Editing Ophrys apifera

{{short description|Species of flowering plant in the orchid family Orchidaceae}}
{{For|other plants also called "bee orchid"|Bee orchid (disambiguation){{!}}bee orchid}}

{{Speciesbox
| image = (MHNT) Ophrys apifera - Villeneuve-lès-Bouloc - Flower.jpg
| image_caption =
| genus = Ophrys
| species = apifera
| authority = [[William Hudson (botanist)|Huds.]]
| synonyms = 
* ''Orchis apifera'' <small>(Huds.) [[Richard Anthony Salisbury|Salisb.]]</small>
*''Arachnites apifera'' <small>(Huds.) [[Georg Franz Hoffmann|Hoffm.]]</small>
*''Ophrys chlorantha'' <small>[[Johannes Jacob Hegetschweiler|Hegetschw.]] & [[Oswald Heer|Heer]]</small>
*''Ophrys insectifera'' var. ''andrachnites''
| synonyms_ref = <ref>{{cite book |title= The Vascular Flora of the National Park of Abruzzo, Lazio and Molise (Central Italy): An Annotated Checklist Geobotany Studies |author1= Fabio Conti|author2=Fabrizio Bartolucci |edition= illustrated |publisher= Springer |year= 2015 |isbn= 9783319097015 |page= 124}}</ref>
}}

'''''Ophrys apifera''''', known in Europe as the '''bee orchid''', is a [[perennial plant|perennial]] [[herbaceous plant]] of the genus ''[[Ophrys]]'', in the family of [[Orchidaceae]]. It serves as an example of [[Sexual mimicry#Interspecific deceptive mimicry|sexually deceptive pollination]] and floral mimicry, a highly selective and highly evolved plant–pollinator relationship.<ref>[http://rspb.royalsocietypublishing.org/content/royprsb/279/1748/4786.full.pdf Royal Society – Pre-adaptations and the evolution of pollination by sexual deception: Cope’s rule of specialization revisited]</ref>

== Description ==
[[File:Illustration Ophrys fuciflora0.jpg|left|thumb|266x266px|Illustration of leaf and flower morphology for ''Ophrys apifera'' (left) and ''Ophrys fuciflora'' (right)]]
''Ophrys apifera'' grows to a height of {{convert|15|-|50|cm|0}}. This hardy orchid develops small rosettes of [[leaf|leaves]] in autumn that continue to grow slowly during winter. Basal leaves are ovate or oblong-lanceolate, and upper leaves and bracts are ovate-lanceolate and sheathing. Leaves exhibit parallel venation. 
The plant blooms from mid-April in continental Europe, but in the [[United Kingdom]] it flowers June to July. A flower spike is produced, composed from one to twelve flowers. Three large, purple [[sepal]]s surround the base of the flower, which can easily be mistaken for [[petal]]s. The true petals lie just above the sepals as two short, pubescent green structures protruding laterally from a central column. A third, modified petal, the [[Labellum (botany)|labellum]], sits at the bottom of the column as a landing pad for pollinators. The labellum is trilobed, with two pronounced humps on the hairy lateral lobes and a hairy median lobe having a pattern that mimics the abdomen of a [[bee]].<ref name="Ray-2015">Ray, H. & Wagner, V. (2015). “Orchid pollination biology”. Environmental Horticulture Department, UF/IFAS Extension (ENH1260). https://edis.ifas.ufl.edu/pdffiles/EP/EP52100.pdf</ref> The pattern of labellum colouration is quite variable.

The central column is an adaptation unique to orchids, in which the stamens and pistil fused together to form one central rib.<ref name="Ray-2015" /> The anther cap can be found at the top, dorsal side of the column, while the stigma is hidden below on the ventral side. Two [[Pollinium|pollinia]] hang from the column over the labellum.

