Definitions

myophily

Pollination syndrome

Pollination syndromes are suites of traits of flowers aimed at attracting a particular type of pollinator (Faegri & van der Pijl, 1979; Proctor et al. 1996). The traits include flower shape, size, colour, reward type and amount, nectar composition, timing, etc. For example, tubular red flowers with copious nectar attract birds; nasty smelling flowers attract flies, etc. The syndromes are the product of convergent evolution in response to similar selection pressures.

Abiotic pollination syndromes

These don’t aim to attract animal pollinators. Nevertheless, they have suites of shared traits.

Wind pollination (anemophily)

Flowers may be small and inconspicuous, green and not showy. They produce enormous numbers of tiny pollen grains (hence wind-pollinated plants may be allergens, but seldom are animal-pollinated plants allergenic). They have large feathery stigmas to catch the pollen grains. They grow in low-diversity stands and are among the taller species in their communities. Insects may visit them to collect pollen, but they are not the most effective pollinators and exert little selection pressure on them.

Water pollination (hydrophily)

Water-pollinated plants are aquatic. Their flowers tend to be small and inconspicuous with lots of pollen grains and large, feathery stigmas to catch the pollen. Many aquatic plants are insect-pollinated, with flowers that emerge into the air.

Biotic pollination syndromes

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.

Bee pollination from mobile beehives is of great economic value for orchards such as apple or almond.

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. 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 butterlies.

Moth pollination (phalaenophily)

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).

Fly pollination (myophily and sapromyophily)

There are two types of fly pollination: myophily and sapromyophily. A diversity of flies (particularly bee flies (Bombyliidae), hoverflies (Syrphidae), etc.) feed on nectar and pollen as adults, and regularly visit flowers, while male fruit flies (Tephritidae) are attracted to and feed on specific floral attractant, which acts as fly's sex pheromone precursor or booster, of some wild orchids (Bulbophyllum species - with highly moveable lip) that do not produce nectar (Tan & Nishida, 2000; Tan et al., 2006). These are the myophiles. Sapromyophiles, on the other hand, normally visit dead animals or dung. They are attracted to flowers that mimic these odoriferous items. They obtain no reward and would quickly leave, but the plant may have traps to slow them down. These plants have a strong, unpleasant odor, and are brown or orange in color. They are not as common as myophilous plants (Jones & Jones 2001). Myophilous plants do not tend to have a strong scent, and tend to be purple, violet, blue, and white, open dishes, or tubes (Kastinger & Weber, 2001). Flies generally utilize many different sources of food making their pollinating activity infrequent and unreliable. However, their sheer numbers and the presence of some flies throughout the year make them important pollinators for many plants (Gullan & Cranston, 2005).

Flies tend to be important pollinators in high-altitude and high-latitude systems, where they are numerous and other insect groups may be lacking (Larson et al., 2001).

Bird pollination (ornithophily)

Although hummingbirds are the most familiar nectar-feeding birds for North Americans, there are analogous species in other parts of the world: sunbirds, honeyeaters, flowerpeckers, honeycreepers, bananaquits, flowerpiercers, lories and lorikeets (Lotz & Schondube, 2006). Hummingbirds are the oldest group, with the greatest degree of specialization on nectar (Lotz & Schondube, 2006). Flowers attractive to hummingbirds that can hover in front of the flower tend to be large red or orange tubes with a lot of dilute nectar, secreted during the day. Since birds do not have a strong response to scent, they tend to be odorless. Perching birds need a substantial landing platform, so sunbirds, honeyeaters, and the like are less associated with tubular flowers.

Bat pollination (chiropterophily)

Bat-pollinated flowers tend to be large and showy, white or light coloured, open at night and have strong odours. They are often large and bell-shaped. Bats drink the nectar, and these plants typically offer nectar for extended periods of time. Sight, smell, and echo-location are used to initially find the flowers, and excellent spatial memory is used to visit them repeatedly (Von Helversen et al. 2003). In fact bats can identify nectar-producing flowers using echolocation, a talent that was only recently discovered (Von Helversen et al., 2003). In the New World, bat pollinated flowers often have sulfur-scented compounds, but this does not carry to other parts of the world (Pettersen et al. 2004). Bat-pollinated plants have bigger pollen than their relatives (Stroo 2001).

