Richard Bateman on stability and change

Richard Bateman
Still looking for any hints to shed some light on the albiflora phenomenon, I visited Richard Bateman in London. The white-flowered morphs “are of greatest interest to me because of their relative frequencies in the diploid and the tetraploid groups of Dactylorhiza”, he told me. “If your mind works its ways through the different diploids – incarnata, fuchsii, sambucina – they all show colour polymorphism. And they all have a certain number of very pale or white individuals.” Quite different are the observations with tetraploid Dactylorhiza species like praetermissa, majalis or alpestris. Bateman noted: “I’ve only found one albino praetermissa and one albino traunsteinerioides in 30 years of going in the field.” Quite younger is the project – but up to now only some scattered findings of white-flowered Dactylorhiza majalis have been reported – and none of praetermissa or traunsteineri. As a possible explanation Bateman noted: “Presumably, in the tetraploids there has to be a minimum of four copies of a gene that is malfunctioning to cause the albinism. So I think the tetraploids are buffered against albinism by having additional copies of the genes that generate the anthocyanin pigments.”

Arguing with him about the negative connotations of the term malfunction, Bateman answered: “Most organisms are ‘designed’ to remain the way they are and not to change [substantially]. So, from a genetic viewpoint, any change that is expressed is a malfunction. I agree the malfunction could be beneficial rather than negative but most times it’s negative.”

Bateman’s main interests in research are the questions of speciation or at least the question of what might lead to evolutionary divergence between populations: “The genus level – for me at least – is solved. The species level interests me the most now. That’s were the most challenging topics still have to be addressed – how orchids speciate.” Despite a huge literature on the topic, Bateman noted, those questions are still not adequately solved. “Each time I address a particular set of orchids, the answer [to this question] is different.” So up to now, no generalization is possible. But, Bateman said, “I strongly believe that the importance of pollinator [specificity] is being exaggerated by a lot of workers.”

At least one general observation can be stated according to Bateman: “New [evolutionary] strategies are tried out constantly – more than most people believe – but I think they succeed less often than most people believe.”

In addition to such reflections on stability and change in the genetics of orchids, we wondered why hypochrome forms of Ophrys are rather green than white – obviously the Ophrys flowers still contain chlorophyll even if they lack the anthocyanins – and with good reason: “The rosette leaves of Ophrys (and Himantoglossum as well) tend to be dead before the flowers properly open”, Bateman said. “So I don’t think there is much supply of nutrient coming from [root to flower]. The flower has become autonomous … whereas in Orchis or Anacamptis the flowers are far less independent.” So, Ophrys flowers are quite special. “One of the most striking things when you start working on the flowers, cutting them up looking at them under microscope, you realize how much energy is invested in an Ophrys flower. There is a lot of tissue.”

After the visit, the Royal Botanical Gardens in Kew have been the very right place to further contemplate on the miracles of nature. (With thanks to Richard Bateman for reviewing his quotes, additional notes are marked with brackets)
Kew Gardens

Colour AND form variety of Anacamptis morio

Anacamptis morio
Oops, that’s a quite special Anacamptis morio which Norbert Griebl has found near Sittendorf, southwest of Vienna. In addition to the absence of anthocyanins (which happens quite often with this species) the lip has the same form as the sepals, with green veins. Here, not only the colour of the flower has changed, but also its morphological pattern.

Colour plays with Nigritella rhellicani

Nigritella rhellicani
In July, the dark red heads of Nigritella rhellicani (syn: Nigritella nigra ssp. rhellicani) are covering many alpine meadows. In some rare places, the flowers show remarkable colour variatation. After studying the Nigritella hues of the Dolomite Alps, this year I visited the Swiss canton Valais: Near Chandolin there is a place in an altitude of about 2400 m with pink and yellow flowering Nigritella rhellicani. The tableau above shows the colour varieties in both the Dolomites and Switzerland. The yellow flowering forms grow near Chandolin – they obviously miss the anthocyanins, but have other pigments as probably carotenoids. The reasons for this special forms are unknown up to now.
Nigritella rhellicani

