Which Came First the

Flower or the Bee?

Landscapes West 2009Sheryl Williams

swilliams@dmtc.edu

Co-evolution• Flowering plants have co-evolved

with their pollinator partners over millions of years producing a fascinating and interesting diversity of floral strategies and pollinator adaptations.

• The great variety in color, form, and scent we see in flowers is a direct result of the intimate association of flowers with pollinators.

80% of plants are pollinated with other

organisms• 20% without

– 98% wind– 2% water

http://www.fs.fed.us/wildflowers/pollinators/plantstrategies/index.shtml

The pollen from an anther must make contact and be physically and chemically correct in order to be taken into the stigma

Anther

Stigma

Pollen Grains• Extraordinary• Microscopic – the size

of dust particles• Unimaginable numbers

– One birch catkin can contains 5 ½ million pollen grains

– One birch tree will have thousands of catkins

Scanning Electron Microscope image of English Daisy pollen and lily pollen

http://www.vcbio.science.ru.nl/en/virtuallessons/pollination/

Wind Pollination

Pollination History• “The first fossil record for abiotic pollination is from

fern-like plants in the late Carboniferous period(350 mya).

• Gymnosperms show evidence for biotic pollination as early as the 251-199 mya

• Many fossilized pollen grains show characteristics similar to the biotically-dispersed pollen today.

• The gut contents, wing structures, and mouthpart morphologies of fossilized beetles and flies suggest that they acted as early pollinators. “

Purdue 1-7-08 Plant Reproduction General

• “The association between beetles and angiosperms during the early Cretaceous (145-65.5 mya) period led to parallel radiations of angiosperms and insects into the late Cretaceous.

• The evolution of nectaries in late Cretaceous flowers signals the beginning of the mutualism between hymenopterans* and angiosperms.”– *Those with membranous wings

Purdue 1-7-08 Plant Reproduction General

Wind Pollination - oldest• If a flowering plant is to reproduce

sexually, it must ensure that its pollen reaches the style of another individual of the same species

• Smallest can be carried by the wind• Grasses, sedges, conifers and many

broadleaved trees– Walnut, oak, birch, poplar and hazel

Cottonwood CatkinsCatkins appear in early spring before the leaves emerge to prevent interference with wind dispersal

http://www.fs.fed.us/wildflowers/pollinators/plantstrategies/index.shtml

Stigmas on a Black Walnut are relatively large to catch pollen

http://www.cas.vanderbilt.edu/bioimages/pages/pollination.htm

Dandelion“Parachute” dispersal

Blue grama grass anthers releasing pollenhttp://www.fs.fed.us/wildflowers/pollinators/plantstrategies/images/bouteloua_gracilis_lg.jpg

Grass anthers and stigma extended

http://mac122.icu.ac.jp/gen-ed/higher-plants-etc.htmlhttp://www.vcbio.science.ru.nl/en/virtuallessons/pollination/

• Wind is an effective transporter.• It can take the tiny dry grains as high as

19,000 feet and carry them for 3,000 miles• Totally haphazard• Most will not reach the stigma of another

and therefore be wasted• Pollen is rich in oils and proteins and

producing it constitutes a significant loss to the plant

Flowering Plants

Magnolia• Magnolia is an ancient genus • Having evolved before bees appeared,

the sturdy flowers developed to encourage pollination by beetles

• Magnolia flowers do not produce nectar but they do produce large quantities of pollen, which is high in protein and good food for beetles

http://www.lsa.umich.edu/mbg/see/inbloom_summer.asp

Magnolia grandiflora flower(Southern Magnolia)

http://www.cas.vanderbilt.edu/bioimages/biohires/m/hmagr4-fl10949.jpg

Magnolia Family• There are no specialized adaptations

to exploit pollinators• Insects simply crawl around on the

flowers looking for the nectar reward and become dusted by pollen if they crawl over the strap-like anthers

• “Relatively unintelligent insects like beetles can act as pollinators.” 1  

1 http://www.cas.vanderbilt.edu/bioimages/pages/pollination.htm

http://flickr.com/photos/oroboros72/2578117137/

Beetle covered with pollen on Magnolia

http://farm1.static.flickr.com/151/436570953_91be748c40.jpg?v=0

HIGHER EVOLUTION PLANTS AND POLLINATORS

Bees – the Major Pollinator of Flowering Plants

• Bees are adapted for feeding on nectar for energy and pollen for protein and other nutrients

• Most pollen is used as food for larvae

• Have a long proboscis – a complex “tongue” that enables them to obtain the nectar from flowers

• Bees that are deliberately gathering pollen are more efficient pollinators

• It is estimated that one third of the human food supply depends on insect pollination, most of which is accomplished by bees

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

Wasp->Bee• Bees, like ants, are a specialized form of wasp• Change from predator to collecting pollen• “The switch from insect prey to pollen may

have resulted from the consumption of prey insects that were flower visitors and were partially covered with pollen when they were fed to the wasp larvae.”2

2 ^ Poinar, G.O. Jr., Danforth, B.N. 2006. A fossil bee from early Cretaceous Burmese am 4. ber. Science 314: 614.

