Monday, March 7, 2016

Natural Pollination of the Genus Narcissus

[This article first appeared in The Bulb Garden (Volume 13, issue 2 - Spring 2015), the quarterly publication of the Pacific Bulb Society. I was displeased with the original article for a number of reasons, and that it could only be read by members of the PBS, so I decided to rewrite it here so it can be available to everyone. I hope you enjoy it!]

The genus Narcissus is arguably one of the most iconic and recognizable insect pollinated plants in the world. Most of this attention is attributed towards the appearance of the flower, the typical “daffodil,” but little is attributed to the purpose of the form. Why purpose does the corona serve? Why are the anthers of some species tightly constricted in the floral tube while those of others protrude out past the cup? Is there significance of pendant versus upward facing flowers? The answers to these questions and more can be clarified by illuminating some of the relationships between different groups of Narcissus and their natural pollinators. Most species are not self-compatible, and instead require insects to pollinate the flowers. After all, the purpose of any flower is sexual -- to propagate the species and to facilitate adaptation to changing conditions through gene flow.

Narcissus hybrid
For those not familiar with the genus Narcissus (though I suspect most are quite familiar, perhaps enough to dislike them) I can offer the following brief description: All Narcissus grow from true bulbs, underground storage organs composed of modified leaf scales. The roots of Narcissus are contractile, meaning they pull the bulb to the optimal depth for the location (therefore it is best to err on the shallow side when planting Narcissus bulbs rather than too deep, which can decrease flowering or kill the plant). Flowers are produced singly or in umbels of up to 20, depending on the type. With the exception of a few Autumn blooming species, Narcissus are mostly Winter or Spring blooming perennial bulbs from Portugal and Spain in the west, France in the north, southward into North Africa, and eastward into the Middle East. While the exact natural range is subject to debate (due to centuries of naturalization by ancient growers), the center of diversity for Narcissus is in the Iberian Peninsula. Where species distributions intersect, natural hybrids occur, aiding in the confusion (many named “species” may in fact be discovered to be naturally occurring hybrids).

Soft-winged flower beetles (Family Melyridae) on a Narcissus jonquilla hybrid
Species grow at many different altitudes, ranging from near sea level to over 8,000Ft. Some require a cold period to flower, such as the large yellow trumpet daffodils so commonly grown, but there are many lowland species that grow well even in subtropical climates. For example, the Berkeley Botanical Garden (USDA zone 9) grows a variety of species that require little to no chilling. Cold requirements transcend to the hybrids, which after all were bred from species of varying needs. Typically the larger flowered hybrids need a chilling period while some of the small flowered hybrids (with lineages including the species N. tazetta, N. jonquilla, N. papyraceus, and others) can do without low temps and will flower mid-Winter.

Narcissus 'Jetfire': an early blooming N. cyclamineus hybrid that is attractive to bumblebees
Most Narcissus bloom in late Winter or early Spring, often when weather is unpredictable and the sun is not guaranteed to show up every day. The few pollinators that are active at this time of year have to contend with the adverse and unpredictable weather conditions, and may not be able to leave their nests on days when weather is too poor. Narcissus overcome this setback by having a relatively long bloom period of around two weeks, cooler temperatures apparently extending the bloom period (compared with my observations of late blooming species such as N. poeticus L. which has a brief bloom period when it is warm). The stigma remains receptive for most of the bloom period, while the anthers and pollen are subject to the elements. Pendant flowers or those with concealed anthers, as well as large coronas, are well adapted to avoid the impact of such weather. Downward facing flowers also keep rain out so as not to dilute the nectar (various types of bees have been known to select the flowers with the highest sugar content, dilution by rain being an obvious drawback).

Bombus sp. on Narcissus 'Thalia'
Spencer C.H. Barrett, a notable researcher and professor in the Department of Ecology and Evolutionary Biology at the University of Toronto, has split the genus Narcissus into two main groups based on morphology and correlated pollinator preference. The "daffodil" type is characterized by a broad or extended corona, relatively short floral tube (corolla tube), and anthers within or longer than the corona. The flowers are often held horizontally or are pendant as in N. triandrus L. This type is best exploited by bees, including solitary Anthophora sp. and colony forming Bombus sp. Both are active early in the year and able to fly in overcast and/or cold conditions, unlike honeybees, by vibrating their flight muscles to generate the necessary warmth. Other bees in the family Apidae, which includes Anthophora and Bombus, as well as Apis (honeybees), Andrena, and others have been observed foraging on the flowers of various species in their native locales or in gardens abroad. Various types of flies also make use of this flower type early in the year and may contribute to pollination. Examples of the “daffodil” form include Narcissus bujei (Fern.Casas) Fern.Casas, N. calcicola Mendonça, N. hispanicus Gouan, N. longispathus Degen & Hervier ex Pugsley and N. pseudonarcissus L. and many more.