Beetle pollination (cantharophily)

Beetle-pollinated flowers are usually large, greenish or off-white in color and heavily scented. Scents may be spicy, fruity, or similar to decaying organic material. Most beetle-pollinated flowers are flattened or dish shaped, with pollen easily accessible, although they may include traps to keep the beetle longer. The plant's ovaries are usually well protected from the biting mouthparts of their pollinators (Gullan & Cranston, 2005). Beetles may be particularly important in semi-desert areas, like South Africa and southern California (Jones & Jones, 2001).

Biology

Pollination syndromes reflect convergent evolution towards forms (phenotypes) that limit the number of species of pollinators visiting the plant (Fenster et al., 2004). They increase the specialization of the plant with regard to pollination. They are responses to common selection pressures exerted by shared pollinators, which generate correlations among traits. That is, if two distantly related plant species are both pollinated by nocturnal moths, for example, their flowers will converge on a form most attractive to the moths (i.e. pale colour, sweet scent, nectar released at the end of a long tube, night-flowering), because the most attractive forms will produce the most offspring.

Advantages of specialization

  • Efficiency of pollination: the rewards given to pollinators, commonly nectar or pollen or both, but sometimes oil (Buchmann 1987), scents, or wax, may be costly to produce. Nectar can be cheap, but pollen is generally expensive as it is relatively high in nitrogen compounds. A plant seeks to obtain the maximum pollen transfer for the minimum reward. Different pollinators, because of their size, shape, or behaviour, have different efficiency of transfer of pollen. And the floral traits affect efficiency of transfer: columbine flowers were experimentally altered and presented to hawkmoths, and flower orientation, shape and colour were found to affect visitation rates or pollen removal (Fulton and Hodges 1999; Hodges et al., 2002).
  • Pollinator constancy: to efficiently transfer pollen, it is best for the plant if the pollinator focuses on one species of plant, ignoring other species. Otherwise, pollen may be dropped uselessly on the stigmas of other species. Animals, of course, do not aim to pollinate, they aim to collect food as fast as they can. However, many pollinator species exhibit constancy, passing up available flowers to focus on one plant species. Why should animals specialize on a plant species, rather than move to the next flower of any species? Although pollinator constancy was recognized by Aristotle, we don’t fully understand the benefits to animals (Gegear and Laverty, 2005). The most common hypothesis is that pollinators must learn to handle particular types of flowers, and they have limited capacity to learn different types. They can only efficiently gather rewards from one type of flower.

some insects have specialisations as do the flowers and this limiting of pollination/nectar source partners may be natures way of creating a niche to deter other species of insect; almost as if success for those with the right adaptations is guarunteed.

Advantages of generalization

Pollinators fluctuate in abundance and activity independently of their plants (Petterson, 1991), and any one species may fail to pollinate a plant in a particular year, thus a plant may be at an advantage if it attracts several species or types of pollinators, ensuring pollen transfer every year. Plants do, in many species, have the back-up option of self-pollination, if they are not self-incompatible.

Criticisms of the syndromes

Some species of plants are visited only by one type or species of animal. These plants often conform to the expectations from the syndromes. Yet pollination syndromes have been criticized because biologists observe that many plant species are visited by very different pollinators (Herrera, 1996, Waser et al., 1996). A flower may be visited by a bee, a butterfly and a bird. Also, relying on one species or type of pollinator causes variable reproductive success across years because pollinator population sizes vary independently (Waser at al. 1996). In such cases, plants should generalize.

Such criticism has led to re-evaluation of the syndromes. First, it is important to realize that pollinators should be grouped not taxonomically, but by their function: how they collect pollen and nectar, and how they find flowers (Fenster et al., 2004). Such functional groups of pollinators may contain many species that exert similar selective pressures. Additionally, pollinator effectiveness is often more important than frequency of visits (Fenster et al., 2004). A frequent visitor may be a poor pollinator, if it does not pick up and deposit much pollen or if it visits plants of many different species. The most effective pollinator may be less frequent, especially as visitation may vary over time. Some of the studies critical of the syndrome concept measure visits, but not actual pollen transfer (Fenster et al., 2004)..

Analysing flower traits and visitation in 49 species in the plant genus Penstemon, Wilson et al. (2004) found that they could separate bird- and bee- pollinated species quite well, but could not easily separate different types of bee visitation. In Tasmania, Hingston & McQuillan (2000) found the syndromes did not usefully predict the pollinators. However, Fenster et al. (2004) concluded in their review that there is “overwhelming evidence that functional groups exert different selection pressures on floral traits.” This conclusion is based largely on studies that either experimentally manipulate flowers beyond the normal range of variation, or that compare related plant species with different pollinators.