Albiflora studies on the Crimean Peninsula

Orchis simia
Exploring the Crimean Pensinsula for orchids, species like Comperia comperiana, Steveniella satyrioides or Orchis punctulata are especially noteworthy. Albiflora forms, though, are quite rare in this Ukrainian region. Vladimir Isikov of the Nikita Botanical Garden told me that he has seen only three species with white-flowered forms: Orchis simia, Neotinea tridentata and Anacamptis morio ssp. caucasica (which he referred to as Orchis picta). Obviously there are no orchid species on the Crimean Peninsula heading to a direction which favours white flowering.

But near тылобое (Tylovoye) we found an edge of a forest with a group of 26 Orchis simia under a pine and 5 albiflora plants among them. In this small population there was obviously some kind of reproduction of the white-flowered plants.

Neotinea tridentata has a marked variability, as it is also noted by H. Kretzschar, W. Eccarius and H. Dietrich in their book „Die Orchideengattungen Anacamptis, Orchis, Neotinea“ (Buergel 2007, p. 206/207). On the Crimean Peninsula the dominant colour of flowers is light purple. I’ve found 3 white flowered plants, which led me to a rough estimate of 2 albiflora plants per 1000 Neotinea tridentata.
Neotinea tridentata

Among the Anacamptis morio, Orchis mascula, Orchis purpurea or Anacamptis pyramidalis seen on our 10-day-trip there have been no white-flowered plants. But in a forest near гончарное (Goncharnoye) there was an albino form of Epipactis helleborine.
Epipactis helleborine

Beyond the orchid flora I noticed white flowers of Polygala major, the endemic Onosma taurica and Papaver spec. Interesting was also a Polygonatum odoratum with half white leaves.
Polygonatum odoratum

Colour influences pollinator behaviour

The Flower of the European Orchid

Form and function of the flower organs are the main focus of the new fascinating book The Flower of the European Orchid by Jean Claessens and Jacques Kleynen. Illustrated by great macro as well as microscopic photos this important opus presents a comprehensive description of the structure of orchid flowers with the different European genera. In a foreword, Richard Bateman writes: „No other family of plants can match the orchids for their sheer charisma“. But the excitement goes along with a certain scientific pain – Bateman stresses that there still remain major scientific uncertainties which „further torment us“ – among them questions of evolutionary adaptation.

The orchids’ strategies of fertilization are manifold and the book explains how the specific construction of the column (gynostemium) supports allogamy by pollinators or autogamy (self-fertilization). Especially intriguing are the strategies of Dactylorhiza, Orchis and other genera without any nectar in the spur. Claessens and Kleynen explain that the pollinators of Orchis mascula are „recently emerged, naïve bees or exploratory insects that have not yet learned that the flowers offer no reward” (p. 220). The authors also cite the study of L. Dormont, R. Delle-Vedove, J.-M. Bessière, M. Hossaert-Mc Key und B. Schatz about the presence of white-flowered Orchis mascula which underlines „the importance of visual cues for attracting pollinators“ (p. 220).

In the Dactylorhiza chapter the authors write: „Colour can also influence pollinator behaviour“ (p. 240). With regard to the red and the yellow forms of Dactylorhiza sambucina they refer to experiments showing that experienced bumblebees „preferred by far the morph that most resembled the rewarding plant on which they have fed previously“. Vice versa it may be presumed that there may be a form of evolutionary adaptation directed to develop visual cues which are different from non rewarding plants being abundant in a certain region – as it could be the case in Western Ireland with the many white-flowered forms of Dactylorhiza fuchsii on meadows with earlier flowering Orchis mascula.

Ophrys speculum f. flavescens

In the latest issue of “Berichte aus den Arbeitskreisen Heimische Orchideen” (27/2, 2010), Klaus Boie presents a rare hypochrome form of Ophrys speculum in his article about orchid-findings in western Andalusia (p.117-122). He found this forma flavescens in the Spain region of Andalusia, in the midst of a large group of Ophrys speculum, as he writes.

