pollination by brood-site deception

12
Review Pollination by brood-site deception Isabella Urru , Marcus C. Stensmyr, Bill S. Hansson Department of Evolutionary Neuroethology, Max-Planck-Institute for Chemical Ecology, Hans-Knöll-Strasse 8, 07745 Jena, Germany article info Article history: Available online 16 March 2011 Keywords: Brood-site pollination Mimicry abstract Pollination is often regarded as a mutualistic relationship between flowering plants and insects. In such a relationship, both partners gain a fitness benefit as a result of their interaction. The flower gets pollinated and the insect typically gets a food-related reward. However, flower–insect communication is not always a mutualistic system, as some flowers emit deceitful signals. Insects are thus fooled by irresistible stimuli and pollination is accomplished. Such deception requires very fine tuning, as insects in their typically short life span, try to find mating/feeding breeding sites as efficiently as possible, and following deceitful signals thus is both costly and time-consuming. Deceptive flowers have thus evolved the ability to emit signals that trigger obligate innate or learned responses in the targeted insects. The behavior, and thus the signals, exploited are typically involved in reproduction, from attracting pheromones to brood/ food-site cues. Chemical mimicry is one of the main modalities through which flowers trick their pollen vectors, as olfaction plays a pivotal role in insect–insect and insect–plant interactions. Here we focus on floral odors that specifically mimic an oviposition substrate, i.e., brood-site mimicry. The phenomenon is wide spread across unrelated plant lineages of Angiosperm, Splachnaceae and Phallaceae. Targeted insects are mainly beetles and flies, and flowers accordingly often emit, to the human nose, highly pow- erful and fetid smells that are conversely extremely attractive to the duped insects. Brood-site deceptive plants often display highly elaborate flowers and have evolved a trap-release mechanism. Chemical cues often act in unison with other sensory cues to refine the imitation. Ó 2011 Elsevier Ltd. All rights reserved. Contents 1. Introduction ........................................................................................................ 1656 2. Brood-site deception in basal Angiosperm ................................................................................ 1656 2.1. How wide-spread is the phenomenon? ............................................................................. 1656 2.2. The trap-release mechanism...................................................................................... 1656 2.3. Modalities of attraction.......................................................................................... 1657 2.3.1. Olfactory signaling ...................................................................................... 1657 2.3.2. Visual signaling......................................................................................... 1657 2.3.3. Heat and carbon dioxide ................................................................................. 1658 3. Different types of brood-site mimicry ................................................................................... 1658 3.1. Brood-site-mimicking chemistry: carrion odors ...................................................................... 1658 3.1.1. An example of carrion mimicry: the dead horse arum ......................................................... 1659 3.2. Brood-site-mimicking chemistry: fecal and urine odors................................................................ 1659 3.2.1. A complex of waste product mimicry: Mediterranean Arum lilies ................................................ 1660 3.2.2. Volatile chemistry of Arum lilies ........................................................................... 1660 3.2.3. Arum visitors and pollinators .............................................................................. 1662 3.3. Brood-site mimicking chemistry: fermentation odors ................................................................. 1663 3.3.1. An example of fermenting fruit mimicry: the Solomon’s lily .................................................... 1664 4. Concluding remarks .................................................................................................. 1664 Acknowledgement ................................................................................................... 1664 References ......................................................................................................... 1664 0031-9422/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.phytochem.2011.02.014 Corresponding author. Tel.: +49 3641 57 1405; fax: +49 3641 57 1402. E-mail address: [email protected] (I. Urru). Phytochemistry 72 (2011) 1655–1666 Contents lists available at ScienceDirect Phytochemistry journal homepage: www.elsevier.com/locate/phytochem

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Phytochemistry 72 (2011) 1655–1666

Contents lists available at ScienceDirect

Phytochemistry

journal homepage: www.elsevier .com/locate /phytochem

Review

Pollination by brood-site deception

Isabella Urru ⇑, Marcus C. Stensmyr, Bill S. HanssonDepartment of Evolutionary Neuroethology, Max-Planck-Institute for Chemical Ecology, Hans-Knöll-Strasse 8, 07745 Jena, Germany

a r t i c l e i n f o a b s t r a c t

Article history:Available online 16 March 2011

Keywords:Brood-site pollinationMimicry

0031-9422/$ - see front matter � 2011 Elsevier Ltd. Adoi:10.1016/j.phytochem.2011.02.014

⇑ Corresponding author. Tel.: +49 3641 57 1405; faE-mail address: [email protected] (I. Urru).

Pollination is often regarded as a mutualistic relationship between flowering plants and insects. In such arelationship, both partners gain a fitness benefit as a result of their interaction. The flower gets pollinatedand the insect typically gets a food-related reward. However, flower–insect communication is not alwaysa mutualistic system, as some flowers emit deceitful signals. Insects are thus fooled by irresistible stimuliand pollination is accomplished. Such deception requires very fine tuning, as insects in their typicallyshort life span, try to find mating/feeding breeding sites as efficiently as possible, and following deceitfulsignals thus is both costly and time-consuming. Deceptive flowers have thus evolved the ability to emitsignals that trigger obligate innate or learned responses in the targeted insects. The behavior, and thusthe signals, exploited are typically involved in reproduction, from attracting pheromones to brood/food-site cues. Chemical mimicry is one of the main modalities through which flowers trick their pollenvectors, as olfaction plays a pivotal role in insect–insect and insect–plant interactions. Here we focus onfloral odors that specifically mimic an oviposition substrate, i.e., brood-site mimicry. The phenomenon iswide spread across unrelated plant lineages of Angiosperm, Splachnaceae and Phallaceae. Targetedinsects are mainly beetles and flies, and flowers accordingly often emit, to the human nose, highly pow-erful and fetid smells that are conversely extremely attractive to the duped insects. Brood-site deceptiveplants often display highly elaborate flowers and have evolved a trap-release mechanism. Chemical cuesoften act in unison with other sensory cues to refine the imitation.

� 2011 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16562. Brood-site deception in basal Angiosperm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1656

2.1. How wide-spread is the phenomenon? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16562.2. The trap-release mechanism. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16562.3. Modalities of attraction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1657

2.3.1. Olfactory signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16572.3.2. Visual signaling. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16572.3.3. Heat and carbon dioxide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1658

3. Different types of brood-site mimicry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1658

3.1. Brood-site-mimicking chemistry: carrion odors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1658

3.1.1. An example of carrion mimicry: the dead horse arum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1659

3.2. Brood-site-mimicking chemistry: fecal and urine odors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1659

3.2.1. A complex of waste product mimicry: Mediterranean Arum lilies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16603.2.2. Volatile chemistry of Arum lilies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16603.2.3. Arum visitors and pollinators. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1662

3.3. Brood-site mimicking chemistry: fermentation odors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1663

3.3.1. An example of fermenting fruit mimicry: the Solomon’s lily . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1664

4. Concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1664Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1664References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1664

ll rights reserved.

x: +49 3641 57 1402.