Narcissus 'Minnow': a N. tazetta hybrid that attracts few to no pollinators in my garden, but is nonetheless a delightful miniature and quite welcome here.
The "paperwhite" type is characterized by having a short flared corona, a long narrow tube, and anthers concealed in the corolla tube, often three stamens longer than the other three so that only three anthers are visible. This type most often has flowers held horizontally or even slightly upwards, particularly in the case of umbel forming species. These are best suited for Lepidoptera (moths and butterflies) as opposed to bees. Moths such as the diurnal hawk moth Macroglossum stellatarum, are the most documented floral visitors to many species of “paperwhite” form Narcissus in Europe, and are the confirmed primary pollinators of many species. Narcissus assoanus Dufour ex Schult. & Schult.f., N. dubius Gouan, N. jonquilla L., N. papyraceus Ker Gawl., N. poeticus L., and N. rupicola Dufour are examples of the "paperwhite" form. Bees and flies occasionally visit species of this type, but are often morphologically unable to pollinate the flowers since the stamens are within the corolla. Nocturnal moths have been suspected as pollinators of species such as night scented N. viridiflorus Schousb., but no published observations have been made to date.

A honeybee inside a trumpet daffodil
Other strategies are utilized by Narcissus to lure pollinators. One study on Narcissus longispathus (Herrera 1995) discovered a mini greenhouse effect created by the species' corona. There was an astonishing 10°F difference inside the corona (warmer closest to the anthers) when compared to the ambient air temperature surrounding the flower. The temperature difference was enough to entice solitary Anthophora mining bees to enter the flowers for the pollen and nectar, as observed in the study. Anthophora were proven to have the ability to generate heat when in flight, but not while they weren't flying , so the warmth inside the flowers of N. longispathus had enabled them to stay warm enough to take off and fly to the next flower. In my view it is worth exploring an assumption that all "daffodil" types have this greenhouse effect, and that it has evolved to entice bees to enter the flowers.

Wood-boring beetles (Anthaxia sp.) coupled on a highly scented jonquil hybrid
Scent is utilized by many species of Narcissus to attract its pollinators, though human noses are only occasionally able to detect the various fragrances. Some of the scents produced are more obvious than others (my wife will tell you that N. papyraceus smells like burning rubber!), and some have even been known to induce nausea, as is the case with N. poeticus. Based on the observed pollinators of a variety of Narcissus species, a distinct “Lepidoptera odor” was identified in a study on the various fragrances produced by different species of Narcissus (Dobson, Arroyo, et al. 1997). This odor is sometimes perceived by humans as being musky or spicy. Narcissus assoanus, N. gaditanus Boiss. & Reut., N. papyraceus, and N. serotinus L. (Autumn blooming) were all identified as possessing the Lepidoptera odor. These results correlate with the "paperwhite" form described above by possessing relatively short coronas and stamens that are partially concealed within the corolla tube. By contrast, Narcissus bujei, N. bulbocodium, and N. triandrus, which all have somewhat elongated open coronas and correspond to the "daffodil" form, lacked the Lepidoptera odor and had not been observed to attract moths or butterflies.

A solitary bee (possibly a male Andrena) inside Narcissus 'Jetfire'
In my observations in my garden of pollinator activity and pollinator interest in Narcissus hybrids, the earliest blooming types are most attractive to pollinators. Mind you, I live far from their native range, across an ocean even. The generic yellow flowered trumpet daffodils, with large open coronas, seem to be the most alluring to bees, particularly bumblebees, and occasionally to honeybees. The hybrid N. 'Jetfire', a N. cyclamineus DC. cross, has also attracted bumblebees, possibly because of its early blooming habit. Later in the season, bumblebees had previously been somewhat attracted to N. 'Thalia', a N. triandrus hybrid, yet tend to have little interest in the jonquil or tazetta types blooming nearby.

