| BEN |
| BOTANICAL ELECTRONIC NEWS |
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| ISSN 1188-603X |
| No. 305 March 11, 2003 | aceska@victoria.tc.ca | Victoria, B.C. |
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This was to start with the statement that Don Britton has been the most important Canadian pteridologist in over a century, but then I realized that such a claim would be unfair. In fact he is the most important Canadian pteridologist ever as no other has so influenced North American fern taxonomy. And that influence extends world-wide, as his extensive network of international associates and correspondents demonstrates.
Don's pteridophyte research has spanned six decades and has been documented in over 90 scientific publications. Appropriately, the first of these in 1953 was an article on fern chromosome numbers. And Don quickly established himself as one of the continent's premier pteridophyte cytologists. The pioneering work he and his associates have undertaken with such genera as Dryopteris, Polypodium, Pellaea and Isoetes has literally rewritten several books. Over and above his co-authorship of the Flora of North America Quillwort (Isoetaceae) treatment, for example, Don has been a principal in the identification and description of some 15 new North American Isoetes taxa, 7 of which occur within Canada. One of these, I. prototypus, may well be Canada's most globally unique aquatic plant. And most of the Isoetes work was conducted after he had officially retired !
It is difficult to describe what Don brings to his work without resorting to clich‚s such as inspiring, thoroughly professional and ground-breaking. But that's really how it is. To work with Don is first and foremost to participate in a remarkable program of old fashioned scholarship. It begins with a review of all background aspects of the question/ issue (sometimes almost literally starting with when the earth was cooling!). And then moving through a careful examination of each bit of pertinent information up to the present day and the new information at hand. His literature searches are legendary in their scope and value. His cytological and taxonomic insights are both illuminating and practical. He conducts good science which is based firmly on real life observations. And it is, in short, a treat to be along for the ride.
Those of us privileged to have enjoyed being along for parts of 'the ride' look forward to each of Don's uniquely expressed correspondence (by mail or Fax ... only begrudgingly of late by email). Each is a wide-ranging, often cryptic and always thought-provoking review of the issues at hand. For decades he has produced such missives on a truly ancient Underwood typewriter, infamous and beloved for it's misplaced and often missing letters (particularly 'e's). We joked that we'd have it bronzed when he retired. When the ancient machine finally gave up the ghost some years back, however, we were astonished to see that Don produced another one just like it, complete with missing/ misplaced letters! We believe he has a stash of such relicts in a secret cavern found during his Dryopteris hybrid research along the Niagara Escarpment.
A particularly important and appreciated aspect of Don's performance is his entirely constructive attitude towards research associates. There's not a hint of academic or professional snobbery about him and he treats everyone involved in the venture equally, be they high-powered, international scientists or dedicated local amateurs. Those of us in the latter group find that approach to be both enlightening and inspirational. It's a great example and lesson for us all that no matter what our formal position in the search for scientific knowledge is, to share what we know and how we learned it, is of benefit to everyone.
Well done Don, and thank-you. Now back to work ....
In Canada it is has been collected three times, all three within the Atlantic region. The most recent observation was made in 1942 near Rimouski on the Gasp‚ Peninsula. It was also collected in 1902 near Bonaventure, Quebec and in 1904 near Clair, New Brunswick (Wagner and Wagner 1994). It is ranked SU (unrankable) in New Brunswick, SH (historical) in Quebec and NH nationally (Natureserve 2003). In the United States it is ranked N1 and is a candidate for protection under the Endangered Species Act (Rey-Vizgirdas and Behan 2001). It has been known from Montana, Idaho, Washington, Oregon, Utah, Colorado and California, however, four localities are now considered historical as they have not been relocated in over 20 years (Rey- Vizgirdas and Behan 2001). Globally, it is ranked G1.
Botrychium lineare is distinguished from other moonworts by the narrow, linear divisions of its pinnae. It most closely resembles Botrychium campestre W.H. Wagner & Farrar (prairie moonwort), a species characterized as bearing a broad rachis with overlapping or fused pinnae lobe tips. Botrychium campestre generally has a broader, stouter appearance and is more common in grassy areas whereas Botrychium lineare is generally a montane species (Wagner and Wagner 1994).
