floridana.[16]

Torrey realised that Croom was quite mistaken, and that the specimens represented a species new to science.[17] Croom and his entire family drowned in a shipwreck off the coast of North Carolina in 1837.[12][13][14][15] The novel species was eventually described by George Arnott Walker-Arnott in April 1838 from specimens sent to Torrey and collected in Florida by Croom.[17][18]

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.[3] In 1873 Karl Heinrich Emil Koch moved the species to Foetataxus taxifolia.[19] In 1891 Edward Lee Greene validated Constantine Samuel Rafinesque-Schmaltz's generic epithet Tumion and erroneously moved this species there as Tumion taxifolium.[20][21]

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.[17] Following the publication of this work, however, he was attributed as the author of this scientific name.[3][4] 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.[3] 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.[4] 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.[5][22] 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![17] 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.[2]

The University of North Carolina Herbarium has a single specimen, originally from the Jesup Herbarium of Dartmouth College, sent hither by Croom from the "Apalache River" in 1833. 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.[12]

It is likely most often known locally by the common name stinking-cedar.[6][7][9][28][8][26][24][29][25] Another more common local name used is gopher wood.[1][6][7][9][28][26][29][25] Nuttall, writing in the early 1840s, coins the name "yew-leaved torreya" for it, but describes that in the land where it grows in the 1830s, it was known as "stinking cedar", which he ascribes to the "strong and peculiar odour" of the timber, especially when it is "bruised or burnt". He also mentions the seed, covered in the aril, are approximately the size of a nutmeg.[17] In 1865 the German botanists Henkel and Hochstetter note that the Americans called the tree "stinking cedar" and "wild nutmeg". They mention 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 describe 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 call the plant "Torrey's Nuss-Eibe", which translates as "Torrey's nut-yew" in English.[3] According to the British gardening writer Nelson in 1866, Torreya species in general were known as "stinking cedars" or "stinking nutmegs" by the locals, though he himself recommended the name "strong-odoured yew" as preferred for British use. This specific species was called "stinking cedar" by the Americans according to him, although he recommended the name "mountain yew" for Britain -this is a calque of the (incorrect) Latin name he was using, he was apparently unaware of the fact that this species grows almost at sea level and nowhere near any mountains![5] In fact, of all species of Torreya, it is the only species which is never found in mountainous areas in its habitat.

Seed cone

Although the vernacular name Florida torreya was formally recommended by most conservation works and internet databases,[6][7][9][28][8][26][24][29][25] this was changed to Florida nutmeg in the late 2010s,[7][30] after the IUCN invented a new name in 2010.[1] Other names for this tree are savin,[7][8][25] polecat wood,[7][25] yew-leaved torreya,[25][17] foetid yew,[25] stinking cedar,[1][31] mountain yew (Britain)[5] or stinking yew (applied to the Californian species Torreya californica).[5]

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."[17]

Torreya taxifolia is an evergreen tree that may reach heights of 18 metres (59 ft) with an 80 centimetres (31 in) diameter trunk,[9] although it typically grew to 9–12 metres (30–39 ft) tall and 30–50 centimetres (12–20 in) in diameter,[7] and most stands today are composed of immature trees of less than 3 metres (9.8 ft) tall.[11] The crown is open and conical in overall shape,[9] with whorled branches.[28] These branches are spreading to slightly drooping. The bark of two-year-old branches are coloured yellowish-green, yellowish-brown or grey.[9] The young branchlets divide into threes.[17]

The stiff, needle-like leaves are sharp to the touch,[28] 1.5–3.8 centimetres (0.59–1.50 in) long[9] and 3 mm broad. These are arranged in two ranks on the branches[24] and are coloured glossy green above and light green below,[28] with a very slightly sunken grayish stripe of stomata on either side of the midrib on the underside,[9][28] and slightly round in transverse profile on the topside.[9] The leaves have an unpleasant, strongly pungent, resinous odor when crushed.[9][28]

It is dioecious, with separate male and female plants.[1] The male (pollen) cones resemble those of a common yew, but are much larger and have imbricated scales (bracts) at their base.[17] They are 5–7 mm long, grouped in lines along the underside of a shoot. The female (seed) cones are single or grouped two to five together on a short stem; minute at first, they mature in about 18 months to a drupe-like structure with the single large nut-like seed surrounded by a fleshy covering called an aril, 2.5–3.5 centimetres (0.98–1.38 in) long including aril,[9] about the size of a nutmeg.[17] The aril is glaucous and coloured dark green and streaked with purple at full maturity in the fall.[9] 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. The aril is fleshy in consistency, like a fruit.[17] When the aril is removed, the seed bears a striking resemblance to a large acorn.[3][17]

