On That Note...

The plant kingdom has an overwhelming number of species many of which have become specialised to their localised environments. An extraordinary adaptation many have developed is mimicry of other organisms in the local ecosystem to achieve pollination or protection. We have discussed many of these deceptive mechanisms over the past 11 weeks. The complexity of each mechanism is astounding. From the protective deception of Lithops to the olfactory mimicry of carrion and pheromones, the variety of mimics we have discussed provides an interesting look into convergent evolutionary tactics.

Perhaps one of the most fascinating families we have looked at is the Orchidaceae, which comprises the most complex and numerous forms of mimicry in the plant kingdom. The orchids have coevolved to attract and rely upon one or few species of pollinators, which involves the development of species-specific olfactory, visual, and tactile cues.

One of the most important pieces of information these co-evolutionary relationships provide, in all examples we have discussed, is the interdependence of organisms within ecosystems. If these plants rely on one or few species to pollinate, as many do, then it is important to realise the detrimental effects disturbance of these ecosystems can have. If, for instance, humans attempt to control certain insect species we perceive as pests, and these insects serve an important pollinating role, many species could suffer.

Lastly, it is important to realise that all of the information researchers have obtained so far is infinitesimally small compared to what is unknown. Many mechanisms behind mimicry and deception, particularly related to evolutionary origin, are poorly understood. It is also good to note that analysis of relationships from a human perspective can be flawed. Though it is all well and good to recognise these relationships as fascinating, many of these co-evolutionary relationships are of vital importance to the balance of the respective local ecosystem. It is my hope that researchers do and will continue to keep this in mind.

The Bulbophyllum Genus

Many species of wild orchids have myophilous, or fly pollinated, flowers (Tan et al., 2002). The genus Bulbophyllum (Orchidaceae) has flowers that produce a foul-smelling or sweet-smelling scent to attract flies (Van der Pijl and Dodson, 1969). Bulbophyllum (Orchidaceae) is probably the largest orchid genus and contains about 1000 species (Vermeulen, 1991). The Bulbophyllum flowers selectively attract male fruit flies of several Bactrocera species (Tephritidae) (Tan, 1998). After attracting flies by the fragrance it releases, Bulbophyllum flowers ensure the removal and deposition of the pollinarium by its floral lip, which has been modified and adapted to a well-balanced structure of hinged see-saw lip that provides a floral mechanism to assist in pollination by flies (Tan et al., 2002).

Bulbophyllum nudda

Males that feed on the substances produced by these flowers, phenylpropanoids, selectively store the intact chemicals or their metabolites in the rectal glands and release them during the courtship period (Nishida et al., 1993). These compounds are known to boost the pheromone and defense systems of male flies (Tan and Nishida, 1996) while also increasing mating success, thereby greatly benefitting the males of these species (Tan and Nishida, 2000).

Bactrocera cucurbitae

Acquisition of the phenylpropanoids may have evolved initially in the context of sexual selection, particularly female preference for males scented with chemicals derived from flowers (Nishida et al., 1997). In terms of coevolution between fruit flies and plants, these phenylpropanoids may mark the point at which divergence of natural fruit fly attractants occurs in the plant kingdom (Tan and Nishida, 2000). On the contrary, it may be a result of manipulation of the phenylpropanoid molecule by the plant to “convergently” attract multiple fruit fly species in a complex tropical ecosystem (Tan and Nishida, 2000).

References

Nishida R, Iwahashi O, and Tan KH 1993, “Accumulation of Dendrobium superbum (Orchidaceae) fragrance in the rectal glands by males of the melon fly, Dacus cucurbitaeI,” Journal of Chemical Ecology, vol. 19, pp. 713–722.

Nishida R, Shelly TE, and Kaneshiro KY 1997, “Acquisition of female-attracting fragrance by males of Oriental fruit fly from a Hawaiian lei flower, Fagraea berteriana,” Journal of Chemical Ecology, vol. 23, pp. 2275–2285.

Tan KH 1998, “Behaviour and chemical ecology of Bactrocera flies,” The Fifth International Symposium on Fruit Flies of Economic Importance, June 1–5, 1998, Penang, Malaysia.

