What's that smell?

Investigation into carrion and faecal mimicry is not the most popular research topic in evolutionary biology. As mammals, it is ingrained in us to avoid such things because of the potential diseases and pathogenic microbes that may be harbored within them.

It is proposed that carrion and faecal mimicry in flowers has evolved to not only attract pollinators, but also to deter herbivorous mammals (Lev-Yadun and Gutman, 2013). Carrion and faecal mimicry is also hypothesised to give a false warning to herbivores of nearby predators. Flowers mimic the scent of carrion which would likely be surrounded by carnivores, or of predator’s urine or faecal matter to fake the recent passing of a carnivore. This fear of predation has been known to influence the herbivores behavior in such a strong way that vegetation structure can be completely changed (Lev-Yadun and Gutman, 2013). Some hypotheses even go as far as to say that carrion odor may assist plants by attracting large carnivores, which may then defend them from herbivores (Lev-Yadun et al., 2009). Research has shown that the mimicking flowers rely heavily on the volatiles used by flies as cues to locate carrion and faeces (Johnson and Jürgens, 2010). It has been discovered that the oligosulphides emitted by the Mediterranean Arum flower are identical to those emitted by animal carrion and trigger the same electrophysiological response in fly antennae (Johnson and Jürgens, 2010). This shows amazing mimicry of the chemical cues given by carrion to successfully exploit carrion flies.

The primary purpose of the odorous emissions is a hotly debated topic, for example the Rafflesia genus only emits odours during its reproductive season, leading to the conclusion that the attraction of pollinators is the primary function of the chemical emissions (Lev-Yadun et al., 2009). Despite this conclusion scientists argue as to whether the evolution of odours was primarily to repel herbivores, or for the attraction of pollinators. 

Rafflesia spp. adapted from http://liseblog.dk/thailand-2012/

Australia - Deception 'hotspot'

The Australian continent is known for its profound concentration of deceptive organisms. Orchids are the favored deception example in the plant kingdom, with sexual deception resulting in over 11 genera and hundreds of species; complementing Australia’s reputation as the deception ‘hotspot’ of the world.  An interesting paper released late last year by Herberstein et al. (2013), suggests and discusses a few distinct reasons why this might be so.

“Is the prevalence of some deceptive systems a reflection of species diversity?”

This hypothesis questions whether the diversification of deceptive species could be a function of overall species diversity. If this were the case then the overall species diversity of plants would be largely proportional to the diversity of the corresponding deceptive species. Using orchids again as an example, only ~5% of worldwide species occur in Australia, which is a very low species diversity and does not explain the high number of deceptive species. Using orchids and other animal and plant examples, Herberstein et al. (2013) concluded that deceptive systems are not a reflection of species diversity.

“Does deception evolve readily in Australia?”

This hypothesis investigates Australia’s environmental conditions, and its isolation and potential for invasion. Australia is mostly dry, with poor soils and frequent fires, phenomena which have been used to explain the production of nutrient poor biomass (can result in low rates of herbivory) along with ample amounts of sap and nectar (which can lead to pollination by larger animals). These environmental restrictions may have increased the selection for behavioral strategies that minimise the costs to survive, e.g. floral rewardlessness in orchids, as well as fragmentation of species due to fire regimes promoting selection for gene flow across larger distances. If harsh environmental conditions are a driver for the evolution of deception, that is where a high number of deceptive systems are likely to occur. Due to limited information in the literature, Herberstein et al. (2013) urge further research into the frequency of deception in harsh environments to help support or disprove this hypothesis.

Australia has been subject to a long history of evolutionary isolation and recent invasions, which may explain a radiation of deception. If this were the case, then it can be predicted that most deceptive species have only recently arrived in Australia, and seek to exploit naïve and endemic species. Australia’s Mediterranean and tropical climates have given rise to high levels of endemism and biodiversity; which provides a broad variety of potential deception targets. Isolated populations are typically vulnerable to exploitation by invasive species, the mixing of invasive species with existing species can lead to new symbiotic relationships; and perhaps even deception relationships.

“Does Australia’s intellectual and research culture encourage discovery of deception?”

Herberstein et al. (2013) discuss their final hypothesis of high levels of Australian deceptive species as being the result of recent research popularity. They predict that the popularity of certain research areas leads to a higher than expected reporting of similar phenomena; including the discovery and investigation of new deceptive species. For example, behavioral ecology in Australia is thriving, especially when the number of research institutions are compared with other nations. Over the years 2010 and 2011 8% of papers published in Behavioral Ecology were authored by Australian researchers and institutions, compared with 16.5% of papers being from the United Kingdom, which has 3 times the number of institutions as Australia. However, Herberstein et al, (2013) issue caution when presenting this hypothesis. This is because a more thorough investigation and analysis on the number of publications on deceptive and non-deceptive systems is needed for a comprehensive evaluation of the high number of Australian deceptive species due to potential publication bias.

