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Monotropa in Essex 2009:                                                                       BACK

The Status of Monotropa hypopitys L. Yellow Bird’s-nest in Essex.

KEN ADAMS

 63 Wroths Path, Baldwins Hill, Loughton IG10 1SH

Essex Naturalist 2009 26: 159-162.

Abstract

Although recorded at several sites in Essex in the past this rare achlorophyllous plant is now only known from two chalk ledges above Grays Chalk Quarry. Monotropa obtains its carbon supply by tapping into the roots of specific tree species utilising a basidiomycete as the intermediary, and there appear to be cryptic genetic strains each of which is faithful to just one species of Tricholoma fungus, which in turn is associated with a narrow range of host trees. In our case Tricholoma cingulatum and the host trees Salix cincerea and S. caprea. This obligate association of each strain with just one species of fungus may explain why Monotropa is so rare in Essex.

 Introduction

Consult any modern flora and you will find Yellow Bird’s-nest described as a saprophyte, capable of breaking down decaying plant matter. As long ago as 1881 however, Kamienski described the fungal sheath that envelopes the peg-like branches of the bird’s nest-like root ball at the base of a Monotropa plant, and realized that this might enable it to indirectly parasitise an adjacent photosynthetic plant with which the fungus had a mycorrhizal association. With developments in the ability to grow Monotropa experimentally from its tiny seed, [no mean feat, as the embryo consists of only four cells supported by just nine endosperm cells], and the use of DNA typing to establish the species of fungi forming the fungal sheaths, it has become possible to study populations more effectively. Monotropa hypopitys L. is our only European species. It occurs right across the northern hemisphere in both N. America and Asia, but the N. American plant has slightly different pollen morphology from our plant and is frequently pink in colour. In N. America another species with just one flower, hence M. uniflora L., the Indian Pipe, utilises several species of Russula as intermediaries to obtain its carbon supply.

DNA samples taken from fungal wefts on Monotropa hypopitys roots in this country, Finland, Sweden and Japan have been matched with Tricholoma cingulatum in the case of associations with Salix cinerea, S. caprea and Salix repens. Whereas plants growing under pines have been shown to be associated with Tricholoma terreum. In Sweden, wefts on plants growing under Beech trees have been typed to T. saponaceum and T. columbetta. In N. America plants determined as M. hypopitys have been DNA profile-linked to T. portentosum, T. flavovirens, T. sejunctum and T. squarrulosum (Leake et al, 2004, Bidartondo et al, 2001). It is not known yet for certain, whether the association of particular species of Tricholoma with Monotropa is due to cryptic genetically specialized forms of Monotropa, or whether it just happens that the only Tricholoma species available at any one site are tied to particular tree species via their mycorrhizal associations. What needs to be done, is for seed from Monotropa plants known to be tied to particular Tricholoma species, to be spread around in the vicinity of other Tricholoma-tree host couplings to see if they will stimulate and maintain germination. In experimental studies it has been shown that following an initial germination to form a small linear axis of tissue, no further development can take place unless the fungal symbiont connects with the seedling and initiates a mycorrhizal mat of hyphae around the developing axis. It then takes around two years of tapping resources from the tree to acquire enough carbon for the development of a bud that will eventually produce a flowering spike. Although Monotropa has a trace of chlorophyll a, it has no chlorophyll b, and cannot fix atmospheric carbon dioxide by photosynthesis. Because it would appear that the relationship is all one sided, Monotropa is often said to be a mycoparasite.

In addition to the post 2001 work on the association of Monotropa with a range of specific Tricholoma-host tree couplings, M. hypopitys sensu lato has been variously split up over the years, on the basis of morphological and chromosome number differences, into two separate species M. hypopitys (2n=48) and M. hypophegea (2n=16), more recently demoted to two subspecies. However according to Stace, 1997 there is so much variation that the only characters that appear to be consistently coupled together are a chromosome number of 2n=48 with pubescence of the stamens, carpels and the inside surface of the petals; and one of 2n=16 together with glabrous surfaces of these organs. As yet too little information is available to determine whether these two taxa are correlated in any way with specific Tricholoma species or tree associates.