Tan KH and Nishida R 1996, “Sex pheromone and mating competition after methyl eugenol consumption in the Bactrocera dorsalis complex,” Fruit Fly Pests—A World Assessment of their Biology and Management: Proceedings, IV International Symposium 1994, St. Lucie Press, Delray Beach, Florida.

Tan KH and Nishida R 2000, “Mutual reproductive benefits between a wild orchid, Bulbophyllum patens, and Bactrocera fruit flies via a floral synomone,” Journal of Chemical Ecology, vol. 26, no. 2, pp. 533–546.

Tan KH, Nishido R, and Toong YC 2002, “Floral Synomone of a Wild Orchid, Bulbophyllum cheiri, lures Bactrocera Fruit Flies for Pollination,” Journal of Chemical Ecology, vol. 28, no. 6, pp. 1161-1172.

Van Der Pijl L and Dodson CH 1969, Orchid Flowers—Their Pollination and Evolution, University of Miami Press, Miami, Florida, 214 pp.

Vermeulen JJ 1991, Orchids of Borneo, vol. 2—“Bulbophyllum,” Bentham-Moxon Trust, Toihaan Publishing Co. and The Sabah Society, Kota Kinabalu, Sabah, Malaysia, 342 pp.

Photos

Bulbophyllum nudda courtesy of orchids-flowers.com

Bacterocera cucurbitae courtesy of National Bureau of Agricultural Insect Resources at nbair.res.in

The Dracula Genus

Dracula is a genus of unusual orchids that occurs in the moist and shady montane cloud forests of tropical America (Endara et al., 2010). Comprising approximately 148 mostly epiphytic species, Dracula can be found mostly in pristine forests and less frequently in disturbed habitats from southern Mexico to Peru (Luer 1993). The genus Dracula belongs to the most diverse subtribe of Neotropical orchids, the Pleurothallidinae, which comprises 5 to 8% of the floristic diversity of the Neotropics (Jørgensen & León-Yánez, 1999), and are a mostly fly-pollinated group (Pridgeon et al. 2001, Pridgeon 2005). This particular genus produces flowers that look and smell like small mushrooms (Dentinger et al., 2010). Most of these orchids exhibit a peculiar morphology of the lip-like lowermost petal of the flower that resembles the reproductive surfaces of gilled mushrooms (Luer 1993; Kaiser 2006). Dracula are thought to mimic mushrooms for deceptive pollination by “fungus gnats” seeking places to lay their eggs.

Some of these orchids even produce scents reminiscent of fungi (Kaiser 1993, 2006). Chemical analysis of scents trapped from greenhouse-grown flowers show they are dominated by the "typical flavour compounds of mushrooms" (Kaiser 1993:31, Kaiser 2006). This scent development likely came about via evolutionary experimentation, but once proved successful, became an important part of the Dracula reproductive ecology. It has also been observed that these flowers grow in similar habitats to the mushrooms being mimicked, further confusing the “fungus gnats” (Dentinger et al., 2010). Though debated whether this example represents true mimicry, given the spectacular resemblance of Dracula flowers in appearance, fragrance, timing, and location to mushrooms, as well as the empirical observation that they are pollinated by fungus-seeking flies, this seems to be a exactly that (Dentinger et al., 2010). Once again, this deception between flower and pollinator creates a fascinating basis for the study of co-evolutionary relationships.

References

Dentinger BTM and Roy BA 2010, “A mushroom by any other name would smell as sweet: Dracula orchids,” McIlvainea, vol. 19, no. 1, pp. 1-13.

Endara L, Grimaldi DA, and Roy BA 2010, “Lord of the Flies: Pollination of Dracula orchids,” Lankesteriana, vol. 10, no. 1, pp. 1-11.

Jørgensen PM and  Léon-Yánez S 1999, Catalogue of the Vascular Plants of Ecuador, Missouri Botanical Garden Press, St. Louis, Missouri, USA.

Kaiser R 1993, The Scent of Orchids: Olfactory and Chemical Investigations, Elsevier Science Publishers, Amsterdam, The Netherlands.

Kaiser R 2006, “Flowers and fungi use scents to mimic each other,” Science, vol. 311, pp. 806-807.