== Distribution ==
''Ophrys apifera'' is widespread across central and southern Europe, as well as North Africa and the Middle East. Its range stretches from [[Portugal]], [[Ireland]] and [[Denmark]] east to [[Iran]] and the [[Caucasus]]. It is quite common in the [[Mediterranean region]] eastwards to the [[Black Sea]],<ref>{{cite web|url=http://apps.kew.org/wcsp/namedetail.do?name_id=140745|title= World Checklist of Selected Plant Families}}</ref> (Codes) <ref>{{cite web|url= http://www.nhm.ac.uk/hosted_sites/tdwg/TDWG_geo2.pdf |title=World Checklist of Selected Plant Families TDWG Geocodes}}</ref> but is less common in its northern range being uncommon or local in [[Germany]] and Ireland.

In the United Kingdom, it has a distinct southeastern preference, being more common in England. Recently it has been found in the southwest of England in [[Butleigh]] near [[Glastonbury]] in [[Somerset]] and Dorchester, Dorset; whereas it is only to be found in coastal regions of [[Wales]] as well as the [[Hodbarrow Nature Reserve]] in [[Millom]], Cumbria,<ref>{{cite web|url=http://www.rspb.org.uk/reserves/guide/h/hodbarrow/index.aspx|title=The RSPB: Hodbarrow|work=The RSPB}}</ref> and some parts of [[Northern Ireland]]. It is relatively common in the northeast of England and in recent years large numbers have appeared in the grass verges surrounding the [[MetroCentre (shopping centre)|Metro Centre]] in [[Gateshead]].<ref>{{cite web|url=http://www.journallive.co.uk/north-east-news/todays-news/2008/06/21/orchid-colony-discovered-in-grass-verge-61634-21129155/|title=Orchid colony discovered in grass verge|author=Tony Henderson|date=21 June 2008|work=journallive|url-status=dead|archive-url=https://archive.today/20130421005112/http://www.journallive.co.uk/north-east-news/todays-news/2008/06/21/orchid-colony-discovered-in-grass-verge-61634-21129155/|archive-date=21 April 2013}}</ref> In [[Scotland]], it was thought to be extinct, but was rediscovered in [[Ayrshire]] in 2003. In some countries the plants have protected status. They are unusual in that in some years they appear in great numbers, then sometimes only reappear after an absence of many years.

The genus ''Ophrys'' is the most species-rich (i.e. diverse) genus of orchids in Europe and the Mediterranean with over 200 species, according to ''Orchids of Britain and Europe'' by Pierre Delforge.

== Habitat and ecology ==
''Ophrys apifera'' generally grows on semi-dry [[Sod|turf]], in [[grassland]], on limestone, calcareous dunes or in open areas in woodland. It prefers well-drained calcareous soils, low in nutrients, in bright light or dim light.<ref name="livrepository.liverpool.ac.uk">[https://livrepository.liverpool.ac.uk/3022579/ PhD Thesis of the University of Liverpool – Diversity and Roles of Mycorrhizal Fungi in the Bee Orchid Ophrys Apifera]</ref> It is a major colonizer of sites disturbed by human activity, such as old quarries, roadside verges and airfields.<ref name="n1500">{{cite book|author=I. F. La Croix|title=The New Encyclopedia of Orchids: 1500 Species in Cultivation|publisher=Timber Press|year=2008|isbn=9780881928761|edition=illustrated|page=320}}</ref><ref>{{cite book |title= Ecological Engineering: Bridging Between Ecology and Civil Engineering |editor= Hein van Bohemen |publisher= Uitgeverij Æneas BV |year= 2005 |isbn= 9789075365719 |page= 224}}</ref> ''O. apifera'' is one of the most likely European orchid species to establish itself within towns and cities.

