http://en.spii.ir/seSPII/default.aspx?page=Document&app=Documents&docId=11507

University Lectures, 30. 5. 2016 Invited by Prof. Behzad Ghareyazie, Founder of ABRII

Prof. em. Klaus Ammann, University of Bern, Switzerland

Lecture 6 in Teheran Pollination Ecology of Flowering

[email protected] Pollination Ecology

http://en.wikipedia.org/wiki/Pollination_syndrome http://www.cas.vanderbilt.edu/bioimages/pages/pollination.htm

Fenster, C.B., Armbruster, W.S., Wilson, P., Dudash, M.R., & Thomson, J.D. (2004) Pollination syndromes and floral specialization. Annual Review of Ecology Evolution and Systematics, 35, pp 375-403 http://www.ask-force.org/web/Pollination/Fenster-Pollination-Syndromes-2004.pdf 1.6.1. incentive: Sources of nectar and pollen INCENTIVES FOR VISITING FLOWERS Plants can not move from one location to another, thus many flowers have evolved to attract animals to transfer pollen between individuals in dispersed populations. Flowers that are insect-pollinated are called entomophilous; literally "insect-loving" in Latin. They can be highly modified along with the pollinating insects by co-evolution. Flowers commonly have glands called nectaries on various parts that attract animals looking for nutritious nectar. Birds and bees have color vision, enabling them to seek out "colorful" flowers. Some flowers have patterns, called nectar guides, that show pollinators where to look for nectar; they may be visible only under ultraviolet light, which is visible to bees and some other insects. Flowers also attract pollinators by scent and some of those scents are pleasant to our sense of smell. Not all flower scents are appealing to humans, a number of flowers are pollinated by insects that are attracted to rotten flesh and have flowers that smell like dead animals, often called Carrion flowers including Rafflesia, the titan arum, and the North American pawpaw (Asimina triloba). Flowers pollinated by night visitors, including bats and moths, are likely to concentrate on scent to attract pollinators and most such flowers are white. Still other flowers use mimicry to attract pollinators. Some species of orchids, for example, produce flowers resembling female bees in color, shape, and scent. Male bees move from one such flower to another in search of a mate. http://en.wikipedia.org/wiki/Flower#Attraction_methods Hedera helix, Ivy Nectar presented in open disk

* Allgemeines Hedera helix, Efeu, Araliaceae Nektarsuche Hedera Parnassia palustris, Saxifragaceae attractive pseudo-glands offered, no nectar

Nektarsuche Hedera Parnassia palustris Studentenröschen Saxifragaceae

Parnassia palustris, Pseudonektarien, schlussendlich Selbstbestäubung Ranunculus bulbosus Ranunculaceae

yellow Corolla actually flower-shaped nectaries green perianth, the actual flower

* Ranunculus bulbosus Ranunculus bulbosus, nektaries flower shaped, Ranunculaceae

* Ranunculus bulbosus, Nektarien Ranunculus repens normal spectrum seen by humans ultraviolett spectrum seen by insects

Ranunculus repens, Nektarmal in UV various shapes of nectaries with Ranunculaceae Nektarien Ranunculaceae Aquilegia vulgaris, Akelei, Ranunculaceae corolla and nectaries

Aquilegia vulgaris Aquilegia vulgaris nectaries only Ranunculaceae

Aquilegia vulgaris Aconitum napellus Ranunculacaee

Aconitum napellus Aconitum paniculatum, Ranunculaceae, view from the side

Aconitum paniculatum Aconitum paniculatum frontal view Ranunculaceae

Aconitum paniculatum Aconitum paniculatum Ranunculaceae Nectaries prepared

Aconitum paniculatum Nektarien Aconitum septentrionale

Ranunculaceae

Aconitum septentrionale Aconitum vulparia gelber Eisenhut Ranunculaceae Bumblebees digging holes in helmet of flowers in order to steal the pollen from the anthers

Aconitum vulparia, Hummelbesuch Manfredini, F., Beani, L., Taormina, M., & Vannini, L. (2010) Parasitic infection protects wasp larvae against a bacterial challenge. Microbes and Infection, 12, 10, pp 727- 735 ://WOS:000282906000005 Examples of the amazing breadth of pollination ecology: The dove tree (Davidia involucrata ) has “naked” flowers that lack a perianth but are surrounded by two large bracts. These turn from green (a) to white (b) when flowers open which increases pollinator attraction Sun, J.F., Gong, Y.B., Renner, Susanne S., & Huang, S.Q. (2008) Multifunctional Bracts in the Dove Tree Davidia involucrata (Nyssaceae: Cornales): Rain Protection and Pollinator Attraction, Vol. 171, pp. 119-124. The University of Chicago Press for The American Society of Naturalists, http://www.ask-force.org/web/Pollination/Sun-Davidia-Multifunctional-Bracts-2008.pdf Examples of the amazing breadth of pollination ecology: Calypso bulbosa (c), a rewardless orchid, has evolved to deceive naïve bumblebees in the early spring to effect pollination without payment in nectar

Dafni, A. (1983) Pollination of Orchis Caspia--A Nectarless which Deceives the Pollinators of Nectariferous Species from other Plant Families. Journal of Ecology, 71, 2, pp 467-474 http://www.ask- force.org/web/Pollination/Dafni- Pollination-Orchis-Deceives-1983.pdf Ackermann, J.D. (1981) Pollination Biology of Calypso bulbosa var. occidentalis (Orchidaceae), a Food Deception System. Madrono, 28, 3, pp 101-110 http://www.ask-force.org/web/Pollination/Ackermann- Calypso-bulbosa-Food-Deception-1981.pdf The perennial vine, Gelsemium sempervirens (d), contains alkaloids in all plant parts including corollas and nectar which deter floral herbivores and nectar robbers but - in high concentrations - also pollinators