Which Came First?• Flowers

• But the bees and the flowers and other pollinators have all evolved –

Co-evolution• Benefit of the flower• Mutually beneficial• Dependent – very specialized

Examples of Co-evolution• Dependence - Yucca and moth • Gentian and Carpenter Bee – Floral

sonication• Benefit to the flower; defenses against

herbivores – Passionflower and Butterfly• Benefit to the flower – Mimicry and fakery –

Orchid and bee• Mutual – Moth and orchid• Mutual – Ant and Acacia• Mutual – Fly and the Flower• Mutual – Columbines and shape shifts

Dependent Partnerships

Some are so dependent upon one another that were one to disappear, the other would very likely either starve or remain sterile.

Secret Life of Plants

YUCCA AND THE YUCCA MOTH - DEPENDENCY

http://cornellcollege.edu/biology/insects2003/ianpat/images/yucmoth2.jpg

• The pistil (female part) of each flower ends in a three-lobed stigma.

• In order for pollination to occur, masses of pollen must be forced down into this central stigmatic hole.

• The female yucca moth gathers pollen from the flower anthers by using her specially adapted mouthparts.

• She forms the sticky pollen into a ball. The pollen ball is then "stuffed" or "combed" into the stigma of the various flowers she visits.

Central Stigmatic Orifice• Mojave Yucca

Yucca shidigera

• Chaparral Yucca Yucca whipplei

• Feathery stigma lobes

•Head of a female yucca moth showing the prominent, coiled, maxillary palpi•Used to collect, compact and carry a pollen ball •Only in females

Pollen masses and a stamen from the chaparral yucca

A female yucca moth pushing pollen into the stigma tube of the yucca flower while visiting the flower to deposit her eggs

http://www.fs.fed.us/wildflowers/pollinators/moths.shtml

•Without this process, the yucca flower will not develop into the fruit or pod with seeds.•When the female moth visits the flower, she backs up to the flower base and inserts her ovipositor to lay an egg in one or more of the six chambers.•The chamber protects the egg while it develops.

•Yucca moth larvae feeding on seeds in the yucca fruit.•The cost of some of the fruit is outweighed by having such an efficient pollinator

•By the time the egg hatches into a larvae the yucca will have begun to develop a pod with little seeds.•The yucca and the yucca moth both benefit in the relationship.

MULTIPLE DEFENSES AGAINST HERBIVORES

Passionflower and Zebra Longwing Butterflies

http://www.stetson.edu/~pmay/woodruff/passiflora.htm

•Passion vines produce beautiful, large flowers that are easy to find once they open.

•These large, complex flowers open quickly at about 11 a.m., and last only one afternoon before shriveling and setting fruit. •Passion vine is chemically protected by cyanogenic glycosides, which prevent most plant-eating insects from feeding on it.  • It is, however, fed upon by the larvae of two specialized butterflies, which feed on no other plants.

http://www.stetson.edu/~pmay/woodruff/passiflora.htm

This is Agraulis vanillae, the Gulf Fritillary. These butterflies are often present in large numbers, especially from mid-late summer. Gulf fritillary caterpillars are more often found on passion vines in open, full sun, and are usually found feeding on older leaves away from the tip of the vine.

•These are the eggs and larva of the Zebra Longwing, Heliconius charitonius. •These butterflies lay their eggs in clusters at the very tip of the growing vine, and are more often found on plants that are at least partially shaded.  •Thus, the two species of butterflies seem to avoid direct competition by feeding on different parts of the plants, and selecting different microhabitats.

http://creatures.ifas.ufl.edu/bfly/Zebra_longwing04.htm

Multiple Defense

• Develop trichomes (hairs) on the leaves – hook caterpillars and they bleed to death

http://www.colostate.edu/Depts/Entomology/courses/en570/papers_2002http://uts.cc.utexas.edu/~gilbert/teaching/zoo369/lect6.html

False Larvae

• In some Passiflora the stipules change to look like butterfly larvae

Egg Mimic Nectaries• Female butterfly egg laying and

larval hatch is damaging to the Passiflora

• One larvae can defoliate and entire juvenile plant or prevent seed formation by devouring the flowers

Passiflora boenderi leaf with egg mimic nectaries.

http://www.mobot.org/mobot/research/passiflora/subgenus_Decaloba.shtml

Photo: J.M. MacDougal

In order to avoid competition for

food and cannibalism, Heliconius

butterflies avoid plants that

already have eggs on them

Extrafloral Nectaries• These spots are “extrafloral” because

they are found outside the flower• The nectar that passion vines secrete

attracts ants, as sugar inevitably does. • The mercenary ants, in turn, are

aggressive defenders of their food sources and will kill or drive off herbivores that would eat those sources.