In order to extract sufficient nutrients from the substrata it grows in, ''Ophrys apifera'' relies upon a symbiotic relationship with [[mycorrhizal fungi]] in the genus ''[[Tulasnella]]'', and possibly other genera.<ref>{{cite journal | url=https://onlinelibrary.wiley.com/doi/full/10.3732/ajb.0900354 | doi=10.3732/ajb.0900354 | title=C and N stable isotope signatures reveal constraints to nutritional modes in orchids from the Mediterranean and Macaronesia | date=2010 | last1=Liebel | first1=Heiko T. | last2=Bidartondo | first2=Martin I. | last3=Preiss | first3=Katja | last4=Segreto | first4=Rossana | last5=Stöckel | first5=Marcus | last6=Rodda | first6=Michele | last7=Gebauer | first7=Gerhard | journal=American Journal of Botany | volume=97 | issue=6 | pages=903–912 | pmid=21622461 }}</ref><ref name="livrepository.liverpool.ac.uk"/>

Bee orchids are threatened by mowing during flowering, or before the seed has been released. However, they often also disappear from sites that become overgrown with shrubs and/or trees, as the orchids fail to compete with these large plants for light. For these reasons, bee orchids are often found on the edge of mown areas, beside paths or within areas that are mown very infrequently. The Sussex Wildlife Trust recommends mowing at the end of July and removing the cuttings to benefit bee orchids.<ref>[https://www.suffolkwildlifetrust.org/beeorchids Suffolk Wildlife Trust – Bee Orchids]</ref> In prehistory, the species presumably relied upon seasonal grazing pressure, or was limited to early succession habitats and permanent grassland.
[[File:Bee Orchid - Ophrys apifera (11776055286).jpg|thumb|266x266px|Flower of ''Ophrys apifera''. Sepals, petals, labellum, column, and pollinia are all visible.]]

== Reproduction ==

''Ophrys apifera'' has been considered to preferentially practice [[self-pollination]].<ref>{{cite book |title= The Correspondence of Charles Darwin:, Volume 14; Volume 1866 |author= Charles Darwin |editor1= Frederick Burkhardt|editor2=Duncan M. Porter|editor3=Sheila Ann Dean|editor4=Shelley Innes|editor5=Samantha Evans|editor6=Alison M. Pearn|editor7=Andrew Sclater|editor8=Paul White |edition= illustrated |publisher= Cambridge University Press |year= 2004 |isbn= 9780521844598 |page= 129}}</ref><ref>{{cite book |title= The Various Contrivances by which Orchids are Fertilized by Insects |author= Charles Darwin |edition= second |publisher= D. Appleton and Company |year= 1898 |page= 52}}</ref> The flowers are almost exclusively self-pollinating in the northern ranges of the plant's distribution, however pollination by the [[solitary bee]] ''[[Eucera longicornis]]'' occurs in the Mediterranean region, where ''Ophrys apifera'' is more common. ''E. longicornis'' males have been observed attempting to copulate with the flowers,<ref>{{cite journal|last1=Fenster|first1=Charles B.|last2=Marten-Rodrıguez|first2=Silvana|year=2007|title=Reproductive Assurance and the Evolution of Pollination Specialization|url=http://english.xtbg.cas.cn/rh/rp/200905/P020090810528272663000.pdf|journal=International Journal of Plant Sciences|volume=168|issue=2|pages=215–228|citeseerx=10.1.1.476.8678|doi=10.1086/509647|s2cid=1890083 |access-date=2 September 2013}}</ref> which emit [[allomone]]s that mimic the scent of the female bee. These allomones are also known to attract bee species ''[[Tetralonia cressa]]'' and ''[[Eucera pulveraceae]]''. In addition to chemosensory mimicry, the labellum of the flower acts as a visual decoy that the male bee confuses for a female.<ref>{{cite book |author1=Bill Neal |title=Gardener's Latin |date=1992 |publisher=[[Robert Hale (publishers)|Robert Hale]] |location=London |isbn=0709051069 |page=9}}</ref> It is believed that male bees preferentially select orchids with the most bee-like labellum and attempt copulation, at which point the pollinia stick to the bee during the [[pseudocopulation]].<ref>{{cite journal |last1=Fenster |first1=Charles B.|last2=Marten-Rodriguez |first2=Silvana |title=Reproductive Assurance And The Evolution Of Pollination Specialization |journal=International Journal of Plant Sciences |date=2007 |volume=168 |issue=2 |pages=215–228 |url=http://www.life.umd.edu/biology/fensterlab/PDF/Reproductive%20Assurance%20Reveiw.pdf |doi=10.1086/509647|citeseerx=10.1.1.476.8678|s2cid=1890083 }}</ref><ref>Dawkins, R. (1986) ''The Blind Watchmaker''</ref> This achieves pollen transfer and, potentially, pollination.

