Plant of the Week 13th December 2021 – Wintergreen (Moneses uniflora, Orthilia secunda, and three Pyrolas)

Growing up in the south of England, the whole wintergreen group (Pyrolaceae as it was then) was a thing of distant, exotic wonder.  Being largely plants of pine woods in the northern half of Britain, I didn’t see any of them until a holiday to Norway when I was 16, and it would be several more years before I met any of them on British soil.  They did not disappoint.

In Britain we have five species of wintergreen: Moneses uniflora, Orthilia secunda, and three Pyrolas – P. media, P. minor and P. rotundifolia.  Of these, all occur in northern woods and moors and the first three are more or less exclusive to them, but P. minor does occur in scattered localities further south and sometimes other habitats, whereas P. rotundifolia also has a dune form sometimes separated as subspecies maritima.  This is a group of plants that are all more Scottish than British, but even in Scotland all species except P. minor are rare. 

Pyrola species have a rosette of roundish leaves at the base and a spike of spherical to bell shaped white to pinkish white flowers rising perhaps 10 to 15 cm from the rosette.  On P. minor they look like little hanging eggs with an opening at the bottom, but on P. rotundifolia they are larger and much more open; P. media is, as its name suggests, intermediate. O. secunda is distinguished by its flowers all facing in one direction, and clearly toothed leaves giving it the common name toothed wintergreen.   Finally, as its scientific name clearly indicates, M. uniflora has just the single flower on each stem, all facing downward so one has to press ones head to the ground to see or photograph the intricate detail of the flowers in their natural position. 

Let’s clear up some possible confusion – these are not the wintergreens of “oil of wintergreen”; that comes from American Gaultheria species, mainly G. procumbens and the active ingredient is methyl salicylate.  The oil is used in everything from flavouring chewing gum, dental products and root beer, to fine art prints and lubricants for firearms.  Two species of Gaultheria are naturalised in Britain, G. shallon from plantings in woods on acid soils, and the spiny G. mucronata in places like Skye where it appears bird sown some distance from houses.  There is also the chickweed wintergreen, Lysimachia (formerly Trientalis – that is another story) europaea, which is neither a chickweed nor a wintergreen but, it turns out, a highly specialised relative of yellow loosestrife in the Primulaceae.  Though unrelated, it shares its northern forest habitat with the true wintergreens of Pyrola and its relatives.

Before the advent of molecular data, the British wintergreens were placed in their own family, Pyrolaceae, united by the small herbaceous habit and distinctive flower structure.  However, anyone who encountered Chimaphila umbellata, a plant of boreal pinewoods sadly absent from the UK, might start to doubt this, for this has a slightly woody stem base and looks like a little dwarf shrub, much like certain members of the Ericaceae in fact.  Any observer who then questioned the distinctness of these two families based on this would have been shown to be correct by DNA evidence, which reveals that the Pyrolaceae was in fact a subgroup of Ericaceae, more closely related to the likes of Erica, Vaccinium and Rhododendron than any of these are to Arctostaphylos or the strawberry tree Arbutus unedo.  Hence the wintergreens derive from woody ancestors which had mostly (Chimaphila) or completely (the others) lost their woody habit and become specialised for highly shaded habitats in the far north.  Consequently the group is now reduced to subfamily level as Pyroloidae, or the even lower level of tribe (Pyroleae).  There was another surprise in store, because it was also found that the chlorophyll-less Monotropa hypopitys (now inexplicably renamed Hypopitys monotropa), arose from within Ericaceae, close to Pyroloidae.

Whatever its taxonomic level, Pyroleae is very unusual for being so ecologically consistent.  Most families, even small ones, have species in a wide variety of habitats.  A few have specialised for aquatic habitats (e.g. Alismataceae) and others favour a certain habitat for many but not all species (e.g. coast for Plumbaginaceae).  However all Pyroleae species worldwide occur in woodlands, although a few occur in other habitats as well (notably P. rotundifolia in sand dunes).  The presence of other Pyrolas in moorland habitats in Scotland might reflect populations that hung on after the trees had been felled, rather than natural occupants of such a habitat. 