Adler, L.S. & Irwin, R.E. (2005) Ecological costs and benefits of defenses in nectar. Ecology, 86, 11, pp 2968-2978 http://www.ask- force.org/web/Pollination/Adler- http://alabamaplants.com/Yellowopp/Gelsemi Ecological-Costs-Benefits-2005.pdf um_sempervirens_page.html Adler, L.S. & Irwin, R.E. (2005) Ecological costs and benefits of defenses in nectar. Ecology, 86, 11, pp 2968-2978 http://www.ask-force.org/web/Pollination/Adler-Ecological-Costs-Benefits-2005.pdf Conclusion Secondary compounds in nectar are widespread (Baker 1977, Adler 2000); however, the relationship between these compounds and plant fitness has remained poorly understood. Here we provide experimental evidence that secondary compounds in the nectar of Gelsemium generally decreased the proportion of flowers probed and time spent per flower for most floral visitors. Nectar alkaloids decreased an estimate of male plant reproduction and had little consistent effect on estimates of female reproduction. If nectar secondary compounds provide more fitness costs than benefits in Gelsemium, what maintains variation in this trait? If nectar secondary compounds are heritable, variation could be maintained through a number of mechanisms, including spatiotemporal variation in selection driven by variation in the abundance of pollinators vs. nectar robbers (Thompson and Cunningham 2002). Alternatively, the presence of alkaloids in nectar may be a pleiotropic consequence of their production in other plant tissues and transport through the phloem. To address the possibility that links between defense levels in different tissues constrain the ability of plants to evolve optimal solutions in the context of interactions with multiple antagonists and mutualists, studies of the genetic and environmental factors that determine defense expression across multiple plant tissues, including roots, leaves, stems, flowers, nectar, and fruits, will provide the most constructive ecological and evolutionary insights.

Adler, L.S. & Irwin, R.E. (2005) Ecological costs and benefits of defenses in nectar. Ecology, 86, 11, pp 2968-2978 http://www.ask-force.org/web/Pollination/Adler-Ecological-Costs-Benefits-2005.pdf Hoverflies (e) visit flowers in a large range of habitats, they even pollinate cultivated plants. Though they are numerous, species-rich and wide-spread, their role as pollinators is often still neglected.

Mayer, C.A., Lynn; Armbruster, W. Scott; Dafni, Amots; Eardley, Connal; Huang, Shuang-Quan; Kevan, Peter G.; Ollerton, Jeff; Packer, Laurence; Ssymank, Axel; Stout, Jane C.; Potts, Simon G. (2011) Pollination ecology in the 21st Century: Key questions for future research. Journal of Pollination Ecology, 3, pp 8-23 http://www.ask- force.org/web/Pollination/Mayer- Pollination-Ecology-21fst-Century- Future-2011.pdf Rhododendron ponticum (h) is a highly invasive plant in Ireland. Though it provides food resources for generalist bumblebees, effects on native plant pollinator interactions vary with intensity of invasion.

Mayer, C.A., Lynn; Armbruster, W. Scott; Dafni, Amots; Eardley, Connal; Huang, Shuang-Quan; Kevan, Peter G.; Ollerton, Jeff; Packer, Laurence; Ssymank, Axel; Stout, Jane C.; Potts, Simon G. (2011) Pollination ecology in the 21st Century: Key questions for future research. Journal of Pollination Ecology, 3, pp 8-23 http://www.ask- force.org/web/Pollination/Mayer- Pollination-Ecology-21fst-Century- Future-2011.pdf Heterochelus chiriagricus (Striped monkey beetle), 10mm. [image by M. Picker & C. Griffiths ©, from Field Guide to Insects of South Africa, used with permission]. http://www.biodiversityexplorer.org/beetles/scarabaeidae/r utelinae/hopliini.htm

In the Succulent Karoo of South Mayer, C., Soka, G., & Picker, M. (2006) Africa, monkey beetles (Hopliini) The importance of monkey beetle (Scarabaeidae : Hopliini) pollination for Aizoaceae and Asteraceae in grazed and are important pollinators of many ungrazed areas at Paulshoek, Succulent Karoo, South Africa. plant species Journal of Insect Conservation, 10, 4, pp 323-333 http://www.ask-force.org/web/Pollination/Mayer-Importance- Monkey-Beetle-2006.pdf 1.6.2. Flowers for Pollen Eaters * Pollensammeln, Futterhaare SYNDROME OF FLOWERS VISITED BY POLLEN EATERS considerable amounts of pollen easily accessed as sources, usually offered by flowers without nectar. Typical Flowers: Poppy Papaver, Cistus, Commelina, Rosa, Thalictrum aquilegiifolium sometimes also with intricate deception strategies such as pseudopollinia, see the case of Comelina below. sometimes also fodder hairs and attractive oil sources offered nigrum, Lysimachia vulgaris Papaver rhaeticum, yellow alpine poppy, Papaveraceae

Papaver rhaeticum Cistus albiflorus, visited by pollen eaters

Cistus albiflorus Cistus ladaniferus, nectar and pollen collectors

Cistus ladaniferus Commelina coelestis, yellow and conspicous pseudo-anthers

Commelina coelestis Commelina coelestis, yellow and conspicous pseudo-anthers

Commelina erecta, Staminodien Thalictrum aquilegiifolium coloured anther filaments as attraction for flower visitors

Thalictrum aquilegiifolium Verbascum nigrum attracts flower visitors with colourful hairs of anther filaments