Descriptives of the higher education environments in Australia, Europe, United Kingdom, United States of America, Canada, and Japan, indicating Australia’s surprisingly large proportion of behavioral ecologists and consequent contribution to the journal Behavioral Ecology given the relatively few research institutes. Adapted from Herberstein et al. (2013).

Sexual deception, for males or herbivores?

Sexual mimicry when employed by orchids is incredibly effective, and in many orchids the deception is twofold. Counterfeit insect sex pheromones are released to attract male pollinators over long distances, and when within close proximity, the males are tricked once again with a floral structure visually resembling a female insect (Gaskett and Herberstein, 2010). This tactic is well documented in the Australian orchid species Cryptostylis, which targets a particular male wasp; Lissopimpla excelsa. Although sympatric Cryptostylis species share the same pollinator they never hybridize, even after hand cross-pollination, and their exact phylogenetic relationships are still largely unknown (Gaskett, 2012). 

Gaskett (2012) hypothesise that male pollinators display such strong affinity toward sexually deceptive orchids because normal mating behavior involves the engagement of several sensors, most of which the orchids successfully mimic and cater for. To attract male Lissopimpla excelsa wasps the Australian Cryptostylis send out a single odor compound, a compound which is shared throughout the species. Once attracted and within close proximity, the male wasps are then enticed to land on the flowers by red-orange wavelengths, yellow pollinia and UV reflections; which closely mimic that of a female wasps wings. This deception illustrates an incredibly species-specific mimicry of female wasps, while also exploiting the insect’s intrinsic attraction to UV and yellow wavelengths (Gaskett and Herberstein, 2010). Raised stripes and bumps on the flower surface indicate close mimicry of female wasp body length and thorax dimensions, which may be used to aid in a male wasps grip and help to align him in contact with the pollinia and stigma (Gaskett, 2012).

a C. erecta, b C. subulata,
c and d C. leptochila,
e C. ovata,and f afemale
L. excelsa wasp. Adapted from Gaskett and Herberstein (2010)

While many articles focus on the hypotheses that female wasp mimicry is employed to attract males and aid in pollination, another near forgotten hypothesis is being re-explored. This is the hypothesis that sexual mimicry is actually a sophisticated form of anti-herbivory defense. Lev-Yadun and Ne’eman (2012) revisited the notion that visual bee and wasp mimicry is not just for male pollinators, but also for herbivores. Because many herbivores associate bees and wasps with aggression and nasty stings they are avoided, hence the perceptual biases of herbivores toward these insects may cause a tentative approach to the sexually deceptive orchids and decrease their rate of herbivory (Lev-Yadun and Ne’eman, 2012).

The living stones

Southern Africa is home to the richest source of succulents in the world, with 40 percent of the world’s plants occurring in South Africa alone; the Lithops genus in particular, comprising of a massive 37 species and 93 varieties (Kellner et al., 2011). Kellner et al. (2011) hypothesised that the Lithops are such a large and widespread genus because of their unique mimicry technique. Lithops mimic the geological patterns around them, resulting in their appearance largely resembling a stone, giving them the nickname of “Living stones” or the “Pebble plant”. 

Variation of leaf colour within Lithops
karasmontana (A = L. karasmontana ssp. bella,
B, C = L. karasmontana ssp. eberlanzii,
D, E, F = L. karasmontana ssp. karasmontana). Adapted from Kellner et al. (2011)

 The plant structure consists of two opposite succulent leaves, with the leaf tips almost entirely sunken into the ground. This compact growth form is thought to have developed to protect the leaves against evaporation, and to be hidden from herbivores such as the cape hare (Lepus capensis) and the armored ground cricket (Hetrodes sp.) (Kellner et al., 2011). Because nearly all of the plants light capture and photosynthetic tissue is located underground, the exposed parts of the plant are translucent, which likely allows light penetration deep into the leaves where the chlorophyllous tissues are situated. Despite a seemingly perfect design, Lithops frequently experience overheating from the large amounts of solar radiation allowed though the translucent leaves, which is reported to reduce photosynthetic activity (Martin et al., 2013).

 While many plants have adaptations to minimise overheating, such as high transpiration rates, reflective waxes or convective heat exchange, this is generally lacking in most African succulents, including the Lithops (Martin et al., 2013).