Recent work in Montana by botanist Toby Spribille has led to new records of Botrychium lineare within kilometres of the Alberta-Montana border (Spribille pers. comm. 2000). He suggested that I look for this species in southern Alberta. That opportunity arose last summer while I was in the area conducting a survey of two related ferns, Botrychium paradoxum W.H. Wagner (two-spiked moonwort) and Botrychium pedunculosum W.H. Wagner (stalked moonwort), a project supported by the Alberta Conservation Association. In June of 2002, I was exploring the botanically rich Front Range valleys near Pincher Creek with my colleague Paula Bartemucci. In Drywood Creek, a watershed about 50 km north of the U.S. border, we encountered several species of moonworts, among them, Botrychium lineare. Regrettably there were only two plants, and one had been partially damaged by mollusc herbivory. The plants were located on a road cutbank of loose gravel with no surface organic layer and poor soil development. It was clear that it would not be possible to make a collection of so small a population, so instead I took several photographs which were later mounted onto a herbarium sheet and submitted to the University of Alberta Herbarium.
This newly documented population of Botrychium lineare represents the only known extant population in Canada and is the northernmost in its entire range. It is also a new record for the flora of Alberta. The protection of this population is seen as very important to the conservation of this plant in Canada and significant for the long-term viability of this species globally.
Herbivory and habitat alteration by introduced molluscs and annelids have been identified as conservation threats to rare Botrychium species (Sessions and Kelly 2001; Gundale 2002). Sessions and Kelly (2001) documented a decline in a population of Botrychium australe R. Br. in New Zealand that was strongly associated with the invasion of an introduced slug, Deroceras reticulatum (Mueller), which was foraging on the ferns. Meanwhile, Gundale (2002) observed a correlation between the introduced earthworm, Lumbricus rubellus Hoffm., and extirpated populations of Botrychium mormo W.H. Wagner in Minnesota. Gundale demonstrated that the foraging activities of the earthworm caused a decrease in the surface organic layers of this fern's woodland habitat, thereby rendering the habitat unsuitable to Botrychium mormo. It is unknown whether the herbivory damage observed in the Drywood Creek plant was caused by a native or introduced mollusc. Regardless, herbivory by any animal could extirpate this fragile population. Soil disturbance by earthworms, as observed by Gundale, is not seen as a threat to the Alberta population of Botrychium lineare as the locality lacks a surface organic layer.
During an earlier review of the Botrychium specimens held at the University of Alberta, I annotated two herbarium sheets as possible specimens of Botrychium lineare (Williston 2001). These specimens should be revisited in light of the recent discovery.
References
The oak ferns, Gymnocarpium Newman, are a small genus (about 8 species worldwide) in the fern family Dryopteridaceae with a wide distribution around the northern hemisphere in North America, Europe, and Asia, mostly in temperate regions. With bi- or tri-pinnate, triangular-shaped fronds arising from creeping rhizomes, the plants form large clonal patches in the understory of moist conifer forests. Traditionally, the North American taxa have been treated as two species, the glandular Gymnocarpium robertianum (Hoffmann) Newman, and the glabrous Gymnocarpium dryopteris (L.) Newman. However, the treatment published in 1993 in Flora of North America recognizes five species in North America. Where did all these species come from? It turns out that Gymnocarpium dryopteris, as traditionally circumscribed, is now recognized to comprise three species, of which two are distinct diploids, and the third, an allotetraploid derived from hybridization between the two diploids. This is, after all, a familiar tale in fern evolution, but because of their complex patterns of morphological variation, it was necessary for researchers to utilize other characters - such as chromosome numbers, spore characters, and isozyme banding patterns- to reveal the full story.