Verbascum nigrum Futterhaare 1.6.3. sexual attraction pseudo-copulation Pseudocopulation describes behaviors similar to copulation that serve a reproductive function for one or both participants but do not involve actual sexual union between the individuals. It is most generally applied to a pollinator attempting to copulate with a flower. Some flowers mimic a potential female mate visually, but the key stimuli are often chemical and tactile.[1] This form of mimicry in plants has been titled Pouyannian mimicry.[2] Orchids commonly achieve reproduction in this manner, secreting chemicals from glands called osmophores located in the sepals, petals, or labellum, that are indistinguishable from the insect's natural pheromones. The pollinator then has a pollinia attached to its body, which it transfers to the stigma of another flower when if it attempts another 'copulation'. Pollinators are often bees and wasps of the order Hymenoptera, and flies. from http://en.wikipedia.org/wiki/Pseudocopulation Ophrys insectifera, pseudo copulation as incentive

* Ophrys insectifera: Pseudocopulation Ophrys fuciflora Orchidaceae

Mimikri for attracting male solitary bees for pseudo copulation

Ophrys fuciflora Ophrys scolopax Orchidaceae

Mimikri for attracting male solitary bees for pseudo copulation

Ophrys scolopax Ophrys scolopax Orchidaceae

Mimikri Bienen

Ophrys scolopax Ophrys lutea Orchidaceae

Mimikri for attracting male solitary bees for pseudo copulation

Ophrys lutea Ophrys lutea Orchidaceae

Mimikri for attracting male solitary bees for pseudo copulation

Ophrys lutea Andrena nigroaenea male pseudocopulating with a flower of the Early Spider Orchid, Ophrys sphegodes www.unet.univie.ac.at/ ~a8917722/

Andrena nigroaenea The sexually attracted male pollinator Neozeleboria cryptoides on the stem of the orchid Chiloglottis trapeziformis / www.anu.edu.au/BoZo/ orchid_pollination www.anu.edu.au/BoZo/ Australisches Beispiel Pseudokopulation 1 pr Chiloglottis Chiloglottis trapeziformis on the labellum of on thethe labellum orchid on the labellum of on thethe labellum orchid Neozeleboria cryptoides Neozeleboria Neozeleboria cryptoides Neozeleboria carrying that (pollinia) pollen was removed during attempted copulation The male pollinator trapeziformis with (pseudocopulation) a previous flower The male pollinator attempted mating with the During this flower (pseudocopulation). removalprocess will pollen take plac www.anu.edu.au/BoZo/ orchid_pollination/ Australische Beispiele Pseudokopulation 2 Duftstoffe Gaschromatographie Duftstoffe Gaschromatographie Ophrys apifera Orchidaceae auto-pollination despite of perfect mimikri for pseudo copulation

Ophrys apifera autogam Ophrys apifera, auto-pollination despite of perfect mimikri for pseudo copulation

Ophrys apifera autogam Nelson. Autopoiesis proof: compact speculum as evolutionary derived character

Nelson abgeleitetes Lippenmal Nelson. Autopoiesis proof: H-shaped speculum as ancestral character

Nelson: ursprüngliches Lippenmal 1.6.4. collecting nesting materials Megachile, solitary leaf cutter bees, building nests from cut leaves http://en.wikipedia.org/wiki/Megachile

* Nestbau Mohnbiene Megachile Dalechampia centuncularis Harzquelle Nestbaustoffe Megachile

http://en.wikipedia.org/wiki/Catasetum

Parfum-Sammler: Prachtbienen der Tropen

Parfum-Sammler http://en.wikipedia.org/wiki/Coryanthes Darwins print, copied from Lindley German translation http://en.wikipedia.org/wiki/Coryanthes www.weloennig.de/CorCat.html

1.6.5. summary of pollinator syndromes bee pollination Bee pollination (melittophily) Bee-pollinated flowers tend to fall into two classes: Showy, open, bowl-shaped flowers that are relatively unspecialized (e.g. wild roses, sunflowers) Showy, complicated, non-radially symmetric flowers that are more specialized (e.g. peas, foxgloves) Some bee flowers tend to be yellow or blue, often with ultraviolet nectar guides and scent. Nectar, pollen, or both are offered as rewards in varying amounts. The sugar in the nectar tends to be sucrose-dominated. There are diverse types of bees, however. Honeybees, bumblebees, orchid bees, etc are large groups that are quite distinctive in size, tongue length and behaviour (some solitary, some colonial). Thus generalization about bees is difficult (Fenster at al. 2004.) Some plants can only be pollinated by bees because their anthers release pollen internally, and it must be shaken out by buzz pollination. Bees are the only animals that perform this behaviour http://en.wikipedia.org/wiki/Pollination_syndrome#Bee_pollination_.28melittophily.29 Darwin, C. (1862) On the various contrivances by which orchids are fertilized by insects and on the good effects of intercrossing, The Complete Work of Charles Darwin online, Scanned, OCRed and corrected by John van Wyhe 2003; further corrections 8.2006. RN4 edn. Murray, London, pp 366 http://darwin- online.org.uk/content/fram eset?viewtype=side&itemI D=F800&pageseq=1 1: 3 sepals (outer) and 3 pepals (inner whirl

3: central , Anther, carries 2 pollinia

2: gynostemium or 4: two other stamen reduced to column staminodes http://en.wikipedia.org/wiki/Orchid