The preference of Pyroleae for woodland habitats may reflect a special ability that they have, which makes them especially suited for dark places.  Lurking deep in the forest, most commonly among a canopy of evergreen pines, and often close to the Arctic circle, they live in places where light can be in very short supply.  Sometimes Moneses uniflora can turn up where the canopy is so dense that it lives in perpetual gloom, and where a peaty soil full of barely decomposed pine needles makes obtaining nutrients equally challenging.  Here, it can be almost the only flowering plants present, with otherwise only a few mosses and the odd fern.  Research over the past ten years has revealed how they do it – they are mixotrophs, a technical term which merely means they have more than one energy source.  They photosynthesise when they can, but top it up with energy stolen from fungi (Matsuda et al., 2012).  The related H. monotropa has gone just a single step further and given up photosynthesis altogether, demonstrating that it is possible to survive on nothing but fungi as an energy source.

To learn the root of this strange ability to parasite a group of organisms more accustomed to being the parasites themselves, we have to look beyond the Pyroleae, to the rest of Ericaceae.  Though Ericaceous plants do have a fair range of habitats (Chinese Rhododendrons often grow on limestone, for instance), they almost always grow on poor soils where nutrients are hard to obtain – hence the dominance of heathers and bilberry on Scottish moors.  Difficult conditions in the soil are often made even harder by the release of various toxic compounds from the fallen leaves of the Ericaceae plants themselves (Cairney and Meharg, 2003).  Ericaceous plants do well here because they have a unique advantage over others: Ericoid mycorrhiza.  Mycorrhiza are fungal associates of plant roots, and about 80% of land plants have them; the association dates back to the common ancestor of all living land plants.  Fungi are far better at extracting nutrients from soil and other substrates than plant roots, and these are exchanged for sugars, which the plants can easily obtain through photosynthesis.  However two plant families – Ericaceae and Orchidaceae, have each independently evolved an extra level of mycorrhizal relationship, co-opting a wider range of fungi and drawing from them more nutrients, and sometimes even energy.  This has allowed both families to evolve shade specialists that feed both on light and fungi – Pyroleae in Ericaceae, and genera like Epipactis and Cephalanthera in Orchidaceae – and also full parasites on fungi, like Hypopitys and orchids like Neottia nidus-avis.  Curiously, full parasitism on fungi has evolved five more times among the monocots, often in small and obscure tropical families, but is much rarer among the Dicots.  No-one knows why!

Therefore, it is the ability to exploit fungi for top-up energy that allows wintergreens to live in deep, dark northern forests, and this in turn has given rise to another astonishing feature of the group – the geographic range of its species.  It is quite normal for species of the far north to achieve circumboreal distributions, covering northern Eurasia, arctic North America and sometimes Greenland.  However, most families only have one or two species that have achieved this – British examples include Saxifraga oppositifolia, Juniperus communis, Linnaea borealis and Diapensia lapponica; others like Trientalis (now Lysimachia) europaea and Maianthemum bifolium are widespread only in northern Eurasia. Conversely, an incredible four out of the five British representatives of Pyroloidae have a circumboreal range (the exception being P. media, which is only in central and western Eurasia).  Two more species are circumboreal but not British – P. chlorantha and Chimaphila umbellata, making six in total, out of fewer than 40 species in the whole group.  What makes them so exceptionally good at doing this?  Covering northern Eurasia is not especially different for denizens of cold conifer forests, as such habitats stretch from Scandinavia to the NE tip of Asia.  The difficulty lies in getting from Eurasia to North America. 