The first piece of critical data that suggested that G. dryopteris might be more than one taxon was a 1966 paper by W.H. Wagner Jr. Whereas all previous chromosome counts of G. dryopteris from Europe and North America had been tetraploid, with n=80, Wagner found plants growing along Denny Creek, east of Seattle near Snoqualmie Pass, that were diploid, with n=40 pairs of chromosomes at meiosis. Wagner documented that ploidy in Gymnocarpium was expressed in spore size, and that coastal diploids had markedly smaller spores than the widespread tetraploids. He also noted that some plants with apparently malformed spores might be triploid hybrids. The diploid populations were recognized by Wagner and by other workers as representative of one end of a gradient of morphological variation, with the Pacific Northwest diploids (to which the name "disjunctum" applied) representing the robust, finely dissected extreme. However, there was a great deal of variation, and in some areas (such as Alaska and the Yukon), all points of the morphological and spore size gradient were found to occur. Wagner was "inclined to agree that var. disjunctum should probably merit recognition" (Wagner, 1966) Arthur Cronquist, in Vascular Plants of the Pacific Northwest (1969), noted Wagner's findings but did not adopt the name "var. disjunctum" for the coastal northwest plants (Hitchcock et al. 1969, Hitchcock and Cronquist 1972).
In the 1970's, Jaakko Sarvela, from the University of Helsinki, Finland, undertook a global study of Gymnocarpium (Sarvela 1978, Sarvela 1980). He treated "disjunctum" as a subspecies of G. dryopteris, and in the 1980 paper described a "hybrid subspecies", Gymnocarpium dryopteris ssp. x brittonianum Sarvela, representing the specimens with malformed or abortive spores. A triploid chromosome count, provided by Prof. Britton, was a key piece of evidence needed to demonstrate that these were indeed hybrids between a diploid and a tetraploid.
Wagner (1966) had found abortive spored hybrids occurring across northern North America, as far eastward as Nova Scotia, which was most puzzling, because the diploid parent, "ssp. disjunctum", was only known from the western portion of North America. How could hybrids occur so far from their likely point of origin?
Kathleen Pryer, a graduate student of Prof. Britton, further investigated the systematics of the North American oak ferns in her 1981 MS thesis. In addition to confirming the relationship between spore size and ploidy in Gymnocarpium, she also undertook a chromatography study of the North American taxa, which not only showed distinctions between G. disjunctum and G. dryopteris, but also showed the hybrid G. x brittonianum to be largely (though not completely) additive of the profiles of the two putative parents (Pryer et al, 1983). Still, the pieces did not all fit cleanly together. Of particular note was the emerging realization that there were actually two clusters of triploid hybrids, one in western and one in eastern North America, with a marked gap in the hybrid distribution in central Canada (despite the continuous presence of the tetraploids across Canada).
Fortunately for our story, Pryer continued her Gymnocarpium studies even after completing her MS degree. A more extensive study of herbarium material revealed another cluster of small spored plants -putative diploids- in the Appalachian Mountains of Pennsylvania, West Virginia, and Virginia. This, in fact, was the key piece of evidence that previous workers had missed - there was not one, but two areas of diploid oak ferns in North America, one area in the west, and one in the east. Furthermore, if one only compared the eastern diploids with the western diploids, they were clearly distinct in many respects. The Appalachian diploids , which Pryer and her co-worker Chris Haufler named Gymnocarpium appalachianum Pryer & Haufler, were petite compared to the robust western diploids. Furthermore, Pryer found consistent differences between the two diploids in the patterns of frond morphology. Finally, isozyme analysis showed a clear separation between western and eastern diploids, with an average Nei's genetic identity of 0.274, comparable to the average value for congeneric fern species (Pryer and Haufler, 1993). It was primarily the presence of triploid hybrids, along with the tetraploid G. dryopteris, that muddled the morphological distinctions between the western and eastern diploids.