The marking of the labellum is just white, the other parts of the flower are yellowish-green. As with other hypochrome forms of Ophrys, the photo shows a total lack of anthocyanins. But the flower has still chlorophyll embedded – in contrast to albiflora forms of other orchid genera with their their pure white flowers. Probably the Ophrys species need the flower’s contribution to photosynthesis, because the leaves of the rosette are withering at an early stage.

Albiflora plants influence naïve pollinators

White-flowered orchid varieties are not just a “freak of nature” – they have quite obviously some biological function. A group of scientists in Montpellier in Southern France has found that the existence of albiflora plants in a population of Orchis mascula is connected with a much higher fruit set of the purple-flowered plants than in populations where there are no white-flowered Orchis mascula:

“Surprisingly, our study showed that the presence of co-occurring white-flowered individuals led to significantly higher reproductive success of nearby purple-flowered individuals (mean fruit set 27%), while white-flowered plants themselves had the same low fruit set (6%)”, the authors of the study – L. Dormont, R. Delle-Vedove, J.-M. Bessière, M. Hossaert-Mc Key and B. Schatz – wrote in their article in New Phytologist (2010) 185: 300–310. The flowers studied – overall 11 709 at 805 plants – showed almost the same increased fruit set when the researchers planted some ping-pong balls which mimic the white Orchis mascula inflorescences: “The effect was virtually identical in magnitude (fruit set increased from 6 to 27%), whether the nearby white-coloured object was an O. mascula inflorescence or a ping-pong ball.” The nearer a purple-flowered plant to the white colour, the higher was the fruit set developed due to a successful pollination.

The authors explain their surprising results with pollinator behaviour after visiting Orchis mascula who belongs to the food-deceptive orchids: “It seems plausible to suppose that after unrewarding visits to purple flowers, naïve pollinators probably avoid homogeneous populations of purple flowers, and may then preferentially orient to a different colour or to a colour contrast such as a mix of white and purple flowers.” Pollinators of Orchis mascula are bumblebees (Bombus, Psithyrus), solitary bees (Eucera, Nomada, Andrena, Apis) and the beetle Cetonia aurata.

The albiflora varieties are quite rare in the populations studied in Southern France: The authors counted 0.9 to 1.4 percent in different populations. But this is much higher than the percentage which could be assumed in the case of spontaneous mutations affecting floral pigmentation genes with an average of just 0.1 percent. Regarding the higher percentage of albiflora varieties with Orchis mascula the authors state that “it is unlikely that such high frequencies could be the result of repeated spontaneous mutations alone” – and this should also apply to the case of other orchid species with a higher percentage of white-flowered plants like Anacamptis morio or Dactylorhiza fuchsii in Western Ireland.

The white-flowered Orchis mascula themselves have only a low fruit set, but they “help” the purple-flowered plants of their species to be pollinated. “In O. mascula, the presence of whiteflowered variants might be regarded as an adaptation that benefits the purple-flowered relatives of white-flowered morphs, rather than providing a direct benefit to whiteflowered individuals”, the authors wrote and assumed that there is some “mechanism of kin selection” responsible to grant a higher percentage of albiflora plants.

The scientists in Montpellier are pursuing their research with other species as well. Laurent Dormont wrote me that they have also studied white-flowered plants of Calanthe sylvatica on the Caribbean island of La Réunion (the results to be published in Plant Systematics and Evolution and also the floral volatiles of white-flowered orchis species.

Cephalanthera rubra f. albiflora revisited

Cephalanthera rubraThis year I had the chance to visit the white flowering form of Cephalanthera rubra in the Hesse part of the Rhoen some days earlier than last year. But first I followed a hint and looked up a place further in the South, near Ahlersbach. Quite near a path through the forest a white Cephalanthera rubra with a slight hue of pink! The pink colour is well visible in the buds, where the remaining pigments are more concentrated than in the opened flower.