Narcissus jonquilla hybrids. Beautifully scented, yet not terrific pollinator plants in my garden.
Jonquils and tazettas (usually "paperwhite" forms) tend to be neglected by bees in my garden, with the exception of N. 'Hillstar', a N. jonquilla hybrid, which has attracted a few solitary bees in past years. The strongly scented jonquil and tazetta hybrids bloom a bit late while there are many other nectar and pollen sources available, so it might simply be a case of outcompetition for pollinators. The jonquil and tazetta types were instead of minor interest to small beetles, true bugs, and the occasional syrphid fly. The beetles and true bugs seemed to be interested in the pollen of the tazetta hybrids, and perhaps converging to find mates or use the flowers for shelter. Other arthropods, like earwigs and spiders are also common visitors to Narcissus in my garden for shelter, and may serve a small role as pollen vectors, with the exception of the spiders who do not move between flowers often.

Narcissus 'Thalia': a N. triandrus hybrid
I was not always a fan of the genus, but the facts are hard not to appreciate. Besides serving as some of the beacons of Spring, and some of the earliest flowers to bloom in gardens in the Northern Hemisphere, they are fairly easy to grow and are not bothered by deer or rodents, both of which plague my garden. As pollinator plants, they are rather lacking in their ability to attract many pollinators outside of home, but they are still worth a shot, if not only for their characteristic Spring appearance. If you are planting for pollinators, I suggest the earliest varieties available as there are fewer flowering plants competing to attract pollinators. Every garden is different, no doubt, so experimentation will yield the best route to success in utilizing Narcissus as a pollinator plant, and I'd like to hear about it!

Beauty in decay

Arroyo, J.; Dafni, A., 1995: Variations In Habitat, Season, Flower Traits And Pollinators In Dimorphic Narcissus Tazetta L. Amaryllidaceae In Israel. New Phytologist 129(1): 135-145 Http://Onlinelibrary.Wiley.Com/Doi/10.1111/J.1469 8137.1995.Tb03017.X/Pdf 
Barrett, S.C.H., Cole, W.W. & Herrera, C.M. (2004). Mating Patterns And Genetic Diversity In The Wild Daffodil Narcissus Longispathus (Amaryllidaceae). Heredity 92: 459–465. Http://Labs.Eeb.Utoronto.Ca/Barrettlab/Pdf/Schb_212.Pdf 
Barrett, S.C.H. & Harder, L.D. 2005. The Evolution Of Polymorphic Sexual Systems In Daffodils (Narcissus). New Phytologist 165, 45-53. Http://Onlinelibrary.Wiley.Com/Doi/10.1111/J.1469-8137.2004.01183.X/Pdf 
Barrett, S.C.H., Lloyd, D.G & Arroyo, J. (1996). Stylar Polymorphisms And The Evolution Of Heterostyly. In: Floral Biology: Studies On Floral Evolution In Animal-Pollinated Plants (Eds. D.G. Lloyd & S.C.H. Barrett) Pp. 339–376. Chapman & Hall, New York. Http://Labs.Eeb.Utoronto.Ca/Barrettlab/Pdf/Schb_137.Pdf 
Heidi, E.M. Dobson, Juan Arroyo, Gunnar Bergstrom, And Inga Groth. "Interspecific Variation In Floral Fragrances Within The Genus Narcissus (Amaryllidaceae)."Biochemical Systematics And Ecology 25.8 (1997): 685-706. Research Gate. Web. 25 Dec. 2014. Http://Www.Researchgate.Net/Profile/Juan_Arroyo3/Publication/223459487_Interspecific_Variation_In_Floral_Fragrances_Within_The_Genus_Narcissus_(Amaryllidaceae)/Links/00b49528d34835e33a000000.Pdf?Origin=Publication_Detail> 
Herrera, Carlos M. "Floral Biology, Microclimate, and Pollination by Ectothermic Bees in an Early-Blooming Herb." Ecology 76.1 (1994): 218-28. Ecological Society of America. Web. 28 Dec. 2014.

Pérez, Rocío, Pablo Vargas, and Juan Arroyo. "Convergent Evolution of Flower Polymorphism in Narcissus (Amaryllidaceae)." New Phytologist 161 (2003): 235-52. Print. 
Worley, A.C., Baker, A.M., Thompson, J.D. & Barrett, S.C.H. (2000). Floral Display In Narcissus, Variation In Flower Size And Number At The Species, Population, And Individual Levels. International Journal Of Plant Sciences 161: 69–79. Http://Labs.Eeb.Utoronto.Ca/Barrettlab/Pdf/Schb_167.Pdf

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