1656 I. Urru et al. / Phytochemistry 72 (2011) 1655–1666

1. Introduction

In plants, pollination is the process by which pollen is trans-ferred from anthers to stigmas, thus accomplishing sexual repro-duction. Commonly, the process requires the involvement of anexternal vector, abiotic (e.g., wind) or biotic (animals) (Endress,1995). During the evolution of flowering plants, natural selectionhas favored the selection of a variety of reward-attractants andphenotypic floral traits to suit a variety of animal visitors such asinsects, (e.g., bees, moths, beetles and flies) (Bernhardt, 2000;Endress, 2010; Thien et al., 2009) and vertebrates (bats and birds)(Brown et al., 2010; Knudsen and Tollsten, 1995). Typically, despiteconflicts of interest and costs to both parties, the outcome has beena beneficial–mutualistic relationship for both the plant species andits pollinator(s) (Morris et al., 2010).

Flowering plants are predominantly pollinated by insects(Bawa, 1990; Sallabanks and Courtney, 1992). Most insects relyheavily on the sense of smell for their survival and a variety ofodors guide them in their activities. Some examples of odor-dependent behavior are the recognition and localization of mates,the localization of suitable plants for oviposition or feeding, andescape responses depending on alarm odors warning for the pres-ence of a predator (Brodmann et al., 2009; Burger et al., 2010;Desouhant et al., 2010; Jarau, 2009). The insects’ olfactory systemis capable of identifying many volatile compounds against a noisybackground and the olfactory organs are accordingly fine-tuned todetect a limited spectrum of relevant odors (de Bruyne and Baker,2008). Though olfaction is often the primary modality of plant–insect attraction, visual and tactile signals are also exploited aloneor as a part of an integrated system (Raguso and Willis, 2002,2005). To accomplish efficient insect attraction, plants often dis-play flashy, colorful and fragrant flowers and are visited by insectsthat will primarily try to collect as much food as possible, whileminimizing energy and time expenditure (Grant, 1994; Schiestland Schlüter, 2009). However, selection has also favored certaindeceitful mechanisms and floral traits that trick and sometimeseven involuntarily kill pollinators (Renner, 2006).

Deceptive systems are found among a diverse group of plants,the flowers of which signal the presence of a resource withoutproviding it. These plants have thus evolved cues to cheat insectsinto the act of performing pollination. Already the founder ofmodern plant biology, C.K. Sprengel, discovered the existence ofnectar-less, deceptive flowers in the Orchidaceae family in1793. The discovery was greeted with skepticism for a long time.Darwin (1877, p. 37) could not accept the idea, considering in-sects too ‘‘clever’’ to be duped. Today we know that deceptionhas evolved in various lineages of flowering plants. The phenom-enon is particularly well known in the Orchidaceae, whereapproximately one-third of the species deceive their pollinators(Ackerman, 1986; Renner, 2006). A deceptive mechanism re-quires very fine tuning as insects in their typically short life spantry to find mating/feeding breeding sites as efficiently as possi-ble, and following deceitful signals thus is both costly andtime-consuming. Deceptive flowers have accordingly evolvedthe ability to emit signals that trigger obligate innate responsesin the targeted insects (Stökl et al., 2010). There are many waysby which insects can be duped and one of the most widespreadmodalities is chemical mimicry. In this type of deception, odorsoften signal the presence of a mate (Ayasse et al., 2003), a prey(Di Giusto et al., 2010) or of a brood-site (Atwood, 1985). Herewe will focus on this group of deceptive flowers, which emitodors that mimic oviposition cues and attract female insectsseeking for a site where to lay eggs. Deceptive breeding sitemimicry includes carrion and dung fly flowers (sapromyiophily),dung beetles flowers (coprocantharophily) and fungus gnat flow-

ers (mycethophily). It includes some of the largest and flashiestblossoms of the earth (e.g., the giant Amorphophallus, the easternskunk cabbage (Symplocarpus foetidus), the Brazilian dutchman’spipe (Aristolochia gigantea) and the Indian almond (Sterculia foet-ida)). We will (i) give an overview of the phenomenon across theangiosperms (ii) explore which sensory signals are employed toaccomplish the deception; (iii) present specific examples fromthe Araceae family and compare it with other known brood-sitedeceptive systems.

2. Brood-site deception in basal Angiosperm

2.1. How wide-spread is the phenomenon?

Recent phylogenetic studies exploring floral deception inOrchidaceae suggest that pollination by deceit is either an ances-tral trait or a recently evolved phenomenon during the evolutionof this group of plant (Cozzolino and Widmer, 2005). Irrespectiveof whether an ancient or a recent development, it is well estab-lished that non-rewarded pollination occurs in unrelated plantlineages of Angiosperms occurring in basal lineages such as Nymp-haeceae and Monocots (i.e., Laurales and Magnoliales). Renner(2006) reviewed 63 genera and 32 families of Angiosperms, withat least 17 genera displaying brood-site mimicry, and suggestedthat lack of reward has evolved in at least 7500 species ofanimal-pollinated angiosperms.

The most common type of strategy deployed by brood-sitemimicking flowers is to produce odors signaling the presence ofa carcass or of animal waste products (Dafni, 1984; Jürgens et al.,2006; Wiens, 1978). Visual signaling is however also exploitedand, e.g., in Paphiopedilum barbigerum (Orchidaceae) may representthe primary attractant (Shi et al., 2009). The brood-site mimickingflowers attract mainly Diptera (primarily Calliphoridae, Muscidae,Scatophagidae and Sphaeroceridae) and Coleoptera (Staphilinidaeand Scarabaeidae) and have been described from at least 10 Angio-sperm families: Annonaceae, Araceae, Aristolochiaceae, Apocyna-ceae, Burmanniaceae, Hydnoraceae, Orchidaceae, Rafflesiaceae,Sterculiaceae and Taccaceae and Hyacinthaceae (Endress, 1984;Wiens, 1978). However, the phenomenon is not restricted to theAngiosperms. Recent studies indicate that brood-site deception oc-curs also in the Bryophytes and among fungi. The so-called ‘‘dungmosses’’ (Splachnaceae) exploit insects to disperse their asexualspores to a suitable substrate for germination (Marino et al.,2009). The insect-mediated spore dispersal is thought to be a de-rived condition from the more ancestral wind-dispersal, and seemsto have evolved independently several times (Culley et al., 2002).Among fungi, sapromyiophilous interactions with insects arefound in, e.g., Phallaceae, where mostly flies disperse the spores(Tuno, 1998).