Until around 5 million years ago, a land connection called the Bering Land Bridge linked Alaska to NE Asia, before tectonic movements broke it apart.  Falling sea levels did restore the bridge during later glacial epochs, but at these times it was probably too cold for anything but a few hardy large mammals (including humans) to cross it.  Before 5 million years ago, however, it was a different story.  The world was warmer than it is now, and species growing within the Arctic circle faced a curious challenge not seen on Earth today: how to survive a winter that is relatively mild, but still devoid of sunlight.  For even in the hottest periods of our planet’s life, the sun moved across the sky in basically the same way, and the Arctic would have been dark during the winter months. Furthermore, conditions that are dark but not below freezing likely presented a particular challenge for evergreen plants, for the retention of leaves through the dark winter would have cost energy in maintaining them in a way that the enforced suspended animation of being frozen would not.  But the wintergreens, as we have seen, can get energy from fungi as well as light, and this might just have been the perfect adaptation to get them through the dark winters as they slowly crossed the Bering Land Bridge.

.The Pyroloidae originated in Asia, and split from the rest of Ericaceae around 80 million years ago, towards the end of the age of the dinosaurs (Liu et al., 2014).  Within Pyroleae, Orthilia diverged first, and then Pyrola diverged from the common ancestor of Moneses and Chimaphila, both during the hot Eocene period 65-34 million years ago.  Hence the genera of this group parted ways long before the cold woodland biome they now occupy even existed.  The genus Pyrola began to diversify around 20 million years ago, and contains around 30 species, most of them in Asia but it has reached North America perhaps 5 or 6 times, including the three circumboreal species P. minor, P. rotundifolia and P. chlorantha (Liu et al., 2014).  Ecologically, the genus may be said to contain two groups – the boreal taxa of cold northern woodlands, including all three British species, and the Tertiary Relict group. Tertiary relict floras comprise groups whose species were widespread in the Northern Hemisphere during the warm conditions of the Tertiary period (that’s 65-2 million years ago, post dinosaurs but pre ice ages).  These floras then retreated to parts of the modern world that preserve moist warm temperate to subtropical conditions – mostly east Asia and southeastern North America, but also sometimes around the western North America seaboard and the Black Sea.  Rhododendron, for example, has species in all four regions, whereas Pyrola has species in the first three.  Pyrola seems to have originated as part of this flora ~20 million years ago, at a time when the widespread boreal forests of today did not exist.  Yet the genus was clearly unusually suited to invading this new, cold forest biome as it arose in a cooling world, because multiple Pyrola species subsequently invaded this biome, along with M. uniflora, O. secunda and C. umbellata and once there, all found it easy to spread west and east.  There is also a group of four Tertiary relict species in the genus Chimaphila, suggesting a similar ecological origin for C. umbellata (Liu et al., 2019).

In a warming world, the future may be precarious for these delightful plants, although local rewilding projects may yet provide safe havens for some of them.  Curiously, one species is doing quite well out of certain human activities, and that is P. minor.  This species has developed a taste for reclaimed ground and brownfield sites, especially where enough time has passed to allow trees to return.  It can be found thriving on former coalfield sites south of Loanhead (near the huge metal bridge now crossed by a cycle track), by Oakley and Blairhall (Fife), on Albyn Bing by Broxburn (and possibly other shale Bings in the area), and on waste ground covered by birch trees just south of the Millerhill recycling centre, East Edinburgh, which also houses a remarkable colony of H. monotropa.  

References

Cairney JWG & Meharg AA (2003).  Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions. European Journal of Soil Science 54:735–740. doi: 10.1046/j.1365-2389.2003.00555.x

Liu Z-W, Jolles DD, Zhou J Hua H, Milne RI (2019).  Multiple origins of circumboreal taxa in Pyrola (Ericaceae), a group with a Tertiary relict distribution.  Annals of Botany 114. doi:10.1093/aob/mcu198

Liu Z-W, Zhou J Hua H, Freudenstein JV, Milne RI (2019). Relationships between Tertiary relict and circumboreal woodland floras: a case study in Chimaphila (Ericaceae). Annals of Botany 123:1089-1098. doi: 10.1093/aob/mcz018

Matsuda Y, Shimizu S, Mori M, Ito S-I, Selosse M-A (2012).  Seasonal and environmental changes of mycorrhizal associations and heterotrophy levels in mixotrophic Pyrola japonica (Ericaceae) growing under different light environments. American Journal of Botany 99: 1177-1188.

Richard Milne