Peat, whisky and genomes

Consumerism having taken over the world, it seems that every botany lecture has to start by explaining the value of the organism in question. Bryophytes (especially hornworts) can be a particularly hard sell; however, the peat moss, Sphagnum, is a notable exception.  It has historically been used as bandaging for wounds, even as recently as the First World War (Ayres 2013), due to its highly absorbent nature and some antimicrobial properties. Aside from the serious business of saving lives, peat (including Sphagnum) has more contemporary uses, such as flavouring some Scotch whiskies (Harrison et al. 2012, a video of traditional peat extraction), the twelve-century-old traditional procession of moss men in Salamanca, Spain (see this article) and moss bath mats (see this link).

Typical Sphagnum habitat in Costa Rica. Photos taken during the
"Cryptothallus hirsutus" hunt in Costa Rica  with Gregorio Dauphin
and Norman Wickett (2006)

            However, the most economically important role of peat mosses may well be the efficient trapping of CO₂ in boreal forests. Bogs are a feature of temperate regions, where they serve an ecological role as carbons sinks (Gorham et al. 2012). The current warming of the planet may threaten to impact such fragile ecosystems, causing subsequent release of greenhouse gases. Although Sphagnum is not the only components of bogs and fens, it is by far the most abundant in terms of biomass, and the most charismatic. The rather distinctive gametophyte is arranged in a capitulum with spreading and pendent branches, while the leaf contains a network of alternating chlorocysts (chlorophyllous cells) and the hyalocists (dead cells) that give it its extraordinary water-holding capacity. The sporophyte is raised on an elongate pseudopodium of gametophytic tissue, rather than on a sporophytic seta. The capsule bears enigmatic pseudo-stomata and has a rather explosive nature (see the movie here); all this renders Sphagnum a morphologically isolated lineage.

Due to its high ecological importance, Sphagnum has been studied extensively and its nuclear genome is to be sequenced. This will make the first non true-moss sequenced (Physcomitrella and Ceratodon are true mosses), the most phylogenetically distinct of the three and only the fifth bryophyte to have a genome sequenced.

With nearly 350 species in four genera (Ambuchanania, Eosphagnum, Flatbergium and Sphagnum), the Sphagnosida may well be the most studied bryophyte class to date. High morphological plasticity of the species, high levels of introgression and hybridization make it a daunting task for taxonomists. Nevertheless, the biology of the plants can be captivating. Two recent papers illustrate the fascinating biology of Sphagnum. Karlin et al. (2010) demonstrate that a single multilocus genotype of Sphagnum subnitens exists along a 4,115 km track, all the way from Coos County, Oregon, to Kavalga Island in the Aleutian Islands. This monoicous plant seems to do extremely well despite its apparent lack of genetic diversity!

Secondly, Stenøien et al. (2011) show that the narrow Norwegian endemic Sphagnum troendelagicum originated prior to the Holocene (40-80,000 yrs ago), before the last Glacial Maximum. The authors have previously demonstrated that S. troendelagicum is a recent allo-polyploid, with Sphagnum tenellum as the maternal progenitor and S. balticum as the paternal progenitor. In contrast to the rather restricted nature of the hybrid, S. balticum is relatively widespread in North America, Greenland, the Nordic countries, Northern Asia and the Alps.

Sphagnum balticum (orange-coloured) among Sphagnum
magellanicum at Muckle Moss in S. Northumberland.
Photo by R. Porley

            Sphagnum balticum (Baltic Bog-moss) is a member of section Cuspidata. It is dioicous, and sporophytes have not been found in Britain. It has a typical orange-brownish colour, and is generally restricted to nutrient-poor ombrotrophic bogs. The species is rather rare in the British Isles (Porley et al. 2013, see here a short review of the book), only known from a limited number of sites in Scotland and England. Porley describes a famous moss hunt organized by J. Turner in 2000 in Muckle Moss, Northumberland, to attempt to find S. balticum. The successful event gathered attention from the local press.

Sphagnum balticum appears to be sensitive to high nitrogen deposition, sulphur deposition and high temperatures, factors that are highly intertwined (Granath et al. 2009). Habitat quality seems to be one of the main factors of its rarity in Britain.  The lack of sporophytes in Britain is potentially worrying. If the UK populations derive from a highly restricted number of introductions their extinction threat could be higher than their scarcity alone might implicate.  A recent study (see Forsman et al. 2013) suggests that the level of phenotypic and genotypic diversity in colonizers has a great impact on successful establishment and spread of newcomers. The knowledge of the genotypic diversity of the species is essential to quantify how much variability exists and will provide a genetic argument for future re-introductions. However, given that we have earlier seen that a single Sphagnum subnitens clone spreads for over four thousand km in western North America, it seems that risk cannot be assessed on either genetic information, or rarity information, alone.

Genetic resources for bryophytes lag well behind those for vascular plants, particularly the crop-plant relative angiosperms. The two exceptions to this are Sphagnum and the funariod mosses. Highly variable microsatellites, transcriptome data and soon nuclear genomic data for Sphagnum will allow focused population studies on S. balticum that although rare in Britain is common across its entire distribution, but that is also the father of a truly rare taxon, the Norwegian Sphagnum troendelagicum.

Thanks to L. Forrest and E. Karlin for comments.