5: Rostellum 7: ovary, inferior 9: stigma- covers cave sticky 8: spur, in disks Orchis and 6: Labellum Dactylorhiza without nectar http://www.denniskunk el.com/DK/Plants/893 1B.html

http://www.orchids.co.in/plant-facts/orchid-pollination.shtm In the tribe Orchideae , the pollinia are included in special bags called bursicles ,which slit open upon maturation . As soon as the insect enters the flower, the two viscidia attach themselves to the two sides of the insect’s head. When the insect leaves the flower , the two pollinia are drawn from the bursicles and carried away on the insect’s head. By a special hygrophilous quality of the caudicle ,the pollinia which are at first held upright on the insect’s head slowly bend forward , till it comes to occupy a position at right angles to the insect’s head . In this position ,when the insect visits the next flower , the pollinia immediately come in contact with the stigma . This hygrophilous nature of the caudicle is characteristic of some of the advanced Sarcanthine orchids such as Vanda teres , Luisia sp.etc. Here the caudicle is transparent and ribbon-shaped . Immediately after removal from the anther it appears straight . But while it is being carried on the insect’s head, it absorbs it appears straight . But while it is being carried on the insect’s head , it absorbs water and curves in an S-shaped manner Dactylorrhiza bringing the pollinia forward , so that they are deposited on the stigma maculata of the flower which the insect visits next Orchis purpureus, Purpur-Knabenkraut, Orchidaceae, Pollinien-Versuch Orchis purpureus, Purpur-Knabenkraut, Orchidaceae, Pollinien-Versuch Orchis purpureus, Purpur-Knabenkraut, Orchidaceae, Pollinien-Versuch Himantoglossum hircinum Bocks-Riemenzunge

Bienen Himantoglossum hircinum Bocksriemenzunge Orchidaceae Bienen Adenostyles leucophylla, filziger Alpendost, Asteraceae, Bienen usw. Cephalanthera rubra, rotes Waldvögelein, Orchidaceae, Bienen, Hummeln, Glockenblumen-Mimikri Orchis morio, kleine Orchis, Orchidaceae, Bienen Orchis coryophora Wanzen-Knabenkraut

Orchidaceae

Bienen Orchis papilionaceae Schmetterlings- Knabenkraut Orchidaceae

Bienen Asclepias curassavica, Milkweed, Pollinien-Bestäubung Asclepias curassavica Asclepias curassavica Milkweed Pollinienbestäubung Asclepias curassavica. One flower with the gynostegium in longitudinal section. Note the gland (corpusculum) and pollinia in the upper left. The corolla tube has been dissected to show the 2 free, superior ovaries, while the top of the gynoecium is connate and then adnate to the androecium to form part of the gynostegium. Asclepias curassavica

http://en.wikipedia.org/wiki/Asclepias of description see pollination slide 82

http://delta-intkey.com/angio/images/ascle551.gif

http://www.inhs.uiuc.edu/~kenr/prairieplants.A.html Pollination is very unusual in Milkweed, because the pollen is grouped into structures called pollinia rather than being individual grains.. The flowers of the milkweed are very smooth and quite rigid, usually pink or white pink in color, while the leaves are a rounded, oval and waxy to the touch and to view. The insects will slip into notches in the flowers, where the bases of the pollinia which are very sticky, will then attach to their feet, so that they will pull the pollen sacs free when they fly away. Some bees, including some honey bees, only gather nectar from milkweed and since they visit no where else, are not really effective as pollinators for the plants.

Asclepias variegata, White Milkweed, pollinia pollination as Orchids pollination bee asperula Asclepias www.sbs.utexas.edu/.../asclepias_asperula.htm Lamium orvala, Karawanken, pollination with bumble bees Lamium maculatum gefleckte Taubnessel Lamiaceae Bumble bees and bees Salvia pratensis, Wiesensalbei left Lamium maculatum, gefleckte Taubnessel right, typical pollination through honey bees Salvia pratensis Wiesensalbei, Lamiaceae classic mechanism how bees press anthers on their back Salvia pratensis Wiesensalbei, Lamiaceae

Hebelmechanismus Bienen Rosmarinus officinalis Rosmarin Lamiaceae

Mechanism female stage Dolchfliege Galeopsis speciosa prächtiger Hohlzahn above: no parking guard rails sidewards yellow and purple nectar traffic sign

Parkverbot oben, Leitplanken seitlich, Saftmal als Verkehrs- zeichen classic honey bee pollination Pedicularis tuberosa knolliges Läusekraut Scrophulariaceae asymmetric flowers only specialists can enter the flowers with a special trick Final remarks about bee pollination Example from the PRRI ASK-FORCE Are GM crops killing honey bees ?

http://pubresreg.org/index.php?option=com_content&task=view&id=63 http://www.spiegel.de/international/world/0,1518,473166,00.html Walter Haefeker, the German beekeeping official, speculates that "besides a number of other factors," the fact that genetically modified, insect-resistant plants are now used in 40 percent of cornfields in the United States could be playing a role. The figure is much lower in Germany -- only 0.06 percent -- and most of that occurs in the eastern states of Mecklenburg- Western Pomerania and Brandenburg. Haefeker recently sent a researcher at the CCD Working Group some data from a bee study that he has long felt shows a possible connection between genetic engineering and diseases in bees. http://www.spiegel.de/international/world/0,1518,473166,00.html Researchers have found an imported virus that may be associated with the sudden disappearance of honey bees in the United States, known as colony collapse disorder (CCD). This baffling syndrome, which earlier this year made headlines around the world, may have afflicted as many as 23% of beekeepers in the United States and caused losses of up to 90% of hives in some apiaries. The identification of a suspect is an important step, says Nicholas Calderone of Cornell University. “Before, we didn’t even have circumstantial evidence.”