• Thus both parties benefit from the relationship

http://www.virtualherbarium.org/GardenViews/ShapeShifters.html

Chameleon shapes

• Visual Clues can be almost as important as chemical clues

• Passion vines can escape by looking like other nearby plants

• The camouflage pays off just often enough for the Passiflora to reproduce

Heliconius-egg mimicry in Passiflora and shape camouflage

http://www.ucl.ac.uk/~ucbhdjm/courses/b242/Coevol/Coevol.html

THE GENTIAN AND THE CARPENTER BEE

FLORAL SONICATION

• The flowers of the Orphium frutescens in South Africa have 3 large stamens with a long thick anther that seems to be covered in yellow pollen.

• But the yellow anther is hollow and the pollen is held inside.

• The only way it can escape is through a tiny hole right at the top of the anther and there is only one way to extract it.

• The bee knows how3

3 Secret Life of Plants by Peter Tompkins

Orphium frutescens anthers and stigmahttp://fernkloof.com/species2.mv?Orphium%20frutescens

• A Carpenter Bee which has a particular resonance vibrates the pollen from the flower.

• Bees that do not match this resonance cannot pollinate the flower.

• One would think with the vibration of the pollen, it would be scattered everywhere and self-pollination would be a problem. Not so.

• The stigma is not receptive until all the pollen is gone

http://bibleprobe.com/pollination.htm

• The bee makes a high-pitched buzzing noise with its wings as most bees do.

• It continues to beat its wings but lowers the frequency so that the note of its buzz suddenly falls to approx. middle C.

• This causes the anther to vibrate at just the right frequency needed to release the pollen and the grains spout out of the hole at the top in a yellow fountain.

• The bee gathers it up and packs it into the carrying baskets on its back legs.

A Female Carpenter Bee, Xylocopa caffra, buzz-pollinating Orphium frutescens. Cape Peninsula, South Africa

http://home.worldonline.co.za/~cpjones/pollination.htm

Floral Sonication• There are approximately 20,000

flowers that need to be pollinated by vibrations

http://gears.tucson.ars.ag.gov/ic/buzzpol/buzzpol.html

Here we see a small andrenid bee (Protandrena mexicanorum) perched atop a stamen of Buffalo Burr (Solanum rostratrum) follwing a vigorous bout of floral sonication.

DEEP COROLLA TUBES

Some plants have evolved flowers of extraordinary depthThis puzzled DarwinHe suggested that this was a response to a kind of ‘race’ with pollinating insectsThe length of the tongues of pollinating insects could increase to increase nectar foraging efficiency

http://www.missouriplants.com/Blueopp/Phlox_amplifolia_page.html

ORCHID AND THE MOTH

MUTUAL DEPENDENCEORCHID AND SPECIFIC POLLINATOR

Moth and orchid in Madagascar

• Angraecum sesquipedale species word means ‘a foot and a half’

• Long trailing spurs which hold its nectar

• Darwin predicted that the flower was pollinated by a moth with tongue long enough to raid the spur.

• Forty years later, just such a moth was discovered!• Long after Darwin's death, the predicted pollinator

was discovered, a hawk moth now named Xanthopan morganii praedicta (praedicta meaning predicted).

• It had an appropriately long proboscis. This was a perfect example of mutual dependence of an orchid and a specific pollinator

• It is the only pollinator of this orchid

http://www.orchids.mu/Species/Angraecum/Angraecum_sesquipedale.htm

• http://www.geocities.com/pennypoint9/longicalc.jpg

http://www.orchidspecies.com/angsesesquipe.htm

COLUMBINES -SHAPE SHIFTING

Justen Whittall and Scott Hodges 

• University of California, Santa Barbara• Studied the evolution of the Columbine• Spurs are from 1 to 12 cm• Changes in length based on change in

pollinator

• Bumblebees – short tongue• Hummingbirds – longer tongue• Hawkmoths – longest tongue• More variety in North America• No hawkmoths in Eurasia thus

shorter spurs in Eurasia

Reference: Whittall & Hodges. 2007. Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature

447: 706-709.

http://pollinator.com/queen_bumblebee.htm http://www.pbase.com/mroper/image/71250086 http://www.wunderground.com/data/wximagenew/n/novembergale/214.jpg

http://fireflyforest.net/firefly/2005/12/15/golden-columbine/ http://www.fs.fed.us/wildflowers/pollinators/plantstrategies/images/black-chin_hummingbird_yellow_columbine_lg.jpghttp://www.fortnet.org/NCBA/Columbine1.jpg

THE FLOWER AND THE FLY

Nectar

• Attracts animals that carry pollen• Corolla spurs are a hollow, hornlike

extension of a flower that holds nectar in its base.

• The length has to be longer or matched to the pollinator to force contact and transfer pollen

Meganosed fly

• Pollination benefits from long floral tubes

• Nectar-seeking insects must press their bodies closely against pollen-bearing floral parts to reach nectar pools at the end of the floral tube

• Cycle of lengthening organs in both flower and fly

http://www.naturalhistorymag.com/master.html?http://www.naturalhistorymag.com/0305/0305_feature.html

Photo © Steven D. Johnson

Meganosed Fly

• Moegistorhynchus longirostris of southern Africa has the longest mouthpart of any know fly

• 4 inches from it’s head• 5 times the length of

its body

Plant Guild• A group of unrelated plant species

that benefit each other• In this case the meganosed fly is the

sole pollinator to a guild of species• All have long, straight floral tubes or

spurs• Brightly colored flowers open during

the day and no scent

The Guild

Iris – Lapeirousia anceps

African Corn Lily - Ixia paniculata

Orchid - Disa draconis

Geranium-Pelarbonium suburbanum

Differences within the

Guild• Each deposits

their pollen on differing parts of the nectar-seeking fly

http://picasaweb.google.com/Marland.CapeTown/GERANIUMSOfTheCapePeninsula#5149176058538116722

MIMICRY AND DECEPTION

THE ORCHID AND THE BEE

Ophrys speculum

http://www.plata.gr/chania/flaura.asp http://www.treknature.com/gallery/Europe/Spain/Extremadura/photo49863.htm

• The Mediterranean orchid Ophrys speculum manufactures whiffs of the same scent that the female wasp Campsoscolia ciliata does.

• The flower misleads male wasps into mating attempts that benefit the plant by spreading pollen

• The orchids produce the fragrance more abundantly than female wasps do, and males prefer the stronger bouquet

• With brushy red hairs, the Ophryrs speculum blooms look vaguely like the wasps that pollinate them.

http://www.guenther-blaich.de/fmd/ospecwas.jpg

Campsoscolia ciliata

Ophrys speculum Mirror Orchid

In an extreme case of sex fakery, an orchid produces oddball chemicals that mimic a female wasp's allure so well that males prefer the floral scents to the real thing, scientists say.

ACACIA AND THE ANT

MUTUALLY BENEFICIAL

Bullhorn Acacia

Acacia and the Ant

• Acacia’s defense against browsing animals are long, strong thorns.

• Soon after the acacia grows a thorn a queen ant who has already mated lands upon it and gnaws a hole near the tip, just big enough to allow her to crawl into the hollow base.

• There she lays her eggs

Bullhorn acacia and ant mutualism: thorn and extra-floral nectary, Costa Ricahttp://ecolibrary.cs.brandeis.edu/display.php?id=Ant_w_bullhorn_acacia_thorn_DP162

• The young works come out of their thorn home every day and patrol the stems and leaves hunting for insects that may land on the acacia trying to nibble its leaves

• The ants eats these insects

Nectary Hole in the thorn

The acacia produces nectar from glands along the lower part of the leaf-stalksThe nectar flows all year round

http://www.marietta.edu/~biol/biomes/images/tropseas/20dimg_1253cu.jpg

• The ants also destroy seedlings of other kinds of plants that might germinate within a radius of about a foot.

• They also mutilate leaves from other plants that touch the acacia causing the branch of the other plant to die back.

• The plant also provides solid food in the form of small orange beads, rich in fat on the tips of the leaflets.

• A worker cuts up the beads into pieces and places into a pocket below the head of the larva – available to eat later.

• These are called Beltian Bodies, formed particularly on the tips of newly developed leaves. 

Beltian bodieshttp://pick5.pick.uga.edu/mp/20p?see=EL_DP161

Conclusion

• The flower did come first• These are just a few examples of

the fascinating modifications among plants and pollinators

• Co-evolution is all around us• Observe and enjoy!