Cephalanthera rubraAt the second place near Huenfeld, characterized by an old beech mentioned by Marco Klueber in his great book about “Orchids in the Rhoen” the albiflora plants of Cephalanthera rubra are splendidly flowering. The Swedish botanist L. Anders Nilsson showed (in an article in Nature, 1984) that Cephalanthera rubra mimics the floral coloration of Campanula in the visual system of bees in order to be pollinated by them, especially by male bees of the genus Chelostoma. Since Cephalanthera rubra is flowering before Campanula, they are quite attractive for the bees. It would be interesting to see how bees are reacting to the albiflora forms of Cephalanthera rubra.

With regard to pollinators my visit on June 24th had a special highlight when I saw a wasp (Argogorytes mystaceus) pollinating Ophrys insectifera. The insect pseudocopulated two flowers in a timeframe of more than seven minutes.

Even more fuchsii diversity

Dactylorhiza fuchsiiDactylorhiza fuchsiiSimilar to The Burren there are also some continental locations where Dactylorhiza fuchsii tends to develop white or at least bright flowers. In the Belgian province of Liège, near Lanaye, there are dozens of albiflora forms of this species, as Jeroen Gerdes told me – he sent me the photo at the left.

Today I visited a meadow near Biebergemuend in the Hesse part of the mountain range called Spessart. On a space of about 5,000 square meters I counted about 300 Dactylorhiza fuchsii with the following distribution of flower colours (in per cent):

Dactylorhiza fuchsii with %
dark pink flowers 2
medium pink flowers 6
bright pink flowers 45
white flowers and labellum marking 44
white flowers without marking 3
total 100

In total 10 of about 300 Dactylorhiza fuchsii are albiflora forms – such a frequency is quite higher than usually observed with this or other orchids species and leads to the assumption that there might be some gradual or saltational evolution under way.

Dactylorhiza fuchsii x majalis Among the other plants in this area I noted Dactylorhiza majalis (withered), Dactylorhiza fuchsii x majalis, Platanthera bifolia, Neottia ovata, Rhinanthus minor, Cirsium arvense, Campanula persicifolia, Picris hieracioides and Arnica montana. Dactylorhiza majalis grows in the neighbourhood of wet ditches along the meadow – and there are also hybrids of D. majalis and D. fuchsii – still flowering while D. majalis is already withered. The hybrids are rather strong, some of them with a height of up to 50 cm. They can easily be determined by their broad leaves and the rounded labellum of the flowers with a reduced medium lobe. There is also an albiflora form of Dactylorhiza fuchsii x majalis (right).

Albiflora studies in Ireland

Dactylorhiza fuchsii
The evolution of certain orchid species is far from being finished. The Burren, a region in County Clare at the Western coast of Ireland, illustrates this fact by its manifold colour varieties of Dactylorhiza fuchsii. In 1988, R.M. Bateman and I. Denholm, came to the result that the Burren populations of Dactylorhiza fuchsii show more often a lack of the purple pigment anthocyanin than plants in other regions of the British Isles:

Percentage of Dactylorhiza fuchsii lacking Burren other regions
leaf markings 43 13
labellum markings 48 15
labellum anthocyanins 48 12
all floral anthocyanins 35 8
all anthocyanins in flowers, stem, leaves and bracts 25 6

(Source: R.M. Bateman/I. Denholm: A reappraisal of the British and Irish dactylorchids, 3. The spotted-orchids. In: Watsonia 17 (1988), p.332)
When exploring the fascinating area around the Lough Gealain and the Mullaghmore mountain these results seem to be quite realistic. In other areas as well there are many plants, which have bright or white flowers but still retain anthocyanins visible in the markings of the labellum. In a limited area of 40 square meters in the region of Rockforest, northeast of Corrofin, I counted 50 flowering Dactylorhiza fuchsii (in addition to 7 with buds) with the following characteristics:

Dactylorhiza fuchsii with
dark pink flowers 0
medium pink flowers 11
bright pink flowers 17
white flowers and line markings 3
white flowers and dot markings 17
white flowers without markings 2
total 50

Among the other plants in this area in the middle of a vast limestone pavement there are Orchis mascula, Geranium sanguineum, Rosa pimpinellifolia, Calluna vulgaris, Lotus corniculatus and Pteridium aquilinum.