2.2. The trap-release mechanism

Plants that imitate an oviposition substrate often display so-called ‘‘chamber flowers’’, though there are examples of ‘‘openflowers’’, e.g., in the genus Stapelia (Ollerton and Raguso, 2006).The development of a floral chamber has been hypothesized tobe based on an increasing demand to protect the reproductive or-gans and to minimize pollen loss during the evolution of theAngiosperms (Dafni, 1984). In deceptive systems the formationof a floral chamber might additionally have been selected to forcethe pollinators to stay longer, since after an unrewarded visit theywould quickly leave the flower thus reducing the probability of asuccessful pollination (Dafni, 1984). In the Araceae family, theevolutionary trend from numerous and bare flowers towards

I. Urru et al. / Phytochemistry 72 (2011) 1655–1666 1657

relatively few flowers situated in a closed protective chamber hasbeen found in, e.g., the genera Acorus, Gymnostachys and Orontium(bare flowers), Zantedeschia, Monstera, Diffenbachia (semi opened),Arisaema, Arisarum, Arum and Cryptocoryne (chamber) (Dafni,1984). Most of the species equipped with floral chambers are pro-togynous (Lloyd and Webb, 1986), where female flower receptiv-ity precede male flower maturation, presumably in order to avoidinbreeding and to increase cross-pollination (Lloyd and Webb,1986). Brood-site-mimicking species with a floral chamber traptheir pollen vectors and release them after a shorter or longerperiod of time. Striking examples are found in the Araceae, Aris-tolochiaceae, Hydnoraceae and Orchidaceae (Bolin et al., 2009;Gibernau et al., 2004; Proctor and Lack, 1996). The trappingmechanism is quite stereotyped across species and families. Inthe Araceae, the trap is formed by a large, fleshy, modified leaf(the spathe), which holds an unbranched axis, the so-called spa-dix, in its central part. The spadix bears the female and male flo-rets at its base inside the chamber (Fig. 1A and C). In theAristolochiaceae the trap is a tubular calyx; the basal part ofwhich forms a chamber (the utricle) connected to a tube that isexpanded at its end and is often very colorful (Sakai, 2002). Theflower shape gives the common name of ‘‘Dutchman’s pipe’’ tothe family. In the root-parasite family, Hydnoraceae, the trapchamber is trilobite with no leaves (Bolin et al., 2009). Insectscrawl down into the trap-chamber, where they are forced to stayuntil the male florets release their pollen. To detain the pollinat-ing insects many of the Araceae–Aristolochiaceae species use aring of trichomes (Fig. 1B) and sterile-modified flowers in combi-nation with waxy-smooth walls. The sterile-modified flowers lo-cated above the male flowers act both to block the exit/entrance to the floral chamber and as a filter to allow only suit-ably sized pollen-vectors to enter (Dormer, 1960; Oelschlägelet al., 2009). In members of the genus Sterculia (Sterculiaceae),and Tacca (Taccaceae) no tube-shaped floral trap is present andinsects are instead drawn in from lateral entrances (Endress,1995; Van der Pijl, 1953; Young, 1984). An example of convergentevolution is represented by the orchid Pterostylis coccinea and thearoid Arisaema hunanense, where both have evolved remarkablysimilar designs and mechanisms to trap flies (Bown, 1988).

Not all brood-site mimicking flowers have, however, evolved atrap to detain pollinators as, e.g., in Ceropegia (Heiduk et al.,2010; Ollerton et al., 2009). In the closely related genus Stapelia, in-sects land freely in the bright and translucently purplish petal, of-ten several times before accomplishing pollination (Meve andLiede, 1994). The latter, conversely to, e.g., Arum (though withsome exceptions), have a prolonged odor production and floweringtime that can last for over a week, and it is thus not of essence toget pollinated within a very short time-window.

Fig. 1. (A) Longitudinal section of A. pictum inflorescences displaying the trap chamber dpollinators towards the reproductive organs, are clearly visible: white in the chamber anthe ring of sterile flowers. The light emerging from the chamber due to the lack of pigmflowering when sterile flowers already have dehydrated, pollen has been released and i

2.3. Modalities of attraction

2.3.1. Olfactory signalingBrood-site deceptive systems rely mainly on olfactory signals as

the primary modality of pollinator attraction. The deceptive plantsthus dupe insects, which to a very large extent are smell-driven.The imitation of the oviposition substrate is achieved primarilythrough false odor cues targeting mainly gravid females; howevermales seeking for mating opportunities might also be attracted andact as pollinators, potentially being rewarded with sexually-mature females (Renner, 2006).

The imitated oviposition substrates fall into four classes: (i)dung and urine (Diaz and Kite, 2002; Kite, 1995; Quilichini et al.,2010); (ii) carrion and rotten flesh (Borg Karlson et al., 1994;Stensmyr et al., 2002); (iii) fermenting fruits and yeast (Goodrichand Raguso, 2009; Stökl et al., 2010) and (iv) fungi (Kaiser, 2006).The floral odors are, in general, produced by fragrance-emittingglands called osmophores localized in the limb (Aristolochia) orin the sterile part of the flower (Araceae). At anthesis, with therelease of the volatiles, the osmophores’ starch reserves becomecompletely depleted, indicating that considerable metabolic en-ergy is required during odor production and emission (Hadacekand Weber, 2002).

Carrion/dung insects duped by flowers simulating an oviposi-tion substrate, to which insects are innately attracted, have evenbeen observed ovipositing in the flower, e.g., in Stapelia (Jürgenset al., 2006) and Helicodiceros (Stensmyr et al 2002). This ishowever not the behavior usually observed. In fact, ovipositionnormally requires an interplay between olfactory, taste andmechanosensory input to be released. This releasing combinationof signals is, in most instances, missing in the flower.