The implications of these findings are several. First, our western North American diploid should clearly be treated as a distinct species from G. dryopteris, using the name Gymnocarpium disjunctum (Rupr.) Ching. The blurring of boundaries between G. disjunctum and G. dryopteris is due to the presence of triploid hybrids with malformed spores, but because these hybrids are presumable sterile, there is no avenue for gene flow between these two species so they are reproductively isolated. Second, G. dryopteris is an allopolyploid, and presumably a rather ancient polyploid, formed at some time in the past when the ranges of the two diploid taxa came together (perhaps under different climatic conditions than today), allowing the species to hybridize. The primary hybrids were sterile diploids, but one or more hybrid individuals underwent chromosome doubling to produce a fertile tetraploid species. Third, the abortive-spored members of the G. dryopteris complex could represent one of two different hybrid combinations - G. dryopteris x G. disjunctum (represented by the type of G. x brittonianum [Sarvela] Pryer & Haufler), or G. dryopteris x G. appalachianum. Unfortunately there is no easy way to distinguish these two hybrid combinations with herbarium material. However, it is likely that the hybrids in western North America represent the former, while hybrids in eastern North America are primarily the latter (Pryer and Haufler, 1993).
There is one piece of this story in the Pacific Northwest that is still unresolved. In Pryer and Haufler (1993), the records for G. dryopteris in Oregon and Washington (where G. disjunctum is the primary representative of the complex) are based on unpublished spore measurement data from specimens at WTU and ORE that I provided to the authors. I documented certain individuals that had longer spores than typical G. disjunctum, although their total spore "volume" was less than typical G. dryopteris and readily distinguished from the latter taxon. Pryer and Haufler chose to treat these "long spored" individuals as representatives of G. dryopteris, but I disagree with that conclusion on the basis of spore "volume". As such, I do not believe that G. dryopteris should be cited as a member of the flora of Washington or Oregon until its presence is confirmed by a tetraploid chromosome count.
In the west, G. dryopteris is generally a Rocky Mountain species, and the places where it would most likely occur in Washington is in Pend Oreille Co., where the hybrid G. x brittonianum has apparently been documented. Botanists working in the Rocky Mountain region of British Columbia, Alberta, and adjacent portions of Idaho and Montana have the greatest challenge in naming Gymnocarpium taxa, because both western species, plus the hybrid G. x brittonianum, are common in this region. Workers in this region should study the illustrations of oak fern frond morphology in Pryer and Haufler (1993). However, the best (and possibly only) method to identify oak ferns with certainty in this region is to collect voucher material with mature spores, and examine the spores under a microscope.
References
My work today is largely devoted to Hawaiian ferns and fern allies in connection with the preparation of a pteridophyte flora of Hawaii. The Hawaiian pteridophyte flora is a difficult one, one reason being that the Hawaiian ferns, like the flowering plants, are not quite what one would expect. Violets and lobelias, for instance, form little trees in Hawaii. The Hawaiian Athyrium also forms a little tree; other athyrioid species bear their sporangia pushed out beyond the margin. Two species of Dryopteris in Hawaii bear sori up on little stalks. Chromosomes are often a help in assigning these strange plants to their proper genera and families.
In my work with Hawaiian pteridophytes species, usually diploids, but also occurring at various ploidal levels, tetraploids, hexaploids, and octoploids. Because Hawaiian species are often so different from their ancestral or sister species in other parts of the world, I would like to find more aneuploids, genomes showing loss or addition of a chromosome, to account for the striking variations we find in Hawaiian species. But that has not been the case. One interesting chromosomal variation, however, has turned up in Hawaiian filmy ferns. The genus Gonocormus has two species in Hawaii and both are known also in other parts of the Old World. One is G. saxifragoides (C. Presl) Bosch and it is a sexual species with 36 pairs of chromosomes. The other species is much rarer, G. prolifer (Blume) Prantl, known in other parts of the Pacific as an apogamous fern with 72 chromosomes in the Solomon Islands, and also as apogamous with 108 chromosomes in Sarawak. Instead of the normal 64 spores, the formation of diads instead of tetrads often is part of the apogamous life cycle and the sporangia therefore contain only 32 spores. But the Hawaiian G. prolifer I found to have 64 spores, and at meiosis 72 pairs of chromosome. Gonocormus prolifer in Hawaii then is a sexual tetraploid, and not apogamous, and an example of a Hawaiian fern being different from its non-Hawaiian relatives.
Nothospecies, that is hybrid species, account for less than 20 percent of the fern flora of Hawaii, compared to 30 percent in North America. But work on Hawaiian hybrids is just beginning and will be augmented by molecular data now becoming available.