Our ignorance also extends to a lack of knowledge about how the associations are set up in the first place. In the case of the common broomrape Orobanche minor, which parasitizes amongst other species, Red Clover Trifolium pratense, by forming haustoria directly with its roots, it responds to chemical exudates from the Red Clover. When the clover suffers a reduced supply of phosphorous it has adapted to release compounds known as sesquiterpene stigolactones which stimulate hyphal branching in arbuscular mycorrhizal fungi so that it can use the fungi to scavenge phospohorus from the soil. The Orobanche has in turn adapted to use these compounds to detect the nearby roots of Red Clover and can then home in on, and parasitise the red clover, by establishing haustoria (Yoneyama et al, 2006).

There are therefore several possibilities for chemical signalling in the case of Monotropa. Maybe the Monotropa seeds secrete a chemical that mimics a chemical signal secreted by the tree to ‘invite’ the mycorrhizal fungus to associate with its roots. This would seem to me unlikely for such a tiny seed with such limited resources, unless there are captive substances in the seed coat that mimic the root surface, and the fungal hyphae come across the seeds by chance as they grow through the soil. Such a strategy might explain why in experimental germinations with seeds buried in various locations, those buried near existing patches of mature Monotropa plants seem to be more successful, - only to be expected if the seeds have landed in up in Tricholoma territory.

Monotropa in Essex

There are Essex records for Monotropa in the 1880s; from Danbury, found by Thomas Benson; in two places at Debden, George Gibson; and there is a specimen that should be in the Passmore Edwards Museum collection (now in our store?), collected by Gibson from a patch growing in small quantity under Beech near Audley End in 1884. We must examine this specimen for the presence or absence of pubescence when we can gain access to it. There are also several records from Epping Forest;  James L. English found it on the 26 July 1887. He sent the record by post to William Cole, who unfortunately did not open the letter until JLE had died, so the location was lost. Essex Naturalist 1892. 6. p.131. It was then found by Mr Conway Gould in Great Monk Wood, under hawthorn bushes, (Essex Naturalist 1922. 20.p.109); and again in August 1926, this time under Beech (Essex Naturalist 1926. 22.p.47). As the location was never disclosed, although both Bernard Ward and Percy Thompson new where it was, and as Monk Wood is a huge area, despite a lifetime of searching I have been unable to refind it. In 1954 it was found at the edge of Norsey Wood, Billericay, by Miss N Needham (confirmed Dr D R Crofts), but again was not localized and we have been unable to refind it (Jermyn, 1974).

Our only known site for Monotropa in Essex at the present day is from Grays Chalk Quarry. The first record here was by Brian Ecott, who photographed it on the main floor of the pit in 1970, when the pit was still very much an open site. Ten years later Fred Rumsey found it again on the floor of the quarry, with ‘27 fruiting spikes in a patch c.1m square under hawthorn scrub with a dense ivy layer, next to the path skirting the damp sunken area at the far northern end of the quarry, 1 January1980; and c. 90 flowering spikes 1 August 1981. TQ608,791’. We have been unable to find it on the floor of the quarry since then, but on 24 August 2007 I found a colony with a total of 15 spikes on the lower of two upper ledges to the north west of the main quarry, on chalk talus at the base of a low north facing cliff, growing with Pyrola under Salix cinerea (TQ60537,78938). On the same day, three more colonies were located on the ledge above immediately to the south; 26 spikes under the edge of birch scrub on the upper ledge north west of the main quarry just south of the track, and by a pile of Celcon blocks (60628,78964); with a few more spikes at (60644,78961); and at the eastern end of the ledge near the main quarry, one patch of 9 and another of 8 spikes (60657,78960 & 60680,78912). On 24 July 2008, 42 spikes were counted at the first site, and 104 spikes on the upper ledge. During our EFC mycology group visit on 15 October 2008 we found a scattering of Tricholoma cingulatum fruit bodies in association with all the Monotropa patches (see photo Fig.XXX). The 2009 season was apparently a bumper one for Monotropa all over the country, and Grays was no exception, new warden Adam Taylor’s team finding 32 spikes on the lower ledge and no less than 391 on the upper ledge, mostly at the western end. Interestingly, I noted that on the lower ledge in 2009, the spikes were roughly forming a ‘fairy ring’ suggesting they were associating with the leading edge of the expanding fungal mycelium. All the spikes looked at had glabrous flower parts, which would suggest subspecies hypophegea, but the perianth segments are hairy on the outside! and we have yet to do a chromosome count. The flowers of Monotropa are radially symmetrical, pendulous, and somewhat bell-shaped, (Fig. XXXX) with 4-5 pale ochre-yellow petals and sepals separated right to the base of the flower, the latter being saccate at the base enabling bumble bees, its main pollinator, to gain access to nectaries at the base of the 4-5 lobed superior ovary. The 8-10 stamens and large disc-like stigma are bright yellow. Contrary to earlier claims, recent work has shown that they are largely out-cross pollinated (Klooster & Culley, 2009). The somewhat succulent whitish to brownish-yellow stem is clothed in yellowish brown-tipped scales, effectively camouflaging the spikes. The seeds are minute, elongated, dust-like and even smaller than those of orchids and broomrapes, although they are not related to either group. Instead they clearly belong to the Ericaceae and are closely related to Pyrola which has almost identical seeds and seed pods.