Although the Lithops incur operational problems, this has not hindered their highly effective ability to adapt to and mimic their local surroundings. The extremely variable geological patterns of southern Africa has been suggested as the cause of such a large variety of colours, patterns and surface structures in the genus. Species of Lithops can be found on every soil formation in southern Africa, ranging from limestone to granite, with each species flawlessly blending in with the local geology (Kellner et al., 2011).

It has been theorised that it is the Lithops’ mimicry capability that has triggered such a large variety of species and their widespread occurrence across southern Africa, and although Lithops experience lowered photosynthetic activity, it seems that the skill of mimicry is enough to overcome the genus’ photosynthetic constraints (Kellner et al., 2011).

Don't touch me, I'm sick

Caladium steudneriifolium is a plant found in the rainforest of south east Ecuador, that has evolved a method to avoid herbivore attacks. The plant has evolved two distinct leaf phenotypes; one which is green, and one which is variegated. The development of the variegation phenotype is believed to be (Soltau et al., 2008) a form of mimicry; posing as a leaf that has been attacked by the larvae of the mining moth. This mimicry was seen in one third of C. steudneriifolium leaves randomly chosen and studied by Soltau et al. (2008), and it was estimated that infestation by a mining moth was 4 – 12 times higher for the green leaf phenotype than it was for the variegated form. 

To support their hypothesis of damaged leaf mimicry, Soltau et al. (2008) set up a test to decipher if the mining moth was using visual cues to detect and avoid previously hosted leaves. To do this they painted green leaves with white correction fluid in a similar pattern to the variegated leaves. To ensure that neither the chemistry or texture of the correction fluid was effecting a female’s propensity to lay her eggs, un-pigmented correction fluid was placed on green leaves. It was then established that there was no significant difference between untreated and treated leaves. It was found that the leaves painted with white correction fluid experienced the similar low rates of moth attack as the leaves with natural variegation; herbivore attack mimicry was then successfully supported as a hypothesis and the female moths are indeed using visual cues to determine oviposition sites.

a. is a plain leaf, b. is a leaf infected with mining moth larvae, c. is a variegated leaf, d. is a plain leaf painted with correction fluid. Adapted from Soltau et al. 2008.

 

 

 

 

 

Although variegation successfully reduces the risk of mining moth oviposition, the overall growth and health of the leaf is compromised. This is because the leaf sacrifices chloroplasts to create the whitish patterns; which effects the absorption and utilisation of light, hence reducing overall net photosynthesis.

Despite the leaf’s handicap of a lower net photosynthetic rate, variegated leaves become comprehensible when the life span of a damaged leaf is taken into consideration. Once epidermal damage is caused by the mining moth larvae, the leaf is then open to attack from varieties of fungi which can quickly destroy leaves. Leaf variegation in Caladium steudneriifolium has consequently been shown to be of high selective advantage, regardless of the loss of photosynthetically active leaf area.

Orchids; The masters of floral deception

Orchids are well known to be the masters of floral deception, with up to one third of all species completely lacking floral rewards such as nectar or harvestable pollen (Internicola and Harder, 2012). Generalised food deception (GFD) is the most common mechanism utilized by orchids to attract pollinators (Peter and Johnson, 2013), and operates by using a pollinator's instinctive expectations of a rewarding flower, and copying it. Orchids use sweet scents, bright contrasting colours and petal patterns which trigger powerful food seeking behaviors in pollinators, to allure them into their flowers (Peter and Johnson, 2013).

Internicola and Harder (2012) describe how although deceptive orchid species pose very little competition to rewarding species, they have developed adaptations for successful reproduction;  

•  Flowering early in the season, which avoids competition with rewarding species and exploits naive pollinators (pollinators which are young and inexperienced).

• Flowering for extended periods, which maximizes the chance of pollination when faced with infrequent visits and experienced pollinators.

Although orchids can reproduce successfully when employing GFD, they are very restricted. For example a deceptive orchid species can only exist as a few individuals over a large area to reduce the risk of associative learning (the ability a pollinator to remember, and avoid reward lacking species). After investigating associative learning between Calypso bulbosa and bumble-bees, Internicola and Harder (2012) discovered that while associative learning had severe consequences for most deceptive orchids, it had a limited effect on deceptive species that were specifically mimicking a co-occuring rewarding species. It is assumed that overall, the bumble-bees associated that particular morphology of flower with a reward; after visiting a rewarding species after a deceptive species, the bumble-bee was left with no negative associations. This provides evidence supporting that the use of GFD in orchids is far more successful in mimics than general deceptionists, due to positive associative learning, resulting in continued visitation from pollinators.

Calypso bulbosa flowers, photographed by Magnus Manske