Foliage

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,[1] near the town of Chattahoochee, Florida;[25] there is also a small colony west of the Apalachicola at Dog Pond in Jackson County.[7][32] It grows along the Apalachicola River just south of the confluence of the Chattahoochee River and the Flint River, which reach northwards through Columbus and Atlanta to drain the southern Blue Ridge Mountains, a subrange of the Appalachian Mountains.[17] It only occurs in the Florida counties of Gadsden, Jackson and Liberty, and extends one mile into Decatur County, Georgia[7] (another source states the northernmost wild individual currently growing in Georgia is within 200 metres (660 ft) of the Florida state line). The outlying population west of the Apalachicola, in Jackson County, has always been small: In 1938 H. Kurz reported it to be restricted to one stand with a few trees,[33] in 1974 this was reported as consisting of 60 trees,[7] and in 1989 Mark William Schwartz and R. Nicholson reported it to consist of five trees.[33]

The area in which it naturally occurs is 203 square kilometres (50,000 acres), stretching 35 kilometres (22 mi) along the Apalachicola River.[33]

There is a small introduced population on the Biltmore Estate in Asheville, North Carolina, where it was planted as an ornamental plant.[7]

It grows at altitudes of 15–30 metres (49–98 ft), mostly on wooded ravines, bluffs and steep,[1][9][8] north-facing slopes.[1] These ravines have nearly permanent seeps. It also occurs in the bottoms of ravines and adjacent floodplains.[8] It grows in the shade under the canopy of larger trees.[1][7][8] The soils of this region are calcareous,[8][17] moist, dark-coloured, sandy loams.[8]

It occurs in two types of habitats restricted to the river drainage, an oak-tupelo-cypress forest or an oak-pine forest.[7] These forests are mostly deciduous, but evergreen hardwoods and conifers are also common.[8] R. M. Harper, who travelled throughout northern Florida by horse and train to document the compositions of various forests, stated in 1914 that the most frequent species in the Apalachicola ravines were Magnolia grandiflora (9.5%), spruce pine (Pinus glabra, 5.6%, American beech (Fagus grandifolia, 4.1%) and the understory Torreya taxifolia (4.0%) and Ilex opaca (3.5%).[33] According to the IUCN the large trees in this habitat are Fagus grandifolia, tulip tree (Liriodendron tulipifera), Acer barbatum, sweetgum (Liquidambar styraciflua), white oak (Quercus alba), and occasionally loblolly pine (Pinus taeda) and Pinus glabra.[1] Magnolias also grow in these woods.[8] Often these woods are hung with vines such as Smilax species and crossvine (Bignonia capreolata).[1] Another rare conifer, the Florida yew (Taxus floridana), occasionally grows with Torreya taxifolia.[1][37] A rare salamander found in these ravines is Desmognathus apalachicolae. The ravines boast the southernmost parts of the ranges of a number of more northern species such as the plants Hydrangea quercifolia, Epigaea repens and Kalmia latifolia and the copperhead snake Agkistrodon contortrix.[37] Upland around these woodlands are flatwoods, which are a longleaf pine/wiregrass (Pinus palustris/Aristida stricta) sandhill plant community.[7][37] It is uncommon in its native habitats, with individuals spaced far apart.[7]

Various animals eat the seeds.[7] Rodents favour the seeds.[8] Squirrels apparently remove the seeds, which they eat, from the arils, which they do not eat, and often store them in caches for the winter, where they may sprout into new trees.[38]

View of Apalachicola River at Torreya State Park

In a 2001 newsletter, the writer 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 a now-extinct animal. She made this suggestion based on the fact that this species is rare, that it grew well in the cooler temperatures of North Carolina, and her belief that the species was only found on the east bank of the Apalachicola and was unable to disperse to the west bank with the animals she thought might be the main dispersal agents today, squirrels. She theorised than during the last interglacial (the geologically short periods between ice ages) and the proceeding ones, the species grew further north. According to her theories, because there might have been an unknown and now extinct animal in the past which was better suited to eat and defecate the seeds, or otherwise move the seeds, the species was now "stuck" behind the Apalachicola which served as a refuge habitat for a relict population during the long periods of glacial conditions which characterised the Pleistocene. She further supposed that because the arils contain terpenes which are usually toxic for mammals, and the seed's shell is so thin that mammal molars would crush the seeds, that the purported extinct animal might not be a mammal and instead suggested some unknown species of large tortoise as the extinct ecological partner.[38]