According to accounts of occurrences elsewhere, Monotropa is generally associated with fairly deep leaf litter in dark or at least shaded sites either on calcareous soils, under Beech or Hornbeam, on dunes in association with Salix repens, or on acid soils under pines. It has also been found under Oak and Hazel. There have also been two reports of it growing on recently established sites under Salix cinerea over pulverized fuel ash (Henrici, 2008). Intriguingly, all our Grays Chalk Quarry sites are on virtually bare, but soft upper chalk rock, that has in the recent past been strewn with dumped pulverized fuel ash building blocks, most of which have now disintegrated. The relatively recently established scrub is dominated by Salix cinerea subsp. cinerea, in association with S. caprea, Cornus sanguinea, Betula pendula and young Quercus ilex. The ground flora consisting of an almost continuous cover of the equally rare Pyrola rotundifolia var. rotundifolia, and scattered Neottia (Listera) ovata, Twayblade and Dactylorhiza fuchsii, Common Spotted Orchid; plus a few plants of Hypericum hirsutum, Origanum vulgare and Brachypodium sylvaticum.  Only in one spot was the substrate other than a granular mix of chalk and pulverized fuel ash, and that was a mound of rotting wood chips with a cluster of 20 spikes and a few T. cingulatum fruitbodies.

Elsewhere it has been recoded in c.270 x10k sqs. in England Scotland and Wales, since 1930, and c.130 since 1987.  Its distribution is closely correlated with calcareous soils, but it thins out rapidly north of a line from  Barrow to Scarborough, suggesting a northern climatic limit, possibly Summer temperatures, as it is mostly south of the 1901-1930 July mean isotherm of 60oC (15.6oC).

As it is such a rare plant in Essex, any additional records would be welcome. Particularly if it can be found under Beech or Hornbeam, when I suspect, it is likely to be subsp. hypopitys. If anyone does find it, please be sure to note what it is growing under, and whether or not the insides of the flowers are hairy.

Acknowledgements

Many thanks to Brian Ecott and Fred Rumsey for details of their finds, to Mary Smith for identifying the Tricholoma cingulatum, and to Adam Taylor and his team for carrying out the meticulous 2009 counts of flowering spikes. 

References

BIDARTONDO, M I & BRUN, T D (2001) Extreme specificity in epiparistic Monotropoideae (Ericaceaea): widespread phylogenetic and geographical structure. Molecular Ecology 10: 2285-2295. 

GIBSON, G S (1862) Gibson’s Flora of Essex. William Pamplin. London. 

HENRICI, A (2008) Notes & Records. Tricholoma species with Monotropa. Field  Mycology. 9(4)139-141.

JERMYN, S T (1974) Flora of Essex. Essex Naturalist Trust. Colchester.                                                                                                                                                        

KAMIENSKI F. (1881) Die Vegetationsorgan de Monotropa hypopitys L.   Vorlaufige Mittheilung. Botanische Zeitung 39: 458-461.  

KLOOSTER, M R & CULLEY T M (2009) Comparative analysis of the reproductive ecology of Monotropa and Monotropsis: Two mycoheterotrophic genera of the Monotropoideae (Ericaceae). American Journal of Botany 96: 1337-1347.

LEAKE, J R, McKENDRICK, M, BIDARTONDO, M & READ D J  (2004) Symbiotic germination and development of the myco-heterotroph Monotropa hypopitys in nature and its requirement for locally distributed Tricholoma spp. New Phytologist 163: 405-423.

STACE, C (1997) New flora of the British Isles. 2nd edition. Cambridge University Press.

YONEYAMA, K (x2), SEKIMOTO, H TAKEUCHI (2006) Strigolactones, chemical signals for parasitism and symbiosis, from dicotyledonous plants. In: 11th IUPAC International Congress of Pesticide Chemistry. Kobe, Japan.