Preceding blogs in this series:

A short review of Ron Porley’s book on rare English bryophytes http://internationalassociationofbryologists.blogspot.co.uk/2013/09/an-alien-in-need-of-protection.html

On the complex thalloid Dumortiera hirsuta

 http://internationalassociationofbryologists.blogspot.co.uk/2013/10/a-tropical-invader-of-european-lands.html

 On Splachnaceae (dung-mosses), particularly Aplodon

http://internationalassociationofbryologists.blogspot.co.uk/2013/12/deceived-by-old-and-foul-trick.html

On British orchards and their bryophytic diversity

http://internationalassociationofbryologists.blogspot.co.uk/2013/11/the-forbidden-fruits-and-their-mossy.html

Deceived by an old and foul trick

Fly visiting a Tayloria mirabilis' capsule and holding to its 
enlarged hypophysis. Photo by Adam Wilson 

The interaction between insects and flowers is just plain fascinating. For example, Aline Martins, a colleague of mine here in Munich, works on oil-collecting bees (check one of her recent papers here). These bees are attracted to particular malpighioid and Plantaginaceae flowers and the bees have specialized hairy legs brush to pick the oils, but of course also help with pollination. Another classic and perhaps less glamorous example is in the aroid family: The giant inflorescence of the titan Arum Amorphophallus titanum releases a foul smell, like rotting flesh, to attract small flies that pollinate the flowers. Some mosses have also "learned" this trick, in particular some members of the Splachanaceae, or dung moss, family, which develop ‘flower-like’ capsules.

Splachnaceae  compose a small family, with only 73 species. Several genera within the family grow on carrion or faeces (coprochory) and have evolved the ability to attract flies to disperse their spores between habitats (entomochory). The association is complex and fascinating (see a good review on the topic here). A number of anatomical and chemical characters of entomophilous Splachnaceae have potential significance for the syndrome. The sporophytes have bright-coloured capsules with inflated hypophyses (swollen or otherwise expanded sterile necks at base of the capsules, between the seta and urn); these emit low-weight volatile ‘aromatic’ chemicals that attract flies, the flies are deceived by the foul smell, land on the moss and pick up a mass of sticky spores before heading on to the next substrate, where they distribute the spores ready for establishment on their preferred habitat.… As you can guess by now, depending on the species, these dung mosses grow on herbivore, carnivore or omnivore droppings and even carcasses. The association between species and substrate seems to be non-random. In contrast, the diversity of flies visiting members of Splachnaceae is rather large and probably non-specific (Marino et al. 2009).  Entomochory (in this case insect-mediated spore dispersal) evolved a few times independently within Splachnaceae (Goffinet et al. 2004), leading to one of those eternal phylogenetic questions: is it a recent ‘invention’ within the family?

Aplodon wormskioldii
Photo by Blanka Shaw

            The story of the Carrion-moss Aplodon wormskioldii is included in Porley’s book on endangered English bryophytes (2013). Aplodon wormskioldii is the sole member of the genus, with a circum-arctic distribution (here an outdated map). UCONN Professor BernardGoffinet works on the family while my former labmate, PhD student Lily Lewis, works on another dung moss, Tetraplodon. I approached them for a quick update on dung mosses and in particular on Aplodon.  

            Aplodon wormskioldii is characterized by having leaves with a single costa and with a border of enlarged cells. The species is the only one in the family with a hyaline seta, it has brownish capsules and produces sporophytes frequently. Aplodon is quite isolated phylogenetically from all other Splachnaceae genera. The species is currently only found sporadically, on fresh dung, but somewhat puzzling fossil records from Greenland from a warm post-glacial interval 4000-6000 years ago (see here) show that Aplodon was then rather more abundant. Has this species only recently become an exclusive ‘dung lover’? Does the entomophilous ‘syndrome’ represent recent parallel adaptations in Splachanaceae? The answers remain enigmatic.

Phylogeny of the Splachnaceae (redrawn from Goffinet et al., 2004).

Solid black circles refer to copro/entomochorous species and

 open grey to coprochorous species with indehiscent capsules.

Aplodon is marked with a red arrow.

In the UK the species is considered to be at an extremely high risk of extinction as it has only been found in a few places in the Scottish Highlands and five sites in England (Porley 2013). It is listed as critically endangered in the British Red list.  The species is also listed under the UK Biodiversity Action Plan (BAP, see Hodgetts et al.2013) in Scotland.  Hodgetts et al.(2013) give some success stories for finding new localities for endangered bryophytes; one is the liverwort Adelanthus lindenbergianus. It was only known at a single site on the isle of Islay. However effective BAP surveys yielded a second Inner Hebridean site for A. lindenbergianus, on the isle of Jura. Such successful survey is lacking for Aplodon; Hodgetts et al. stress that very little is known about dung mosses such as Aplodon, Tayloria tenuis or Splachnum vasculosum, but the ephemeral nature of their habitat makes resurveying projects particularly difficult. For the time being, genetic material of the Carrion-moss is also kept ex-situ at the bryophyte threatened facility at RBGK.    

Porley suggests that the rare occurrence of the Carrion moss in England and Scotland may be because Aplodon is an ‘early casualty of climate change’: the species seems to love cold habitats and perhaps it is less happy with increasingly warmer temperatures. A potentially exciting phylogeographic study could sort out the genetic structure of Aplodon and whether the moss is a recent colonizer of the British Isles and continental Europe. Knowing whether the non-Arctic populations are genetically depauparate or filled with local adaptations would assist the conservation of this charismatic yet deceitful moss.
Thanks to B. Goffinet  and L. Forrest for comments.