''Ophrys'' like other orchids are dependent on [[symbiotic]] [[fungus|fungi]] at some point during their life cycle, but especially for [[germination]], which may take months or even years underground. Orchid roots contain [[orchid mycorrhiza]], coils of fungal hyphae inside orchid root cells.<ref name="schweiger">{{Cite journal |last=Schweiger |first=Julienne M.‐I. |last2=Bidartondo |first2=Martin I. |last3=Gebauer |first3=Gerhard |date=April 2018 |editor-last=Field |editor-first=Katie |title=Stable isotope signatures of underground seedlings reveal the organic matter gained by adult orchids from mycorrhizal fungi |url=https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2435.13042 |journal=Functional Ecology |language=en |volume=32 |issue=4 |pages=870–881 |doi=10.1111/1365-2435.13042 |issn=0269-8463}}</ref>

== Phytochemistry ==
Floral parts display the presence of [[quercetin]] and [[kaempferol]] glycosides, which are supposed to be acylated, as well as cinnamic acid derivatives. The pink outer tepals show the presence of anthocyanins.<ref>Function of floral pigments in the orchid genus Ophrys. Kheim, Doris (2009), Diplomarbeit, University of Vienna ([http://othes.univie.ac.at/3643/ abstract])</ref><ref>Occurrence of flavonoids in Ophrys (Orchidaceae) flower parts. Anastasia Karioti, Christine K. Kitsaki, Stella Zygouraki, Marouska Ziobora, Samah Djeddi, Helen Skaltsa and Georgios Liakopoulos, Flora – Morphology, Distribution, Functional Ecology of Plants, Volume 203, Issue 7, 1 October 2008, Pages 602–609, {{doi|10.1016/j.flora.2007.09.009}}</ref>

== Culture ==
The name ''Ophrys'' derives from the Greek word ''{{lang|el|ophrys}}'', meaning "eyebrow." It is believed that women in ancient Rome used to darken their eyebrows with the orchid plant, thus giving it its name.<ref name="Addam-2015">Addam, K., Takkoush, J., Bou-hamdan, M., & Itani, J. (2015). Five established orchids Ophrys apifera var. Chlorantha, Aurita, Purpurea, Purpurea. F. Alba. and Flavescens (Orchidaceae) in Lebanon as part of the native flora. Journal of Ecology and Environmental Sciences, 6(2), 163–169. ISSN: 0976-9900 & E-ISSN: 0976-9919</ref> The Latin [[specific name (botany)|specific epithet]] ''{{lang|la|apifera}}'' means "bee-bearing" or "bee-bringing"<ref name="Latindict">[http://www.archives.nd.edu/cgi-bin/wordz.pl?keyword=fer WORDS Latin-to-English Dictionary by William Whittaker, AbleMedia Classics Technology Center], accessed 2014-11-13</ref> and refers to the bee-shaped labellum of the orchid.

Its root tubers were ground into a powder called [[salep]] in the Ottoman Empire, which was believed to have nutritional, medicinal, and aphrodisiac values.<ref name="Kasparek-199">Kasparek, M. & Grimm, U. (1999). European trade in Turkish salep with special reference to Germany. Economic Botony, 53(4), 396–406. {{JSTOR|4256222}}</ref> The product's popularity spread to England in the 17th and 18th century and then to a few other European countries. Salep is still used today in medicines and traditional dishes in Turkey, which was formerly the region of the Ottoman Empire, and throughout the Middle East. It is also a popular import in the Netherlands, Cyprus, and Germany for its supposed medicinal properties.<ref name="Kasparek-199" />