References

  • Faegri, K and L van der Pijl (1979). The principles of pollination ecology. Pergamon Press: Oxford..
  • Fenster, CB, WS Armbruster, P Wilson, MR Dudash, and JD Thomson (2004). "Pollination syndromes and floral specialization". Annual Review of Ecology and Systematics 35 375–403.
  • Jones, GD and SD Jones (2001). "The uses of pollen and its implication for Entomology". Neotropical Entomology 30 (3): 314–349.
  • Tan, KH and R Nishida (2000). "Mutual reproductive benefits between a wild orchid, Bulbophyllum patens, and Bactrocera fruit flies via a floral synomone.". Journal of Chemical Ecology 26 533–546.
  • Tan, KH, LT Tan and R Nishida (2006). "Floral phenylpropanoid cocktail and architecture of Bulbophyllum vinaceum orchid in attracting fruit flies for pollination.". Journal of Chemical Ecology 32 2429–2441.
  • Kastinger C, and A Weber (2001). "Bee-flies (Bombylius spp., Bombyliidae, Diptera) and the pollination of flowers". Flora 196 (1): 3–25.
  • Larson BMH, PG Kevan, and DW Inouye (2001). "Flies and flowers: taxonomic diversity of anthophiles and pollinators". Canadian Entomologist 133 (4): 439–465.
  • Lotz, CN and JE Schondube (2006). "Sugar Preferences in Nectar- and Fruit-Eating Birds: Behavioral Patterns and Physiological Causes". Biotropica 38 (1): 3–15.
  • Oliveira PE, PE Gibbs, and AA Barbosa (2004). "Moth pollination of woody species in the Cerrados of Central Brazil: a case of so much owed to so few?". Plant Systematics and Evolution 245 (1-2): 41–54.
  • Pettersson S, F Ervik, and JT Knudsen (2004). "Floral scent of bat-pollinated species: West Africa vs. the New World". Biological Journal of the Linnean Society 82 (2): 161–168.
  • P.J. Gullan and P.S. Cranston (2005). The Insects: An Outline of Entomology. Blackwell Publishing Ltd. (ISBN 1-4051-1113-5)
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  • Von Helversen D, MW Holderied, and O Von Helversen (2003). "Echoes of bat-pollinated bell-shaped flowers: conspicuous for nectar-feeding bats?". Journal of Experimental Biology 206 (6): 1025–1034.
  • Buchmann, SL. (1987). "The ecology of oil flowers and their bees". Annual Review of Ecology and Systematics 18 343–70.
  • Fenster, CB, WS Armbruster, P Wilson, MR Dudash, and JD Thomson. Year=2004 "Pollination syndromes and floral specialization". Annual Review of Ecology and Systematics 35 375–403.
  • Fulton M and Hodges SA (1999). "Floral isolation between Aquilegia formosa and A. pubescens.". Proceedings of the Royal Society of London, Series B 266 2247–2252.
  • Gegear, RJ and TM Laverty (2005). "Flower constancy in bumblebees: a test of the trait variability hypothesis". Animal Behaviour 69 (4): 939–949.
  • Floral traits and adaptation to insect pollinators: a devil’s advocate approach. In Floral Biology (1996). Chapman & Hall, New York. .
  • Hingston, AB and PB Mcquillan (2000). "Are pollination syndromes useful predictors of floral visitors in Tasmania?". Australian Journal of Ecology 25 (6): 600–609.
  • Hodges SA, JB Whittall, M Fulton, and JY Yang (2002). "Genetics of floral traits influencing reproductive isolation between Aquilegia formosa and A. pubescens". American Naturalist 159 S51–S60.
  • Pettersson MW (1991). "Pollination by a guild of fluctuating moth populations: option for unspecialization in Silene vulgaris". Journal of Ecology 79 591–604.
  • Waser, NM, L Chittka, MV Price, NM Williams and J. Ollerton (1996). "Generalization in pollination systems, and why it matters". Ecology 77 1043–1060.
  • Wilson, P, M Castellanos, JN Hogue, JD Thomson and WS Armbruster (2004). "A multivariate search for pollination syndromes among penstemons.". Oikos 104 (2): 345–361.

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