Stokstad, E. (2007) GENOMICS: Puzzling Decline of U.S. Bees Linked to Virus From Australia. Science %R 10.1126/science.317.5843.1304, 317, 5843, pp 1304-1305 http://www.ask-force.org/web/Bees/Stockstad-IAPV-Culprit-2007.pdf Stokstad, E. (2007) ENTOMOLOGY: The Case of the Empty Hives. Science %R 10.1126/science.316.5827.970, 316, 5827, pp 970-972 http://www.ask-force.org/web/Bees/Stockstad-Empty-2007.pdf much more information, and stating that the CCD case is still open: http://en.wikipedia.org/wiki/Colony_Collapse_Disorder butterfly pollination Butterfly pollination (psychophily) Butterfly-pollinated flowers tend to be large and showy, pink or lavender in colour, frequently have a landing area, and are usually scented, but many examples in Central Europe lack sents. Since butterflies do not digest pollen (with one exception), more nectar is offered than pollen. The flowers have simple nectar guides with the nectaries usually hidden in narrow tubes or spurs, reached by the long tongue of the butterflies.

http://en.wikipedia.org/wiki/Pollination_syndrome#Bee_pollination_.28melittophily.29 glacialis, butterfly pollination, long proboscis Silene (Melandrium) rubrum narrow entrance long proposcis

Butterfly pollination Gymnadenia conopea, Orchidaceae, butterfly pollination: long spur Dianthus armeria Rauhe Nelke

Caryophyllaceae

Tagfalter Dianthus armeria, rauhe Nelke, , Tagfalter, Cirsium oleraceum Kohldistel Asteraceae viele Bestäuber bulbiferum Feuerlilie

Tagfalter weiss: Nektar-Röhren Gentiana bavarica, butterfly pollination Parnassius apollo on Centaurea spinosa Kure Mountains, Turkey www.pbase.com/efratnakash/image/80997440 moth- pollination Moth pollination (phalaenophily) Day-flying sphinx moth nectaring on Brazilian verain Among the more important moth pollinators are the hawk moths (Sphingidae). Their behaviour is similar to hummingbirds: they hover in front of flowers with rapid wingbeats. Most are nocturnal or crepuscular. So moth-pollinated flowers tend to be white, night-opening, large and showy with tubular corollas and a strong, sweet scent produced in the evening, night or early morning. A lot of nectar is produced to fuel the high metabolic rates needed to power their flight. Other moths (Noctuids, Geometrids, Pyralids, for example) fly slowly and settle on the flower. They do not require as much nectar as the fast-flying hawk moths, and the flowers tend to be small (though they may be aggregated in heads) (Oliveira et al. 2004).

day-flying sphynx moth nectaring on Brazil vervain Platanthera chlorantha print from Darwin

Viscidium in distant position for big moths Platanthera chlorantha, viscidium distant, for big insect heads (moths) Platanthera chlorantha, experiment with reverse pen, viscidia distant Platanthera chlorantha, experiment with reverse pen, after a few seconds Some moth species, however, are exceptional pollinators. Especially well known are the "hummingbird moths" of the Family Sphingidae.

www.kidsbutterfly.org/faq/general/14 Angraecum sesquipedale Angraecum sesquipedale

Orchidaceae moth pollination predicted by Charles Darwin

Pollinator found later: Xanthopan morgani praedictus http://www.criptozoo.com/absolutenm/templates/skin.asp?articleid=217&zoneid=1 http://darwin.gruts.com/weblog/archive/2008/02/ Charles Darwin famously predicted the existence of a species of Madagascan moth (since aptly named Xanthopan morgani praedicta), based on the shape of the nectaries of a species of orchid (Angraecum sesquipedale). Might it not be possible to take a leaf out of Darwin's book and make similar deductions retrospectively? Could parasitologists not study tetrabothiids and other modern parasites, and make deductions about their extinct ancestral hosts' lifestyles? invitation to browse in the website of the Friends of Charles Darwin http://darwin.gruts.com/weblog/archive/2008/02/ Bulbophyllum nocturnum J.J.Verm., de Vogel, Schuit. & A.Vogel: A, habit; B, flower; C, dorsal sepal, petal, lip and lateral sepal; D, lip; E, column and lip; F, pollinia; G, anther. All after Hortus Botanicus Leiden cult. 20080300 (drawing J.J.V.).

Schuiteman,C: appendices, A., Vermeulen, probably J.J., De Vogel, E.D., & Vogel, A.R.T. (2011) Nocturneattract for an unknown pollinator: first descriptionUnknown of a night pollinators-flowering orchid (flies?) (Bulbophyllum nocturnum). Botanical Journal of the Linnean Society, 167, 3, pp 344-350 http://dx.doi.org/10.1111/j.1095- 8339.2011.01183.x AND http://www.ask- force.org/web/Pollination/Schuiteman- Bulbophyllum-nocturnum-2011.pdf Perfect floral gift for a loved one, no? (Bulbophyllum nocturnum by Andre Schuiteman) http://thethao.tuoitre.vn/The-thao/466211/Phat-hien-loai%C2%A0hoa-lan-dau-tien-no-ve-dem.html Bulbophyllum nocturnum with Appendices of unknown function Maybe attract unknown pollinator ?

http://www.trouw.nl/tr/nl/4332/Groen /article/detail/3046913/2011/11/23/ De-knoppen-leken-steeds-te- verwelken.dhtml marsupian- pollination Banksia attenuata Proteaceae grobe Bürsten-Blüten- stände, robuste Staubblätter und Narben mit Beutelmäusen Banksia integrifolia, Proteaceae, West-Australien Banksia attenuata, Proteaceae, Beutler und Vögel Banksia attenuata Proteaceae Beutler und Vögel Callistemon speciosum Myrtaceae Bottle Brush Tree