''Ophrys apifera'' is the [[County flowers of the United Kingdom|county flower]] of [[Bedfordshire]].<ref>Plantlife website [http://www.plantlife.org.uk/wild_plants/county_flowers/ ''County Flowers page''] {{webarchive|url=https://web.archive.org/web/20150430170312/http://www.plantlife.org.uk/wild_plants/county_flowers/ |date=2015-04-30 }}</ref>

This species has appeared on postage stamps in many countries including [[Belgium]], [[Cambodia]], [[Czech Republic]], [[Germany]], [[Republic of Ireland|Ireland]], [[Israel]], [[Liechtenstein]], [[Luxembourg]], [[Slovenia]], the [[United Kingdom]] and the [[USSR]].<ref>[https://www.google.com/search?rlz=1C1GCEU_enGB820GB820&biw=1524&bih=956&tbm=isch&sa=1&ei=SOkIXce8C-qf1fAPocGQmAM&q=bee+orchid+postal+stamp&oq=bee+orchid+postal+stamp&gs_l=img.3...1007824.1012237..1012545...1.0..0.89.1207.24......0....1..gws-wiz-img.......0i67j0j0i8i30j0i24.KcXgpnUH4sg#imgrc=_ Google Images – Bee orchid postal stamp]</ref> In 2009 the bee orchid appeared in a series of stamps printed in the United Kingdom to celebrate the 150th anniversary of the publication of [[Charles Darwin]]'s [[Origin of Species]].<ref>[http://www.norvic-philatelics.co.uk/2009/02a-charles_darwin_200.htm Norvic Philatelics – Charles Darwin]</ref>

== Conservation ==

=== Ecological concerns ===
There are local extinctions of ''Ophrys spp''. and potentially ''O. apifera'' in Turkey and Iran due to the excessive harvesting of wild orchids to produce salep products.<ref name="Kasparek-199" />

Since ''O. apifera'' relies heavily on its symbiotic relationship with ''Tulasnella'' fungi for survival, it is vulnerable to any chemicals, particularly fungicides, and threats which might reduce the fungi's prevalence.<ref name="Addam-2015" />

=== Species status ===
Protected species status in Northern Ireland.<ref>Jackson, M. W., FitzPatrick, U., Cole, E., Jebb, M., McFerran, D., Sheehy Skeffington, M., & Wright, M. (2016). Ireland Red List No. 10: Vascular Plants. National Parks and Wildlife Service, Department of Arts, Heritage, Regional, Rural, and Gaeltacht Affairs, Dublin, Ireland.</ref>

Endangered (EN) species status in Turkey, Ukraine, and Carpathian Mountains.<ref name="Osiadacz-2014">Osiadacz, B. & Kreciala, M. (2014). Ophrys apifera Huds. (Orchidaceae), a new orchid species to the flora of Poland. Biodiversity Research and Conservation, 36, 11–16. {{doi|10.2478/biorc-2014-0027}}</ref><ref>Sandal Erzurumlu, G., Tuluhan Yilmaz, K., & Sogut, Z. (2017). A regional scale evaluation of conservation status of orchid species recorded in the eastern Mediterranean region of Turkey. Turkish Journal of Agriculture– Food Science and Technology, 5(9), 996–1001. {{doi|10.24925/turjaf.v5i9.999-1001.1233}}</ref>

Critically Endangered (CR) species status in Czech Republic and Slovakia.<ref name="Osiadacz-2014" />

=== Laws/regulations ===
The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) named ''O. apifera'' an endangered species that is potentially an object of trade, setting strict regulations on trade of salep products.<ref name="Osiadacz-2014" /> Turkey, Iran, Germany, the Netherlands, and Cyprus are all Parties to CITES and, in theory, must follow those regulations.