The following image illustrates the broad variety not only of colours but also of the labellum forms of Dactylorhiza fuchsii in The Burren (some of the examples obviously showing a certain introgression with Dactylorhiza maculata). It becomes clear that most plants have less floral anthocyanins than continental populations of the species – for example the large forest populations in the French region Causses with its deep pink flowers. The pigments are first reduced in the sepals. This reduction continues in the base colour of the labellum. Then the markings of the labellum are reduced, often only a small rest is retained at the mouth of the spur. Even the very white flowers still have coloured pollinia but their colour is less intense. There is also a wide variety of labellum forms. Especially the central lobes largely differ. And there is the extreme case of a white flowering plant whose lateral lobes are reduced to a minimum (lowest row in the middle).
Colour varieties of Dactylorhiza fuchsii
Most Irish and British botanists stress that the Dactylorhiza fuchsii var. okellyi (some authors view this as subspecies or even as species) must not be mixed up with the albiflora forms of fuchsii. Anne and Simon Harrap (Orchids of Britain and Ireland, Dactylorhiza fuchsii ssp. okellyi 2005) are writing: “A lot of controversy surrounds okellyi” and explain: “In The Burren and elsewhere these classic white-flowered okellyi are just part of a population of plants with a variable flower colour”. Brendan Sayers and Susan Sex (Ireland’s Wild Orchids, 2008) stress that Dactylorhiza fuchsii var. okellyi flowers late, beginning in July. The photo in their field guide shows a flower with a labellum, which is deeply divided into three lobes. Charles Nelson (Wild Plants of The Burren and the Aran Islands, 2008) indicates that Dactylorhiza fuchsii f. okellyi flowers from June to August and has pure white flowers “without any pink tints or marks” and a “lip flat with 3 almost equal, deeply-cut lobes”. According to Pierre Delforge (Guide des orchidées d’Europe, 2005), who mentions a flowering period from May to July, the labellum has a maximum width of 8 mm (in contrast to fuchsii with 8-16 mm). Pat O’Reilly and Sue Parker (Wild Orchids in The Burren, 2007) have noted that “groups of pure-white orchids … are more likely to be O’Kelly’s Spotted-orchids than single plants, which might be just very pale examples of the Common Spotted-orchid”. When exploring the limestone pavements between Poulsallagh and Rockforest you’ll find lots of white-flowered Dactylorhiza fuchsii, rather small and with a pyramidal spike in the beginning of flowering, which are very similar to pink-flowered plants of the species – they should be considered as albiflora forms. Two times I found a pair of taller plants, very slender and with a distinct appearance of spike or flowers, which could be addressed as Dactylorhiza fuchsii var. okellyii.

Dactylorhiza maculata also tends to develop very pale flowers in The Burren. But most of them retain at least a faint marking on the labellum. The variety of Dactylorhiza maculata (the plants in Ireland are in general addressed as Dactylorhiza maculata ssp. ericetorum) seems to be not so wide as the variety of Dactylorhiza fuchsii. The relative frequency of Orchis mascula f. albiflora is in the same range as in continental Europe. Among thousands of plants – Orchis mascula being the most frequent orchid of the region – I’ve seen just two white ones. And there wasn’t one single albiflora form of Dactylorhiza incarnata or Dactylorhiza majalis ssp. occidentalis (on the Aran Island of Inisheer).

Compared with the relative stability of the other plants, the broad variability of Dactylorhiza fuchsii in The Burren clearly shows that this species is still in a state of an ongoing evolutionary process. It can only be speculated why Dactylorhiza fuchsii in The Burren prefers brighter or even white flowering – in the midst of an abundance of pink and purple flower colours on the meadows of the region.