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.