2.3.2. Visual signalingVisual signals play also an important role in the attraction of

pollinators and dung and (particularly) carrion blossoms, displaythe largest inflorescences found on earth (up to 3 m in heightand 40 cm in diameter (Burgess et al., 2004; Meve and Liede,1994)) and the highest rate of floral size increase per million year(Barkman et al., 2008). The floral gigantism associated with theseflowers has been suggested to have been selectively advantageous,as the size of the odor-producing organs and the amount of pro-duced odor are positively correlated (Valdivia and Niemeyer,2006) resulting in a more efficient long distance pollinator attrac-tion. Moreover, the ‘‘carrion model’’ would be mimicked more effi-ciently by larger blossoms, as larger carcasses represent a preferredsubstrate for insects seeking for an egg-laying substrate (larvaewill have a better chance to survive) (Ives, 1991). The large floralplatforms (petals or modified leaves) have dull floral color (dark/

uring the first day of flowering. The characteristic doubled-colored walls, that guided dark red in the upper part. (B) Top view of the entrance to the chamber displayingentation in the walls is clearly visible. (C) The inflorescences on the second day of

nsects are free to leave the chamber.

1658 I. Urru et al. / Phytochemistry 72 (2011) 1655–1666

brown-purple), often checkered with dark spots or filiformappendages, trichomes or hairy structures, closely resembling adead animal (Raguso, 2004).

A clear-cut contrast between dark-opaque (entrance to the trap)and bright-translucent (floral chamber) areas, due to a lack of pig-mentation in the walls around the reproductive organs, is often ob-served in the trap-blossoms species. Thus, the light entering fromthe sides guides insects towards the sexual organs (Endress,1995; Van der Pijl, 1953; Yeo, 1972). Bi-colored floral chamberwalls have often been observed in members of the genus Arum(Gibernau et al., 2004) and are clearly displayed by, e.g., Arumpictum: dark-red in its upper part and white in the chamber(Fig. 1A). Dormer (1960) showed that the flight-activity of insectsinside a cylinder with opaque/translucent walls is deactivated untila certain volume. With a very simple experimental design, hereproduced the floral trap of Arum nigrum using a glass tube witha central bar and introduced a number of insects. As long as the in-sects were calm, they distributed themselves uniformly. However,when exposed to a stress condition, e.g., shaking or over-crowdingthe tube (as in the floral chamber of A. nigrum) they became posi-tively phototactic. Such a behavior would indeed lead insects to thebright reproductive parts of some deceptive flowers.

2.3.3. Heat and carbon dioxideAll flowering plants have a metabolic biochemical activity, and

heat represents a by-product of this process (Seymour and Schu-ltze Motel, 1997). Normally the heat dissipates, as the metabolicreaction is very slow. However, in many brood-site mimickingflowers heat is produced trough an alternative mitochondrialrespiratory pathway that involves a cyanide-resistant alternativeoxidase (Thien et al., 2000; Wagner et al., 2008). The process isnot confined to brood-deceptive systems, but has been encoun-tered in eleven families of extant angiosperms (Thien et al.,2009) and in cycads (Skubatz et al., 1993; Tang, 1987). The functionof the thermogeny has, however, only been investigated exten-sively in the Araceae family. Thermogenic inflorescences can heatup to 30–46 �C, e.g., in Arum dioscoridis and Philodendron selloum(Gottsberger and Silberbauergottsberger, 1991; Skubatz et al.,1990) and the phenomenon is directly linked to the size of theappendix (Gibernau et al., 2005; Seymour, 2010). Some speciescan also thermoregulate their inflorescences and thus maintain acertain temperature independently of that of ambient tempera-tures, e.g., �39.5 �C in Philodendron melinonii (Seymour and Giber-nau, 2008). The heating up of the distal (sterile) portion of thespadix, is closely tied to the emission of the vile odor that occursshortly before or at anthesis, e.g., in A. concinnatum (Urru et al.,2010). Male flowers can also exhibit a thermogenic phase duringthe first or second night of the anthesis (Skubatz et al., 1991),e.g., in A. maculatum a triphasic thermogeny could be observed(Bermadinger-Stabentheiner and Stabentheiner, 1995).

Floral heat is involved in many steps of the flower developmentduring anthesis (Bermadinger-Stabentheiner and Stabentheiner,1995) and has recently been studied for its ecological relevance.Heat has been shown to provide an energy reward for pollinators(Dieringer et al., 1999; Seymour et al., 2003), to increase volatiliza-tion of chemicals and the diffusion rate of CO2 (Grant et al., 2008),and to fine-tune the mimicry of mammalian feces and carrion byguiding insects into the trap (Angioy et al., 2004; Uemura et al.,1993).

Carbon dioxide represents a metabolic by-product of the in-tense respiratory process that occurs during anthesis. Mass-specific rates of CO2 production in the appendix have beencalculated for some aroid species and are the highest recorded inthe plant kingdom (Seymour et al., 2009; Wagner et al., 2008). Car-bon dioxide produced along the appendix tends to concentrate atthe bottom of the floral chamber (due to its chemical–physical

properties), where the insects often are gathered. As suggested(Dafni, 1984), high levels of CO2 could thus act as an anestheticand, in addition to the morphological-optic features of the cham-ber, delay the departure of the pollen vectors. In the parasiticnon-trap flower Rafflesia tuan-mudae, flies have been observed toremain inside the bud as a result of the possible anesthetic effectof the CO2 (Patino et al., 2002). So far, this hypothesis has not beentested. However, high levels of CO2 are also emitted by horse dungand has been shown to be a strong oviposition stimulant for thestable fly Stomoxys calcitrans (Jeanbourquin and Guerin, 2007a),and could thus have a directly attracting effect on potentialpollinators.

3. Different types of brood-site mimicry

3.1. Brood-site-mimicking chemistry: carrion odors

This kind of mimicry is strongly signified by the presence of dis-tinct oligosulfides (dimethyl mono-, di and trisulfides). However,other compounds can be found in these bouquets, (often at lowerabundance) such as monoterpens, long chain organic acid andbenzenoids (Borg Karlson et al., 1994; Burger et al., 1988; Kiteand Hetterschieid, 1997). These sulfur compounds, typical of sapr-omyophilous flowers, are otherwise not common among floweringplants. The only other example is unrelated, New World tropics,bat-pollinated flowers, where these compounds are thought tohave been key-compounds in the co-evolution of bats and bat-flowers (Bestmann et al., 1997; Kaiser and Tollsten, 1995; Knudsenand Tollsten, 1995; von Helversen et al., 2000). The oligosulfideshave also been identified in the fruit bodies of fungi of the genusPhallus and in the Splanchnaceae dung mosses family (Borg Karlsonet al., 1994; Marino et al., 2009).