Beutler und Vögel Melaleuca quinquenervia Myrtaceae

Säuger und Vögel bat- pollination Saguaro Cereus giganteus Fleder- mäuse Saguaro Cereus giganteus

Fledermäuse Agave sp. Agavaceae Fleder- mäuse Solanaceae Cobaea sp. Underwoods longtongued Bat Hylonycteris underwoodii

Opuntia humifusa, niederliegende Opuntie, Fledermäuse Carpobrothus edulis, Mesembryanthemaceae, Fledermäuse Solandra nitida, Solanaceae, Fledermäuse Dombeya wallichii Sterculiaceae, Madagaskar Fledermäuse Dombeya wallichii, Sterculiaceae, Madagaskar, Fledermäuse Thunbergia japonica Acanthaceae Grosse Hautflügler Fledermäuse, Vögel robuste Trompeten- form bird- pollination Aechmea sp. Bromeliaceae Hochblätter rot Kolibri Cata, Venezuela Aechmea, Bromeliaceae, rote Hochblätter Nektar weisslich eintrocknend, Kolibri, Cata, Venezuela Strelitzia reginae, Musaceae, Südafrika, Vögel stehen auf Antheren Columnea fawcettii, Gesneriaceae, epiphytisch, Jamaica, Vögel Columnea fawcettii, Gesneriaceae, epiphytisch, Jamaica, Vögel botit.botany.wisc.edu/.../ Gesneriaceae/Columnea/ Cattleya aurantiaca, Orchidaceae, Vögel Amherstia nobilis, Caesalpiniaceae, ursprünglich Ostasien, Vögel Cestrum hirtum, Solanaceae, Kolibris Anderson, S.H., Kelly, D., Ladley, J.J., Molloy, S., & Terry, J. (2011) Cascading Effects of Bird Functional Extinction Reduce Pollination and Plant Density Science, Science 1199092 Published online 3 February 2011 pp http://www.ask-force.org/web/Pollination/Anderson-Cascading-Effects-Birds-Extinction-2011.pdf AND http://www.sciencemag.org/search?site_area=sci&fulltext=%22dave%20kelly%22&submit=yes Supporting Material http://www.ask-force.org/web/Pollination/Anderson-Cascading-Effects-Birds-Extinction-Supporting-2011.pdf http://www.sciencemag.org/content/early/2011/02/02/science.1199092/suppl/DC1 AND blog material http://www.ouramazingplanet.com/birds-plants-pollination-biodiversity-loss-1058/ A male stitchbird (or hihi) on Tiritiri Matangi Island. This important pollinator vanished off the North Island with the arrival of mammalian predators 140 years ago, but persists on nearby islands. Where stitchbirds and bellbirds survive, the pollination mutualism still works well. Credit: Dave Kelly, University of Canterbury http://www.ouramazingplanet.com/birds-plants-pollination-biodiversity-loss-1058/ for successful fruit set. [Photo: M Walters] presentation is finished, the so require birdflowers visitors a bird. pollen been elongates has by visited stigma after The and the ridged fused pollen whichdisc flower marked is the if tube, long corolla mm narrow 10 underneath, showing the A of flower Rhabdothamnus solandri viewed from set set (meansuccess fruit % remain (A) high. Pollination densities bird where islands offshore adjacent on not extinct, but are functionally pollinators bird its mainland, where Zealand shrub birdpollinated for the limitation pollen strong for Evidence on the mainland, but not on islands (post (post on the but tests,hoc mainland, not onislands text).see flowers worse than significantly did flowers hand-pollinated (unmanipulated) natural cases, both In fruit size). from ± SEM).per (B) fruit Seeds (mean andSEM,estimated Rhabdothamnus solandri on the New on solandri Rhabdothamnus

Anderson et al. 2011 significantly fewer seedlings on the mainland ( on the mainland fewer seedlings significantly sites had similar adult densities ( densities adult sites had similar densities). bird andmainland Island (low and the mainland on centered juvenile (<30 of ( on the adult densities mainland: solandri of Rhabdothamnus for regeneration failure Evidence R. solandri adults, on islands (high bird densities) bird (high adults, islands R.on solandri cm) cm) R. solandri plants (meanplants ± R. solandri P = P = 0.56), but there were ≥ SEM) plots in 30 P = P = cm and tall) 0.020).

Anderson et al. 2011 Melicytus ramiflorus or Geniostoma ligustrifolium (see text). Geniostoma ligustrifolium (see or ramiflorus Melicytus significantly higher for in sown plots after Seedling density plots. unsown adjacent to plots inaugmentation mainland on the compared April 2003, SEM) from three species sown into into sown species three from SEM) October seedlings in of densities solandri: of limitation seed Evidence for Rhabdothamnus 10 R. solandri, solandri, R. not for but x 20 2008 cm seed cm (mean 5 years was years ± beetle- pollination Viburnum opulus, gemeiner Schneeball, Käfer usw. Nymphaea alba, weisse Seerose, Nymphaeaceae, Käfer Nymphaea alba, weisse Seerose, Nymphaeaceae, Käfer Viburnum lantana wolliger Schneeball Käfer usw. Thalictrum flavum gelbe Wiesenraute Ranunculaceae Canthariden, Weichkäfer Thalictrum flavum gelbe Wiesenraute Ranunculaceae Canthariden, Weichkäfer Asarum europaeum, europäische Haselwurz, Aristolochiaceae beetle and fly- pollination Peucedanum austriacum österreichischer Haarstrang