Luer CA 1993, “Icones Pleurothallidinarum X,” Systematics of Dracula (Orchidaceae), Missouri Botanical Garden Press, St. Louis, Missouri, USA.

Pridgeon AM 2005, “Dracula,” Genera Orchidacearum, vol. 4 – Epidendroideae (Part One). Oxford University Press, Oxford, United Kingdom.

Pridgeon, AM, Solano R, and Chase MW 2001, “Phylogenetic relationships in Pleurothallidinae (Orchidaceae): combined evidence from nuclear and plastid DNA sequences,” American Journal of Botany, vol. 88, pp. 2286-2308.

Video courtesy of Jacky Poon from jackypoon.org

Caladium steudneriifolium

Leaf variegation is widespread in different genera of Araceae (Croat, 1994). Variegated leaves are characteristic of many species of Angiosperms, in particular among understorey herbs in tropical and temperate forests (Givnish 1990). The partial loss of photosynthetically active surface in variegated leaves affects absorption and utilization of light and, therefore, net photosynthesis, and as a consequence growth and reproduction (Soltau et al., 2009). The existence and relative success of variegated leaf colour forms within Caladium steudneriifolium populations, therefore, implies that there have to be particular selective pressures that support variegation despite the energetic handicap compared to plain leaves (Smith 1986).

Leaves of Caladium steudneriifolium. (a) Plain leaf. (b) Plain leaf with an infestation of leaf-mining moth larvae. (c) Variegated leaf. (d) Plain leaf painted with white correction fluid in a pattern mimicking the natural variegation. From Soltau et al. 2009.

In the case of Caladium steudneriifolium, the colour patterns are predicted to act as classical Batesian mimicry. Soltau et al. observed that the whitish areas of variegated leaves strongly resemble the leaf damages caused by the larvae of mining moths. This suggested that the colour patterns of the variegated leaves mimic these damages to escape oviposition by adult female moths. Among other chemical, tactile or visual cues, insects can visually detect and assess previous infestation during the process of host plant selection (Lev-Yadun and Inbar, 2002). Soltau’s study showed that in the presence of herbivores, leaf variegation can be of high selective advantage despite the loss of photosynthetically active leaf area compared to plain leaves (2009). As such, these plants provide a strong basis for the study of coevolution between plants and herbivores, and the mechanisms underlying predator-avoidance adaptations. 

References

Croat T 1994, “Taxonomic status of neotropical Aracea,” Aroideana, vol. 17, pp. 33–60.

Givnish TJ 1990, “Leaf mottling: relation to growth form and leaf phenology and possible role as camouflage,” Functional Ecology, vol. 4, pp. 463–474.

Lev-Yadun S and Inbar M 2002, “Defensive ant, aphid and caterpillar mimicry in plants,” Biologial Journal of the Linnean Society, vol. 77,pp. 393–398.

Smith AP 1986, “Ecology of a leaf color polymorphism in a tropical forest species: habitat segregation and herbivory,” Oecologia, vol. 69, pp. 283–287.

Soltau U, Dotterl S, and Liede-Schumann S 2009, “Leaf variegation in Caladium steudneriifolium (Araceae): a case of mimicry?” Evolutionary Ecology, vol. 23, pp. 503-512.

The Australian Mistletoes

The Australian Loranthaceae comprise 64 species in 11 genera. A feature of Australian loranthaceous mistletoes is the close vegetative similarity, especially of the leaves, between many species of mistletoe and their usual hosts (Barlow and Wiens, 1977). The parasitic relationship often involves several dominant Australian genera of host trees such as Eucalyptus, Acacia, and Casuarina, and a number of mistletoe genera, including Amyema, Lysiana, Muellerina, Diplatia, and Dendrophthoe (Barlow and Wiens, 1977). Like other plant and animal parasites, mistletoes live in an intimate association with their hosts and derive nutrition from the host, and, of course, share a life-long association with a single host individual (Norton and Carpenter, 1998).