These substances have been shown to be crucial cues for blow-flies (Calliphora and Lucilia), as they are used as key odors to locatecarrion resources (Stensmyr et al., 2002; see below). They elicit in-nate behavioral responses and it is likely that the blowflies cannotafford to ignore these signals as they signify a totally vital resourceto the female fly (Borg Karlson et al., 1994; Stensmyr et al., 2002).Dimethyl trisulfide, a by-product of methionine degradation is awidespread attractant for ovipositing carrion insects (Jeanbourquinand Guerin, 2007b). Among arums sensu stricto the distinctivesulfur-containing compounds characteristic of many other speciesacross the Araceae family (Bolin et al., 2009; Burger et al., 1988;Stensmyr et al., 2002; Stransky and Valterova, 1999) are, however,not found, and carrion mimicry, signified by the oligosulfides, isthus not present.

Across the plant and fungus kingdoms the universality of thedeceptive carrion signal is striking. If sulfide compounds are con-sidered as key compounds attracting carrion flies, then a similarpool of pollinators across species that produce the same com-pounds should be expected. This is true for several genera, e.g.,Amorphophallus, Stapelia, Hydrosome, Hydnora and Helicodicerosspecies, spanning across three families. In each of the above men-tioned genera there is at least one representative species of the car-rion mimicry emitting sulfide compounds and being pollinated bylarge carrion flies and beetles (e.g., Muscidae, Sarcophagidae, Calli-phoridae, Dermestidae and Histeridae) (Bolin et al., 2009; Jürgenset al., 2006; Stensmyr et al., 2002; Stransky and Valterova, 1999).There are, however, still too few comparative studies investigatingthe floral odor vs. pollinating fauna to allow a complete generaliza-tion and any conclusion would be strongly biased.

The ecological relevance of sulfur-containing compounds forcertain groups of insects is, however, obvious. Carrion flies displaybreeding preferences clearly based on the presence of these odors.Larvae of carrion flies do not develop in herbivorous feces probably

I. Urru et al. / Phytochemistry 72 (2011) 1655–1666 1659

due to the low/absent protein content (Banziger and Pape, 2004),which is also reflected in the absence of sulfur-containing com-pounds in the volatile emission. Recently, flowers of closely relatedEucomics (E. autumnalis and E. comosa, Hyacinthaceae) were chem-ically manipulated. Some species have specialized wasp- and oth-ers carrion-fly-deceptive flowers. Although morphologically verysimilar, the latter type differs in the chemistry of the floral scentby emitting di- and trimethyl oligosulfides in the headspace. Inan elegant experiment, (Shuttleworth and Johnson, 2010) showedthat the addition of sulfur compounds to the wasp-pollinated spe-cies was sufficient to induce a clear shift to carrion fly-pollination.These findings illustrate the importance of the oligosulfides as car-rion cues more specifically, and of flower odor changes in pollina-tor shifts in general.

3.1.1. An example of carrion mimicry: the dead horse arumThe dead horse arum, Helicodiceros muscivorus is a highly con-

spicuous and foul smelling flower that occurs on small islands inthe Mediterranean area. The plant almost always occurs in closeproximity to large gull colonies, and flowers just before the chickshatch. At this time large populations of carrion flies or blowflies arepresent. In combined chemical and electrophysiological investiga-tions we could show that the flower mimics the smell of rottingflesh, attracting these flies as involuntary pollinators by producingthe typical three carcass-mimicking oligosulfides mentionedabove: dimethyl mono-, di- and trisulfide. In a direct electrophys-iological comparison it was clear that the fly nose, the antenna, re-sponds identically to the odors of the flower and of rotten flesh(Fig. 2B). In addition to the odor cues, the flower produces heatup to 15 �C above ambient temperature, thus mimicking the heatproduced in a rotting carcass. The flower is open only for 2 days,and produces odor and heat only during the first of these. This factprovided the opportunity to test the attractiveness of the sensory

O

O

O

acetoin acetate

OH

O

O

2,3 butanediol acetate

O

O

ethyl hexanoate

HO

phenylethyl alcohol

O

O

O

O

hexyl acetate phenethyl acetate

=

A

Fig. 2. Examples of carrion and yeast mimicry Arum species. (A) The Solomon’s lily and toviposition-feeding substrate, a fermenting apple. (B) The dead horse arum and its keyanimal that has already been infested by blowflies. Larvae are already developing. Phot

cues present in the flower. During day two (when the flower nor-mally is scentless and attracts no flies) we first added syntheticodor, and could show that flies were attracted to the same extentas during day one. They did, however, not enter the flower trapchamber. However, when we added heat to the central appendixof the flower, the flies also entered into the trap mechanism. Thedead horse arum is thus using a multi-sensory deception to attractflesh-eating flies. Beyond odor and heat the flower also usesmechanosensory and visual cues to further enhance the attractivity(Angioy et al., 2004; Stensmyr et al., 2002).

A system such as the dead horse arum is an excellent examplehow such a system depends on a perfect mimicry of an irresistibleresource. Female flies just cannot afford to ignore an optimal ovi-position substrate. At the same time the plant exerts a minimumof pressure on the flies to evolve counter measures by using a verylimited window in time (a few weeks) and in space (small islandsin the Mediterranean) for its deceptive action.

3.2. Brood-site-mimicking chemistry: fecal and urine odors

Like the mimicry of carrion, the strategy to copy the smell offeces and urine appears to have evolved many times. However, flo-ral carrion/fecal fragrances may not only have evolved in order todeceive involuntary pollinators, but could initially have evolvedas a defense against herbivores (Lev-Yadun et al., 2009; Pellmyrand Thien, 1986). In support of this view, there is evidence thatmammalian herbivores avoid dung-infested substrates to avoidthe potential risk of parasitism (Lev-Yadun et al., 2009). For exam-ple, reindeer avoid pastures with a high density of dung to mini-mize the risk of gastrointestinal nematode infections (van derWal et al., 2000).

The typical smell of dung is characterized by phenol and indolederivates, such as m- and p-cresol, skatole and 2-heptanone (Kite,

dimethyl disulfideS

S SS

S

S

dimethyl monosulfide

dimethyl trisulfide

B

=he key compounds used to attract Drosophila spp. Beside, an example of a preferredattractive compounds: hydrogen mono-, di and trisulfide. Beside the model, a deados by S. Spano (H. muscivorus) and J. Stökl (A. palaestinum).