Käfer, Fliegen usw. Heracleum sphondylium, Bärenklau, Käfer, Fliegen Heracleum sphondylium, Bärenklau, Randblüten mit Schaufunktion Anthriscus silvestris, Wiesenkerbel, Früchte mit Nektar-Scheiben Peucedanum ostruthium, Meisterwurz, Blitz in Dämmerung Veronica filiformis, Faden-Ehrenpreis, Scrophulariaceae, Fliegen Veronica cymbalaria, Fliegenbestäubung Euphrasia minima, kleiner Augentrost, Fliegen Tozzia alpina, Tozzie, Scrophulariaceae, Fliegen Sarracenia flava, karnivor, Insektenfallen, fliegenbestäubt Sarracenia flava karnivor

North Carolina fliegenbestäubt Sarracenia flava karnivor

North Carolina fliegenbestäubt Arum maculatum Spatha, Kolben und Reusenfalle Fliegen Arum maculatum Spatha, Kolben und Reusenfalle Fliegen Arum maculatum Aronstab Flug- und Gleitbahnen der Fliegen Arum maculatum, Aronstab links: junge Reusen, Anth. geschlossen, Nektartropfen rechts: Reusenhaare verdorrt, Antheren offe The titan arum or Amorphophallus titanum is a with the largest unbranched inflorescence in the world. The largest single flower is borne by the Rafflesia arnoldii; the largest branched inflorescence in the plant kingdom belongs to the Talipot palm (Corypha umbraculifera). The titan arum was originally discovered by an Italian botanist, Odoardo Beccari, in Sumatra in 1878. It thrives at the edges of rainforests near open grasslands. Though found in many botanic gardens around the world it is still indigenous only to the tropical forests of Sumatra. Due to its fragrance, which is reminiscent of the smell of a decomposing mammal,[1] the titan arum is also known as a carrion flower, the "Corpse flower", or "Corpse plant" (in Indonesian, "bunga bangkai" – bunga means flower, while bangkai means corpse or cadaver; for the same reason, the same title is also attributed to Rafflesia which, like the titan arum, also grows in the rainforests of Sumatra).

http://en.wikipedia.org/wiki/Titan_arum Ollerton, J. & Raguso, R.A. (2006) The sweet stench of decay. New Phytologist, 172, 3, pp 382-385 http://www.ask-force.org/web/Pollination/Ollerton-Sweet-Stench-2006.pdf Fig. 1 The scent space of sapromyiophilous stapeliads and aroids. Nonmetric multidimensional scaling (NMDS) analysis of the major scent compounds present in the odour profiles of 15 species of stapeliads (Apocynaceae subfamily Asclepiadoideae, tribe Ceropegieae, subtribe Stapeliinae; data from Jürgens et al., 2006), plus 11 species of Arum, 20 species of Amorphophallus and two species of Pseudodracontium (Araceae; data from Kite et al., 1998). NMDS was performed using a binary (presence-absence) matrix of the 48 plant species and the 54 most abundant (≥ 10% volume) compounds from their scent profiles, resulting in a two-dimensional plot using Euclidean distances between species. Unidentified compounds were omitted from the analysis. Several Amorphophallus species have identical oligosulphide odours and thus occupy the same loci in scent space. Chemical structures indicate scent components that contributed most to the separation of clusters in scent space (Jürgens et al., 2006), and are (clockwise from top): hexanoic acid, p-cresol, octanal, dimethyl disulphide and 2-heptanol (centre). Trimethyl amine (upper left) confers a dead-fish odour to Amorphophallus brachyphyllus (Kite & Hetterscheid, 1997), and is predicted to be present in stapeliads such as Huernia thuretii (not yet studied), which would expand the stapeliad domain in scent space.

Ollerton, J. & Raguso, R.A. (2006) The sweet stench of decay. New Phytologist, 172, 3, pp 382-385 http://www.ask-force.org/web/Pollination/Ollerton-Sweet-Stench-2006.pdf http://www.bulbsociety.org/GALLERY_OF_THE_WOR LDS_BULBS/GRAPHICS/Arum/Arum_palaestinum/Ar um_palaestinum.html

Arum palaestinum

http://picsicio.us/keyword/arum%20palaestinum/ These are vinegar flies trapped in the calyx of the lily Arum palaestinum. Credit: Johannes Stökl, Curr. Biol., Oct. 7, 2010

Deceitful lily fools flies Solomon's lily imitates a yeasty odor to lure vinegar flies into a trap

Stökl, J., Strutz, A., Dafni, A., Svatos, A., Doubsky, J., Knaden, M., Sachse, S., Hansson, B.S., & Stensmyr, M.C. (2010) A Deceptive Pollination System Targeting Drosophilids through Olfactory Mimicry of Yeast. Current Biology, In Press, Corrected Proof, pp http://www.sciencedirect.com/science/article/B6VRT- 51618H5-5/2/4786042e3ee7f68188f5197d1a0d7016 AND http://www.ask-force.org/web/Pollination/Stoekl- Deceptive-Pollination-2010.pdf - 2010.pdf - - 51618H5 - http://www.ask Pollination - Deceptive - Stökl, J., Strutz, A., Dafni, A., Svatos, A., Doubsky, J., Knaden, M., Knaden, J., A., Doubsky, Svatos, A., A., Dafni, Strutz, J., Stökl, M.C. (2010) S.,Sachse, Hansson, B.S., Stensmyr, & through Drosophilids Olfactory Deceptive System Pollination Targeting A In Press,Proof, Corrected pp Biology, Current Yeast. Mimicryof http://www.sciencedirect.com/science/article/B6VRT AND 5/2/4786042e3ee7f68188f5197d1a0d7016 force.org/web/Pollination/Stoekl