Needle-leaved Mistletoe. Photo: David Watson

           The Australian mistletoes show considerable variation in host specificity that makes for an interesting topic of study (Norton and Carpenter, 1998; Barlow and Wiens, 1977). Several species have very low host specificity and occur on many hosts of considerable taxonomic diversity (Norton and Carpenter, 1998). In tropical forest habitats, high host specificity is not likely advantageous because species dominance in the forest is low. There is likely selective pressure for the physiological capacity to infect and grow on a wide range of host species (Barlow and Wiens, 1977). On the other end of the spectrum, however, there are species of Australian mistletoe that are specific to very few, or even one species of host. In open habitats, where the dominance of one or a few tree species is usual, natural selection favours close physiological adaptations in a mistletoe for growth on the predominant host species (Norton and Carpenter, 1998). In other words, the evolution of host specificity is largely correlated with the development of ecological dominance in plant communities (Barlow and Wiens, 1977).

Eucalypt on left, Mistletoe on right (Barlow, 2012)

Mistletoe on left, Eucalypt on right (Barlow, 2012)

                              

           It has been debated whether or not this phenomenon is true mimicry or just visual similarity, however, research has supported a firm genetic basis on which this mimicry could be founded. Analysis of the genetic variation within and between mistletoe races, compared to that occurring between mistletoe species, might indicate speciation that is host-specific (Norton and Carpenter, 1998). Phylogenetic comparison of mistletoes and their hosts would reveal the relative importance of co-speciation and host-switching events in mistletoe speciation (Norton and Carpenter, 1998). Further research is needed to be sure of this mimetic-genetic relation and its implications for parasite-host evolution and ecology.

References

Barlow B 2012, “Do mistletoes show cryptic mimicry of their hosts?”  Mistletoes in Australia, An Australian Government Initiative.

Barlow BA and Wiens D 1977, “Host-Parasite Resemblance in Australian Mistletoes: The Case for Cryptic Mimicry,” Evolution, vol. 31, no. 1, pp. 69-84.

Norton DA and Carpenter MA 1998, “Mistletoes as parasites: host specificity and speciation,” TREE, vol. 13, no. 3, pp. 101-105.

The Sarraceniaceae Family

Sarraceniaceae is a family of carnivorous pitcher plants native to North and South America. These low-growing perennial herbs are notable for their modified pitcher-like leaves, which serve as pitfall traps to ensnare and digest insects and other small prey. They derive their common name from their hollow tubular leaves, which can take the form of a trumpet, a pitcher, or an urn (Encyclopaedia Britannica, 2015).

The carnivorous pitcher plants of the Sarraceniaceae are generally thought to have developed deceptive mimetic systems, advertising visual and olfactory signals, which provide them with the ability to deceive insects by attracting them into traps (Joel, 1988). The leaves are adapted to function like flowers in attracting insects: they are flowerlike in their striking colour patterns and shapes, and, during their active period in the summer, they exude nectar containing fructose, which is highly attractive to some insects. These leaves passively capture prey that are lured to the leaf’s mouth by its glistening surfaces or unusual colouration and transparent patches. Besides having flower-like leaves, all members of Sarraceniaceae produce flowers that are showy and have an agreeable scent. If an insect or other organism falls into the pitcher, stiff downward-pointing hairs and slippery walls prevent it from crawling back out. Exhausted, the animal eventually drowns in the liquid at the bottom of the pitcher. Protein-digesting enzymes and bacteria break down the insect’s body, allowing nitrates and other useful nutrients to be absorbed by the plant to supplement the poor soil conditions of its environment. The nodding flowers are insect-pollinated and are usually borne on long stalks to keep the pollinators away from the deadly pitchers (Encyclopaedia Britannica, 2015). Thus, these flowers have developed a separate system for attracting pollinators and prey.

Little is known about the evolutionary experimentation that led to the development of these carnivorous tactics, but other families of carnivorous plants have developed similar strategies in response to similar soil conditions (Schwaegerle and Schaal,  1979). New phylogenetic analyses are beginning to reveal the evolutionary relationships and the amount of convergent evolution present in the carnivorous plants, but the amount of research done remains somewhat limited (Ellsion and Gotelli, 2001).

References

Ellison, EM and Gotelli, NJ, 2001, Evolutionary ecology of carnivorous plants, Trends in Ecology and Evolution, vol. 16, no. 11, pp. 623-629.