1660 I. Urru et al. / Phytochemistry 72 (2011) 1655–1666

1995; Yasuhara et al., 1984). To a certain extent it is possible tochemically categorize the smell of different types of dung. Forexample, the headspace profile of horse dung is dominated bymonoterpenes (such as limonene and p-mentha-1(7),8-diene)and sesquiterpenes (e.g., b-caryophyllene and a-humulene), whilethe typical dung compounds (e.g., nonanal, decanal and p- andm-cresol) are less abundant (Johnson and Jürgens, 2010). Cow dungcontains p-cresol, nonanal, decanal and hydrocarbons (Kite, 1995).In carnivore feces, such as in the dog, phenol dominates the head-space (Johnson and Jürgens, 2010). Thus, although the encounteredoverlap of the qualitative chemical composition of different typesof dung, the relative abundance of chemicals can vary significantly.The emission of fecal odors to exploit pollinators has been reportedfrom several plant taxa. For example, the dung smell of, e.g., Apter-anthes joannis, Monolluma hexagona and Orbea semota can mainlybe ascribed to the presence of p-cresol and several other minorcompounds (Jürgens et al., 2006); in other species, such as in Duva-lia corderoyi, phenol is the main compound (Jürgens et al., 2006).The floral headspace of Aristolochia cymbifera contains high relativeamounts of aromatic esters (e.g., benzyl propionate, benzyl but-anoate and benzyl pentanoate), p-cresol and indole. However di-methyl di- and trisulfide are also present as minor volatile in theodor profile (Johnson and Jürgens, 2010). Thus, the separation offecal and carrion mimicry in two groups is not always as strict asthe categorization of dung in different types.

High contents of acids (e.g., acetic acid, benzoic acid, phenylace-tic acid, 3-phenylpropanoic acid, octanoic and hexanoic acid) areoften found in urine (Yasuhara et al., 1984). Thus, as suggestedby Jürgens et al. (2006), deceptive flowers with high levels of thesechemicals should subtend a urine-mimicry, as, for example, in var-ious genera of the Apocynaceae family, e.g., Orbea, Echidnopsis andDesmidorchia. However, further investigations are needed to estab-lish whether this type of mimicry is represented also in membersof the other brood-site mimicry families.

3.2.1. A complex of waste product mimicry: Mediterranean Arum liliesArum is one of the Palaearctic genera of the worldwide-

distributed Araceae family, which radiated during the Cretaceous(Grayum, 1990). Modern investigations of this genus start withBoyce and his magnum opus ‘‘The genus Arum’’ published in1993, an impressive book that covers many aspects of the taxon-omy and biology of the genus. In 2004, a revision of Arum pollina-tion biology appeared (Gibernau et al., 2004). According to thelatest classification (Boyce, 2006) the genus is divided into thesubgenus Gymnomesium with a single representative (A. pictumendemic to Balearic Islands, Corsica, Sardinia, West Central Italy),and the subgenus Arum, which includes the sections Arum andDioscoridea, the latter being further divided into six subsections.The 28 species (Boyce, 2006) of the genus are mainly distributedaround the Mediterranean basin, but some species are found inmiddle and northern Europe, the Middle East and Central Asia(Boyce, 2006; Lobin et al., 2007).

Three species emit to the human nose scentless flower odors(Arum rupicola, Arum korolkowii and Arum jacquemontii). For eightspecies no data is available, and we can thus not predict whichtype of pollination system they have evolved.

The imitation of an oviposition substrate is, however, the mosttypical modality of deception displayed by the genus (Linz et al.,2010) and has been verified in 11 species: A. pictum, Arum concinn-atum, Arum italicum, Arum nigrum, Arum maculatum, Arum dioscori-dis, Arum cyrenaicum, Arum apulum, Arum purpureospathum, Arumcylindraceum and Arum palaestinum. Ten of these flowers smell likedung and accordingly attract dung beetles and flies (Drummondand Boorman, 2003; Drummond and Hammond, 1993; Gibernauet al., 2004). One species, A. palaestinum, which has a more fru-ity-yeasty odor, instead attracts drosophilid flies (Stökl et al.,

2010). Three additional species have been indicated to emitdung-like odors: Arum byzantinum, Arum elongatum and Arum ori-entale, with the latter reported to have a second chemotype smell-ing as fermenting fruit akin to A. palaestinum. However, since nodata is available, neither regarding pollinators nor on scent, fromthese species, they will be excluded from further discussion. Thepollination biology of several Arum species has been described ingeneral terms (Braverman and Koach, 1982; Drummond andHammond, 1993; Koach and Feinbrun-Dothan, 1986; Lack andDiaz, 1991; Ollerton and Diaz, 1999), and for some brood-sitemimicking species in quite some detail (Lack and Diaz, 1991;Quilichini et al., 2010; Stökl et al., 2010; Urru et al., 2010). Belowwe provide a review of the present state of knowledge regardingthese brood-site mimicking species. Within the 14 remaining spe-cies, two species are characterized by a sweet-floral odor (Arumidaeum and Arum creticum) and have most likely evolved from anon-rewarding to a rewarding pollination system (Diaz and Kite,2006).

3.2.2. Volatile chemistry of Arum liliesSince the advent of mass spectrometry in combination with

non-invasive headspace sampling techniques, the floral odors ofseveral Arum species have been analyzed. Such detailed analyseshave provided us with the possibility to compare the odor compo-nents produced in the different species.

The fruit-yeast smelling species (A. palaestinum) will be dis-cussed in a separated section below. In headspace analyses of theremaining 10 species, p-cresol, the dung-associated compoundpar excellence, found, e.g., in cow, (Kite, 1995), horse (Johnson andJürgens, 2010), cattle, wild boar and sheep dung (Dormont et al.,2010), is present in all species except A. cylindraceum and A. pictum.Among the p-cresol-containing species, this compound representsone of the main constituents in two species (A. dioscoridis and A.apulum), while otherwise being present as a minor component.

3.2.2.1. Alkene-producers. Beside p-cresol, present in all species ex-cept in A. pictum and A. cylindraceum, different aliphatic alkenes(e.g., 1-decene, dimethyloctadiene) are the main compounds inthe emissions of A. italicum, A. dioscoridis, A. nigrum, A. purpureo-spathum and A. apulum. In A. italicum methyl butyrate and ethanolare as abundant as the alkenes. Methyl 2-methylbutyrate, the estermethyl isobutyrate and two ketones (3-methyl-2-butanone and 2-heptanone) are present as minor compounds. In the others alkene-producering species ethanol together with 2-heptanone is a minorcompound (Table 1 and Fig. 3).