Turkey has banned the export of true salep (salep made from an orchid root).<ref name="Kasparek-199" />

== Taxonomy ==
The specific evolutionary relationships between members of this genus are still poorly understood, and the best method for classifying orchid species and their variants is highly debated.<ref name="Borg-Karlson-1990">{{Cite journal|last=Borg-Karlson|first=Anna-Karin|date=1990-01-01|title=Chemical and ethological studies of pollination in the genus Ophrys (orchidaceae)|url=https://dx.doi.org/10.1016/0031-9422%2890%2980086-V|journal=Phytochemistry|language=en|volume=29|issue=5|pages=1359–1387|doi=10.1016/0031-9422(90)80086-V|issn=0031-9422}}</ref> Some researchers propose classifying species based on their pollination tactics, while others propose classifying them based on the type of chemical emitted from the flower. A widely used and generally accepted method of classification distinguishes orchid species based on flower morphology.<ref name="Borg-Karlson-1990" /> The taxonomy of ''O. apifera'' based on this classification scheme is as follows:

Kingdom Plantae, Phylum Tracheophyta, Subphylum Angiospermae, Class Liliopsida, Order Asparagales, Family Orchidaceae, Subfamily Orchidoideae, Genus ''Ophyrus'', Species ''O. apifera''.

== Varieties ==
* ''Ophrys apifera'' var. ''apifera''
* ''Ophrys apifera'' var. ''aurita''
* ''Ophrys apifera'' var. ''bicolor''
* ''Ophrys apifera'' var. ''botteronii''
* ''Ophrys apifera'' var. ''friburgensis''
* ''Ophrys apifera'' var. ''immaculata''
* ''Ophrys apifera'' var. ''trollii''
* ''Ophrys apifera'' var. ''fulvofusca''
* ''Ophrys apifera'' var. ''belgarum''
* ''Ophrys apifera'' var. ''jurana''
* ''Ophrys apifera'' var. ''atrofuscus''

{{Multiple image
| direction = horizontal
| align = center
| header = Varieties of ''Ophrys apifera''
| width1 = 160
| image1 = Ophrys apifera flower1.jpg
| caption1 = ''Ophrys apifera'' var. ''aurita''
| width2 = 150
| image2 = Ophrys apifera var. bicolor Saarland 004.jpg
| caption2 = ''Ophrys apifera'' var. ''bicolor''
| width3 = 150
| image3 = Ophrys apifera var botteronii Saarland 01.jpg
| caption3 =''Ophrys apifera'' var. ''botteronii''
| width4 = 150
| image4 = Ophrys apifera var. trollii Frankreich 29.jpg
| caption4 = ''Ophrys apifera'' var. ''trollii''
| width5 = 150
| image5 = Ophrys_apifera_var_fulvofusca_190614.jpg
| caption5 = ''Ophrys apifera'' var. ''fulvofusca''
| width6 = 150
| image6 = Bee Orchid var. belgarum (27084826773).jpg
| caption6 = ''Ophrys apifera'' var. ''belgarum''
| width7 = 150
| image7 = Ophrys_jurana3.jpg
| caption7 = ''Ophrys apifera'' var. ''jurana''
}}

== References ==
{{Reflist}}

== External links ==
* {{Commons-inline|Ophrys apifera|''Ophrys apifera''}}
* {{Wikispecies-inline|Ophrys apifera|''Ophrys apifera''}}
* [https://www.biolib.cz/en/taxon/id42170/ Biolib]
* [http://luirig.altervista.org/flora/taxa/index2.php?scientific-name=ophrys+apifera Ophrys apifera]
* [http://powo.science.kew.org/taxon/urn:lsid:ipni.org:names:647746-1 Ophrys apifera | Plants of the World Online]
* [http://www.orchidsofbritainandeurope.co.uk/index.htm Orchids of Britain and Europe]

{{OrchidsYearDE}}
{{Taxonbar|from=Q159291}}

[[Category:Ophrys|apifera]]
[[Category:Orchids of Europe]]
[[Category:Flora of North Africa]]
[[Category:Flora of the Caucasus]]
[[Category:Flora of Western Asia]]
[[Category:Plants described in 1762]]
[[Category:Taxa named by William Hudson (botanist)]]