Encyclopaedia Britannica, 2015, Encyclopædia Britannica Online, Sarraceniaceae. Retrieved 19 April, 2015, from http://www.britannica.com/Sarraceniaceae

Joel, DM, 1988, Mimicry and mutualism in carnivorous pitcher plants (Sarraceniaceae, Nepenthaceae, Cephalotaceae, Bromeliaceae), Biological Journal of the Linnean Society, vol. 35, pp. 185-197.

Schwaegerle, KE and Schaal, BA, 1979, Genetic Variability and Founder Effect in the Pitcher Plant Sarracenia purpurea L., Evolution, vol. 33, no. 4, pp. 1210-1218.

Photo

Photo from Learn About Nature retrieved 19 April, 2015 from http://www.carnivorous--plants.com/pitcher-plant.html

The Passiflora Genus

The Passiflora genus is comprised of about 400 species of tendril-bearing, herbaceous vines commonly called passion-flowers. Some are important as ornamentals; others are grown for their edible fruits (Encyclopaedia Britannica, 2015; Yockteng et al., 2011). Many species of passion-flower are of particular interest to scientists studying coevolution and parasite-host interactions (Williams and Gilbert, 1981). These interactions are particularly complex between certain passion-flower species and Heliconiine butterflies.

One example of a Heliconiine butterfly and a passion-flower.

It is suspected that Heliconiine butterflies have been coevolving with Passiflora for a long time (Gilbert, 1982). Heliconiine butterflies deposit their eggs only on Passiflora vines, where the eggs hatch into larvae that feed voraciously on the leaves of the vine. It’s known that Passiflora plants evolved chemical defences against herbivory by Heliconiine butterflies and other insect herbivores (Williams and Gilbert, 1981). While these defences are effective against its other herbivorous attackers, the Heliconiine butterflies have evolved the ability to circumvent these defenses. The remarkable thing is that some species of the vine now have features that appear to mimic the distinctive bright yellow eggs of the butterflies (Gilbert, 1982). Studies have shown that passion-flower plants that present bright yellow formations on the cuticle of the leaves are likely to deter actual oviposition by Heliconiine (Williams and Gilbert, 1981).

Egg mimic on passion-flower leaf.

It is believed that the morphological development of these yellow spots on the cuticle is the current and ongoing step in the coevolution between these two actors (Williams and Gilbert, 1981).The question of how any one trait of a plant could be causally attributed to natural selection imposed by one species or genus of insects among so many has been investigated in depth for the passion-flower-Heliconiine relationship. With only a few major herbivores such as Heliconiine to account for, interpreting the defensive traits of passion-flower vines is relatively free of ambiguity (Gilbert, 1982). Although not all species that interact with Heliconiine have developed this morphological trait, the hypothesis is that this trait will be developed in the near future, as this coevolutionary step is still in progress (Williams and Gilbert, 1981; Gilbert, 1982). For this reason, these relationships are of particular interest to ecologists and evolutionary biologists. In the far future, who knows how the Heliconiine butterflies will circumvent this new defensive tactic?











References

Encyclopaedia Britannica, 2015, passion-flower, Encyclopaedia Britannica. Retrieved on 14, April, 2015 from http://www.britannica.com/passion-flower
Gilbert, LE, 1982, The Coevolution of a Butterfly and a Vine, Scientific American, vol. 247, pp. 110-121. Retrieved 14, April, 2015 from http://imap.passionflow.co.uk/downloads/gilbert
William, KS and Gilbert, LE, 1981, Insects as Selective Agents on Plant Vegetative Morphology: Egg Mimicry Reduces Egg Laying by Butterflies, Science, vol. 212, no. 4493, pp. 467-469. Retrieved 14, April, 2015 from http://www.jstor.org/stable/1686077
Yockteng, R, d'Eeckenbrugge, GC, and Souza-Chies, TT, 2011, Wild Crop Relatives: Genomic and Breeding Resources, pp. 129-171. 

Photos

Helliconiine retrieved from Heliconius Butterfly Works.
Passiflora retrieved from Grassy Knoll Exotic Plants.
Egg Mimic photo by Lawrence Gilbert.