3.2.2.2. Non-alkene producers. In the remaining five non-alkene-pro-ducing species, terpenes (i.e., 3,7-dimethyl-1-octene, 2,7-dimethyl-1,7-octadiene and 3,7-dimethyl-1,6-octadiene) dominate theheadspace almost completely in A. cyrenaicum and A. concinnatum,with minor compounds being 5-hepten-6-methyl-2-one (A. cyrena-icum) and 2-heptanone (A. concinnatum). In A. cylindraceum, A. pic-tum and A. maculatum the main compounds produced are decanal,nonanal and isopropyl laurate (A. cylindraceum), 2-heptanone andindole (A. maculatum), and ocimene and dehydrocimene (A. pictum).In the latter two species nitrogen compounds (skatole and indole)and several mono-and sesquiterpenes (b-pinene, a-pinene, limo-nene, camphene, sabinene and d-cadinene) are present as minorcomponents. In A. cylindraceum, nonanal, decanal and isopropyllaurate dominate the headspace completely (Table 1 and Fig. 3).

3.2.2.3. Odor-production in a phylogenetic perspective. We can hencedistinguish two main groups: (i) species with aliphatic alkenes:A. italicum, A. dioscoridis, A. nigrum, A. purpureospathum andA. apulum, and (ii) species with no aliphatic alkenes, but with othercompounds as main components: A. cyrenaicum, A. concinnatum, A.

Table 1Main compounds identified in the headspace of the 10 brood-site deceptive Arum species using waste product mimicry, plotted in the Arum phylogenetic tree. The size of thecircles represents the relative abundance of odor components. The two main groups (alkene and non-alkene producers) are color coded: turquoise alkene-producers (A.dioscoridis, A. nigrum, A. apulum, A. italicum and A. pupureospathum); light-orange nonalkene-producers (A. cyrenaicum, A. concinnatum, A. maculatum, A. pictum and A.cylindraceum).

= 10–90%.= 2–10%.

= <2%.

I. Urru et al. / Phytochemistry 72 (2011) 1655–1666 1661

1-decene

dimethyloctadiene

ocimene

O

HN

indole

2-heptanone

OH

p-cresol

3,7-dimethyl-1-octene

3,7-dimethyl-1,6-octadiene

2,7-dimethyl-1,7-octadiene

O

O

O

O

decanal

nonanal

isopropyl laurate

A. concinnatum A. cyrenaicumA. pictum

A. cylindraceum

AB

E

A. maculatum

C D

A. dioscoridis

Fig. 3. Flowers of brood-site deceptive Arum species grouped according to their characteristic main headspace compounds. (A, B, C and E) Non-alkene-producers: (A.cyrenaicum, A. concinnatum, A. pictum, A. maculatum and A. cylindraceum). (D) Alkene-producer (one example): A. dioscoridis. All photographs by I. Urru except A. pictum (M.C.Stensmyr) and A. maculatum (T. Krügel).

1662 I. Urru et al. / Phytochemistry 72 (2011) 1655–1666

maculatum, A. cylindraceum and A. pictum. Within the first group,three subgroups can be discerned: (i.a.) aliphatic alkenes + p-cresoldominate (A. dioscoridis and A. apulum); (i.b.) aliphatic alkenes +ethanol + methyl butyrate dominate (A. italicum); (i.c.) aliphaticalkenes + diverse odors make up the main part of the flower odor(A. nigrum and A. purpureospathum).

Among the non-alkene-producing species, the distinctive odorprofile of A. pictum (ocimene as main component) is reflected alsoin a morphological and phylogenetic perspective. This species (en-demic to Sardinia, Corsica and the Balearic Islands, and the onlyArum flowering in the autumn) forms the (basal) subgenus (Gym-nomesium) and is accordingly distinct from all the other Arumbrood-site-mimicking species that are placed in the subgenusArum (Espindola et al., 2010; Linz et al., 2010). A distinctive odorprofile is also displayed by the two species A. concinnatum and A.cyrenaicum. The odor-based similarity of these two species isreflected from a morphological–phenological point of view,however not supported in a phylogenetic perspective. Thus, both

groups (alkene and non-alkene) are represented in both basaland derived species, indicating an ecologically and pollinator con-strained adaptation (Table 1).

3.2.3. Arum visitors and pollinatorsThe diverse chemical features mentioned above have probably

evolved to exploit different types of pollinators. Here we providean overview over which kinds of pollinators have been observed inthe flowers displaying different types of odor emissions (Table 2).

3.2.3.1. Alkene-producers. Sphaeroceridae flies represent the maingroup of pollinators in A. purpureospathum and A. apulum. Minorgroups are represented by Chironomidae (in both species) andPsychodidae flies in A. purpureospathum (Drummond andHammond, 1993; Gibernau et al., 2004). In A. nigrum and A. diosco-ridis, Sphaeroceridae flies and Staphilinidae beetles are the mainpollinators (Drummond and Hammond, 1991; Gibernau et al.,2004). The floral fragrance emitted by the spadix of A. italicum

Table 2List of pollinator taxa that have been found in the floral chamber of Arum species. Nodata is available for pollinators of A. cylindraceaum.

Plant species Insect visitors References

A. dioscoridis Sphaeroceridae Drummond andHammond (1991)Staphilinidae

A. nigrum Sphaeroceridae Drummond andHammond 1991Staphilinidae

A. purpureospathum Sphaeroceridae Drummond andHammond (1993)Psychodidae

Chironomidae

A. apulum Sphaeroceridae Gibernau et al.(2004)Chironomidae

A. italicum Psychodidae Albre et al. (2003)ChironomidaeSciaridae

A. concinnatum Sphaeroceridae Urru et al. (2010)SciaridaeCeratopogonidaePsychodidaeDrosophilidaeChironomidaeAgromyzidaeHeleomyzidaeEphydridaePhoridaeCecidomyiidaeStaphilinidae

A. cyrenaicum Sciaridae Urru et al. (2010)SphaeroceridaePsychodidaeStaphilinidaeChironomidaeDrosophilidaeAgromyzidaeHeleomyzidaeEphydridaePhoridaeCecidomyiidae

A. pictum Sphaeroceridae (Coproicaand Spelobia spp.)

Quilichini et al.(2010)

StaphilinidaeBraconidaeSciaridaeScatophagidae

A. maculatum Psychodidae (Psychodaphalaenoides)

Albre et al. (2003)

I. Urru et al. / Phytochemistry 72 (2011) 1655–1666 1663

attracts four different families: Psychodidae Sciaridae, Chironomi-dae and Sphaeroceridae at similar proportions (Albre et al. 2003).Within the alkene-producing species A. italicum is the one attract-ing the broadest spectrum of pollinators.