On June 26, 1861, William John Wills lay dying under a tree beside Cooper's Creek in central Australia. For weeks he and his two fellow explorers had survived on food prepared from the sporocarps of a small fern called "nardoo" (Marsilea drummondii A. Braun), but the food did not help. Although they had an abundant supply and ate heartily, the men were emaciated and their legs nearly paralyzed with pain. Wills managed to prop himself up against the tree and, with a pulse of only 48, wrote in his journal:
I have a good appetite and relish the nardoo much, but it seems to give us no nutriment ... starvation on nardoo is by no means very unpleasant, but for the weakness one feels, for as far as appetite is concerned, it gives me the greatest satisfaction.
Three days later the two companions set out to find help, leaving Wills behind, at his insistence, to fend for himself. They left him lying on the ground next to firewood, water, and an eight-day supply of nardoo. He was never seen alive again.
Two days later, Robert O'Hara Burke, one of Wills's companions, ate a full evening meal of nardoo and fell sleep with a full stomach. Early the next morning he died of malnourishment. The third man, John King, was befriended by Aborigines and eventually rescued by a search party, but he suffered permanent nerve damage in both legs.
King's rescue ended one of the first and most tragic exploring expeditions to the interior of Australia. The explorers were extremely unlucky because they would have been saved had they reached their supply camp on Cooper's Creek only ten hours earlier. It was then that the camp's garrison departed after having waited three months past the rendezvous date. But Burke and Wills succeeded in one respect: they were the first to cross the continent of Australia from Melbourne in the south to the Gulf of Carpentaria in the north (Moorehead 1963).
Historians have blamed the explorers' sufferings on nardoo's lack of nutrition. But is this justified? The Aborigines had relished nardoo for centuries as one of their main foods along with fish, crow, and mussels. Why would the Aborigines have continued eating nardoo if it lacked food value?
Recently, John W. Earl and Barry McCleary, two biochemists from Australia, proposed a different explanation for the explorers' suffering (Earl & McCleary 1994, McCleary & Chick 1977). They believe that the explorers were afflicted with beriberi, a disease caused by a dietary deficiency of thiamine (vitamin B1). They point out that Wills' journal contains a textbook account of the progression of the disease and is the only complete description of it in humans.
Yet they also point out that nardoo is not guiltless; it is, in fact, the source of the disease. Why then did Burke and Wills succumb to beriberi whereas the Aborigines did not? What is it about nardoo that causes the disease?
Burke and Wills developed the disease because of the manner in which they prepared nardoo, a manner different from that of the Aborigines. The natives prepared nardoo by pulverizing the sporocarps on a flat, hollowed-out stone and then mixing the nardoo flour with water. These steps were shown to the explorers. In his journal, Wills recorded the second step as demonstrated to him after a meal by an Aborigine he referred to as "Pitchery":
"The fish being disposed of, next came a supply of nardoo cake and water until I was so full as to be unable to eat any more, when Pitchery, allowing me a short time to recover myself, fetched a large bowl of the raw nardoo flour mixed to a thin paste, a most insinuating article, and one that they appear to esteem a great delicacy.
Then, according to custom as described by a Mr. Benny Kerwin, "They eat it by spooning it into their mouths with a mussel (shell), not with a coolibah [Eucalyptus] leaf or with bark, only with a mussel (shell)."
But Burke and Wills did not follow what the Aborigines showed them. They used a different method, preparing nardoo the way Europeans traditionally prepare grains: by grinding and cooking. After pulverizing the sporocarps, they mixed the flour with a lesser amount of water, kneaded it into a dough, and divided it into small cakes that were baked in campfire ashes.
The problem with preparing nardoo this way is that thiaminase, the enzyme that destroys thiamine, remains in the sporocarps. This enzyme occurs in high concentrations in nardoo, with the sporocarps containing more than three times the amount found in bracken fern (Pteridium spp.), a plant well known for its deadly concentrations of the substance, and the leaves containing about 100 times the amount. Because the explorers prepared their food incorrectly, they poisoned themselves to death. (Nardoo also poisons sheep. According to McCleary et al. [1980], during the summer of 1974 to 1975, over 2200 sheep died from nardoo-induced thiamine deficiency in the Gwydir basin area west of Moree, Australia.)