It has been far too rare to harvest commercially since the 1950s, but it has a beautiful, yellow-coloured, close-grained wood. The timber is lightweight, hard, strong and highly durable.[7] In the 19th century, the tree was harvested for wood that was used as fence posts,[7][8][26] shingles,[8][26] cabinets,[7] Christmas trees,[1][8][7] firewood,[8][26] and as a fuel for riverboats on the Apalachicola River.[1] Fences made of this wood in the 1910s were still good in the 1970s.[7] 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.[17]

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.[17]

The first person to notice that the trees were dying was the forester L. T. Nieland in 1938, although he never wrote a formal paper about it. In the same year Kurz made a detailed study of the ecology of species and mentioned that there was no danger to the species vanishing from its habitat if lumbering would cease.[24] In 1954 Kurz and R. K. Godfrey surveyed the population and noticed no symptoms of decline. However, in 1962 Godfrey and Kurz, having surveyed the species again, reported that the natural stands of this species, which was historically never widely distributed, were dying off and extinction seemed assured, if not already accomplished.[24][39] By 1962, only non-reproductive sprouts regrowing from the top-killed stumps remained in the wild,[26][25][39] a situation which has persisted throughout the 20th century.[9][8] They attributed this to deforestation due to the lumber trade.[24][39] However, samples of the afflicted trees were sent to the University of Florida, where Erdman West suggested the decline appeared due to a fungal blight of some kind. In a 1967 article S. A. Alfieri Jr. et al. of the Florida Department of Agriculture presented their research of the phenomenon. The disease presents itself as a small, yellowish spot on the needles (leaves) -one or more per leaf, which soon spreads throughout the leaf until it dies, turns brown and falls off. Subsequently, the disease spreads into the twig, and all of the needles fall off, leaving only a tuft of new growth at the tip. The disease spreads in stages, first affecting portions, later the entire tree. Severely infected trees eventually lose most of their needles and twigs. Fungal fruiting structures grow on wholly necrotic tissue on the underside of the leaves, twigs and buds. In some cases, the stems of affected or dead trees also showed fungal canker. Young seedlings are also affected, but less severely than older trees. Trees growing in the shade are more affected than those in full sunlight.[24]

In 1985 the phytopathologist Nabih Elias El-Gholl, also of the Florida Department of Agriculture, was able to prove that there were at least two pathogens involved; the leaf-spot disease presented as light greyish-green spots, which later became tan-coloured, and were up to 8.4mm long and as wide as the needle, with brown, irregularly-shaped, 2.4mm long × 2mm wide, necrotic centres and were able to infect the plants in the absence of wounds within three days of inoculation. Initially only a few spots, maximally four, developed per plant. After some two weeks the infected needles died and fell off -by this time the undersides had developed spore structures,[40] which were primarily found along the two grey bands of stomata, but may also occur on the twigs.[25]

The canker disease presents as elongated fusiform swellings on the stems which eventually may break open. They are often found at the base of the trees.[25]

In 1993 Schwartz, who has spent much of his career researching the conservation of this species, and Sharon M. Hermann, reported on the progression of the disease. They monitored a census population of some 100 trees for four years, in this time 10% died, mostly the smaller individuals. Most plants consisted of multi-stemmed, regenerating stumps; the mean length of the longest stems were less than one meter. Less than half of the plants showed any growth in length during these four years, and 32% lost their primary stem, which meant the mean size of individuals within the population was decreasing. Death was not strongly related to specific location or if the plants showed disease symptoms, although stem mortality was higher with trees showing a higher severity of foliar pathogens.[32] In 2000 Schwartz et al. reported that despite Godfrey and Kurz's 1962 prediction, a small population size, continued population losses, and no known seed production for decades, extinction of T. taxifolia had not yet occurred, and although the population would likely steadily decline, it was unlikely to go extinct within the next 50 years.[33]