(C) Headspace odor of A. palaestinum (orange trace) and electro-antennograms (EADs) from females of D. melanogaster and D. simulans. The EAD traces shown are the averages of five runs, respectively. Numbers in the EAD trace refer to peaks that elicited antennal reactions in either of the species; blue numbers denote peaks yielding fully reproducible response: (1) acetoin; (2) 1-hexanol; (3) acetoin acetate; (4) 2,3- butanediolacetate (4i, threo; 4ii, erythro); (5) unknown; (6) 1-propionylethyl acetate; (7) ethyl hexanoate; (8) hexyl acetate; (9) 2,3- butanedioldiacetate; (10) 2-phenethyl alcohol; (11) 2-phenethyl acetate; and (12) geranylacetone. Flowers of Ceropegia arabica (Apocynaceae) are pollinated by small Diptera in common with all other members of the genus studied to date (Ollerton et al. 2009). Photograph by Sage Reynolds

Ollerton, J., Masinde, S., Meve, U., Picker, M., & Whittington, A. (2009) Fly pollination in Ceropegia (Apocynaceae: Asclepiadoideae): biogeographic and phylogenetic perspectives. Annals of Botany, 103, 9, pp 1501-1514 http://www.ask- force.org/web/Pollination/Ollerton- Fly-Pollination-Ceropegia-2009.pdf Stapelia, Aasfliegen Stapelia, Aasfliegen Stapelia, Aasfliegen Rafflesia pricei, Sabah, Borneo Tambunan Rafflesia Centre in the Crocker Range National Park, Sabah, Malaysia http://lemberk.vcm.cz/cestopisy/rafflesia2.htm provincie Benkulu ve střední Sumatře a Západní Kalimantan (Indonésie), západní Sarawak (Malajsie) Rafflesia arnoldii Rafflesia arnoldii is a member of the genus Rafflesia. It is noted for producing the largest individual flower on earth. There are some plants with larger flowering organs, the Titan Arum and Talipot palm, but these are technically clusters of many flowers. It occurs only in the rainforests of Sumatra and Borneo in the Indonesia Archipelago.Molecular studies in 2007 have resulted in the final of Rafflesia arnoldii which has been assigned to the family of Euphorbiaceae (Davis et al. 2007).DescriptionSeveral species of Rafflesia grow in the jungles of southeast Asia, many of them threatened or endangered. Rafflesia arnoldii is the largest; its flower attains a diameter of nearly a meter (3 ft) and can weigh up to 11 kilograms (24 lb).It lives as a parasite on the Tetrastigma vine, as its host, which grows only in primary (undisturbed) rainforests. While many parasites appear like normal plants, Rafflesia lacks any observable leaves, roots, or even stems. Likened to fungi, Rafflesia individuals grow as thread-like strands of tissue completely embedded within and in intimate contact with surrounding host cells from which nutrients and water are obtained. Perhaps the only part of Rafflesia that is identifiable as distinctly plant-like are the flowers; although, even these are bizarre because they attain massive proportions and are usually reddish-brown and stink of rotting flesh. The flower is pollinated by flies attracted by its scent.Specimen of Rafflesia arnoldii at the Kyoto Botanical Garden.EnlargeSpecimen of Rafflesia arnoldii at the Kyoto Botanical Garden.Rafflesia arnoldii is rare and fairly hard to locate. It is especially difficult to see in flower; the buds take many months to develop and the flower lasts for just a few days. How many of these strange plants still survive is unknown, but as the remaining primary forests of Borneo and Sumatra disappear, it can only be assumed that their numbers are dwindling. Many are known to be nearing extinction. Some environmentalists are thinking of a way to recreate the species’ environment, in an effort to stimulate a recovery in the population of this endangered species. This has proved unsuccessful so far, but the efforts have continued. However, steps are being taken to conserve the forests of Sumatra and Borneo.Pollination is a rare event due to several factors. The flowers are unisexual and single sites usually produce either male or female flowers. Therefore, in order to have effective pollination, male flowers must be near to, and open at the same time as, the female flowers so that flies can transfer the pollen.While male and female individuals could be closely spaced, flower bud mortality is 80-90% per site thereby reducing the chance of co-flowering two individuals. Furthermore, the flower lifespan is only 5-7 days. Also, the current population distributions are fragmented due to habitat destruction. So, successful reproduction relies on the unlikely event that a male and female would bloom during the same 5-7 days and that a fly could carry pollen between the often widely separated populations.

See also http://www.parasiticplants.siu.edu/Rafflesiaceae/Raff.arn.page.html

Video from BBC Archive: Flies pollinating Rafflesia http://www.arkive.org/rafflesia/rafflesia-spp/video-09.html Rafflesia: Big Daddy of the Spurge Family Unassuming cousin, Euphorbia baylissii Photo: Frank Vincentz, via Wiki

Davis, C.C., Latvis, M., Nickrent, D.L., Wurdack, K.J., & Baum, D.A. (2007) Floral Gigantism in Rafflesiaceae. Science, pp 1135260 http://www.ask- force.org/web/Pollination/Davis -Rafflesia-Gigantism-Evolution- 2007 df Bulbophyllum careyanum Orchidaceae Aasfliegen Bulbophyllum careyanum Orchidaceae Aasfliegen Bulbophyllum dayanum Mimikry: decaying animals attracting flyes feeding on cadavres Bulbophyllum sp. Aasfliegen Bulbophyllum sp. Aasfliegen Altensteinia (Aa), within Sphagnum in Andes of Venezuela tiny 4mm-flowers on, ca. 4000m altitude, pollinator unknown Antelope Orchid Dendrobium minax Orchidaceae Botanic Garden in Bern pollinator ? http://pinterest.com/pin/54817320434794