The Aborigines' method of preparing nardoo prevented poisoning by thinning the nardoo flour with water. This diluted the thiamine, the thiaminase, and any organic molecule that could act as a co-substrate for the thiaminase (a molecule with which the thiaminase must combine to be effective). In a diluted porridge of nardoo, the probability that all three molecules will combine at the same time is highly improbable. (The enzyme activity diminishes by the cube of the dilution. For example, a 1/10 dilution reduces enzyme activity by 1/1000.) Thus, dilution leaves the thiamine intact. Earl and McCleary also believe that the native's custom of spooning nardoo into their mouths with mussel shells, rather than leaves or bark, also reduced the likelihood that the enzyme would find an organic cosubstrate.
Because cooking destroys most enzymes, it is surprising that the explorer's baking nardoo in the ashes of their campfire did not destroy the thiaminase. Perhaps the resistance of thiaminase to heat is related to the plant's ability to survive the scorching summer temperatures of the Australian outback. Nardoo's remarkable heat-resistance is also shown by its spores, which can germinate from sporangia that have been boiled in water for 15 minutes.
Although this article is about nardoo poisoning, I cannot end it without mentioning a few facts about the plant and its bizarre sporocarps. The Australians apply the name nardoo to all their native species of Marsilea, and these typically grow in seasonal ponds that dry up in summer. When the winter rains return and the ponds are flooded, the stems of nardoo send up leaves that resemble long-stalked, four leafed clovers. At the base of these leaves are borne the sporocarps, which resemble small black beans. Although soft and green when young, the sporocarps harden and darken at maturity. This adapts them to drought by retarding water loss--a characteristic important during the dry season when sporocarps lie exposed on the ground. Some sporocarps retain moisture so well that they can germinate and produce gametophytes after 130 years (Johnson 1985).
The sporocarp is a peculiar structure (cf. Puri & Garg 1953). It is derived from a pinna that has, over the course of evolution, become folded and fused. These modifications protect the sori inside, which are attached to a ring of clear, water-absorbing, gelatinous material running around the inner edge of the sporocarp. This ring is called the "sorophore."
When the stony walls of the sporocarp crack or decompose with age, water seeps in and is imbibed by the sorophore, which then swells like a dry sponge in water. This exerts tremendous pressure on the sporocarp walls, which usually split open 15 to 20 minutes after the start of imbibition. The sorophore extrudes from the sporocarp and carries the sori with it. At this point it looks like a transparent, gelatinous worm three to six centimeters long with dangling whitish legs (the sori) along its length.
The outer cover of the sori, the "indusium," soon degrades, and the sporangia release their spores. These germinate and grow into mature gametophytes in less than one day, which is a short time compared to most ferns, which take several months.
The gelatinous material of the sorophore and indusia make up most of the edible part of the sporocarp. It was probably this gelatinous material that, once ingested by the explorers, swelled in their stomachs and intestines to produce bloating. Perhaps this also alleviated hunger pangs, explaining why Wills wrote that nardoo gave him "the greatest satisfaction" as far as appetite was concerned. It would also explain his observation that "The stools it [nardoo] causes are enormous, and seem greatly to exceed the quantity of bread consumed."
After the death of Burke and Wills, central Australia was opened up to colonists and the environment deteriorated. The settlers exterminated many species of plants and animals, and their cattle polluted and destroyed the sparse water sources. The Aboriginies could no longer live off the land and were forced to reside near European-run stations on the remaining supplies of clean water. Here they were weaned on to wheaten flour. Thomas Bancroft (1893) an English botanist on the scene, observed the change: "The civilised blacks, who were supplied with wheaten flour from the station, were not too proud to make and eat Nardoo damper [cakes]." This attitude fostered by the destruction of Aboriginal society, eventually put an end to eating nardoo.
References