3.2.3.2. Non-alkenes-producers. Within the non-alkene producers,three species (A. cyrenaicum, A. concinnatum and A. pictum) areattracting the most diverse entomofauna (Quilichini et al., 2010;Urru et al., 2010). In A. cyrenaicum and A. concinnatum more thaneleven diptera families, e.g., Sphaeroceridae, Drosophilidae andCecidomyidae, have been recorded in the floral chamber (Urruet al., 2010). Similarly to the alkene-producer A. italicum, A. macul-atum is pollinated by Psychodidae flies, but in contrast to A. itali-cum by only one specific species, namely Psychoda phalaenoides(Psychodidae) (Albre et al., 2003). In the third non-alkene pro-ducer, A. pictum, the most abundant visitors are Sphaeroceridaeflies (Coproica hirticula, Coproica ferruginata and Spelobia bifrons),with a strong bias towards females. However Staphilinidae beetles,and Sciaridae and Scatophagidae flies have also been found in floralchambers of A. pictum (Quilichini et al., 2010). To date, there is nodata available on the pollinators of the fifth non-alkene producer,A. cylindraceum.

3.2.3.3. Pollinators vs. chemistry. Whereas Psychoda phalaenoidesrepresent the specific pollinator of A. maculatum, A. italicum (thatalso attracts Psychodidae flies) appears to be more generalistic,attracting a more diverse entomofauna (Kite et al., 1998; Lackand Diaz, 1991). The main compounds found in the headspace ofA. maculatum are not represented in large amounts in the fragranceof A. italicum, which instead appears to be dominated by ethanol,dimethyloctadiene and methyl butyrate and thus could explainthe less specific attraction observed in A. italicum. However theblend of compounds emitted by A. italicum still maintain thesex-specific properties, i.e., both A. italicum and A. maculatumattract almost exclusively females. Three of the main componentspresent in the headspace of A. maculatum (i.e., p-cresol, indole and2-heptanone) are present in the headspace of cow dung, which isthe preferred oviposition substrate of Psychoda flies (Kite, 1995;Kite et al., 1998). Field attraction experiments showed the attrac-tion of Psychoda species to traps baited with p-cresol, 2-hepta-none, indole, or any combination thereof. p-Cresol tested aloneshowed the highest singular attractiveness, while a blend of thethree compounds was shown to be more active than any singlecompound (Kite et al., 1998). Since p-cresol is present in the head-space of most brood-mimicking arum species, it has been hypoth-esized that this molecule represents an attractant for Psychodidaeflies and more in general for dung insects (Kite et al., 1998).

Based on the visitors/pollinators we can divide the Arum intothree distinct groups: (i) species attracting Psychodidae flies (A.maculatum and A. italicum), (ii) species attracting Sphaeroceridaeflies and Staphilinidae beetles (A. pictum, A. dioscoridis, A. purpureo-spathum, A. nigrum and A. apulum) and (iii) species with variousdiptera as pollinators (A. concinnatum and A. cyrenaicum). The pol-linator groups do however not strictly follow the chemical group-ing. The non-alkene producers (A. maculatum and A. pictum) arepollinated by two different taxa, Psychodidae and Sphaeroceridaerespectively; A. concinnatum and A. cyrenaicum are visited by abroader range of dipterans, although they include both Psychodi-dae and Sphaeroceridae. Among the alkene-producers, the pre-dominant pollinators are in common to all species, except A.italicum, and are found among Sphaeroceridae flies and Staphilini-dae beetles. Both the adult and larvae of Sphaeroceridae flies live(mostly) in dung, with some genus clearly displaying preferencesfor certain types of feces (e.g., carnivores vs. herbivores), and incarrion in which the larval stages are developing (Buck, 1997;Laurence, 1955). Staphilinidae beetles (or rove beetles), thoughbeing dung-associated insects, do not feed/breed on dung. Insteadthey are predators’ of small dung diptera, which they ambush ondung by tracking the olfactory cues used by its prey to locate theirfood or breeding substrate (Forsyth and Alcock, 1990). However(for both groups), there are no studies that have investigated theattractiveness or physiological activity of synthetics compoundsidentified in the headspace of different types of dung. Thus, it stillremains unknown which compounds are key elements in theattraction of Sphaeroceridae and Staphilinidae to the arums, par-ticularly whether the aliphatic alkenes (that dominates the profileof several arum species) play an important role. At this state ofknowledge it is thus impossible to determine the specific ‘‘dungmodel’’ in the arum species.

However, it is clear that plants predominantly producing a cer-tain group of chemicals do not specifically and exclusively attractinsects from the same families.

3.3. Brood-site mimicking chemistry: fermentation odors

A recently discovered type of potential brood-site mimicry isrepresented by one of the Mediterranean arums, A. palaestinum.The odors identified in the flowers mimic a substrate that canfunction both as adult food and as a brood-site, so the correct

1664 I. Urru et al. / Phytochemistry 72 (2011) 1655–1666

nomination would be food/brood-site mimicry. As only one speciesdisplaying this syndrome is known, the description of this examplewill serve as the complete background.

3.3.1. An example of fermenting fruit mimicry: the Solomon’s lilyThe Solomon’s lily, A. palaestinum is found in northern Israel and

southern Lebanon. In field investigations it was observed that theflowers of this species attract large numbers of drosophilid flies.One flower could during a few hours attract up to 500 flies. Tothe human nose the odor of the flower resembles wine. Amongthe odor components we found 3-hydroxybutan-2-yl acetate and3-oxobutan-2-yl acetate, both extremely rare in flower odors, butfrequently reported as fermentation products. In addition the flow-er produced a bouquet of known Drosophila attractants: ethyl hex-anoate, hexyl acetate, 2-phenylethyl alcohol and 2-phenethylacetate being the most active components on the fly antenna. Incontinued investigations it became clear that the lily is indeedmimicking a fermentation process by producing a bouquet of theseimportant components. In laboratory attraction assays it wasshown that a mixture of these components competed very wellwith naturally highly attractive substrates like, e.g., rotting banana(Stökl et al., 2010) (Fig. 2A).

The A. palaestinum pollination syndrome is thus another exam-ple of how evolution has shaped an irresistible stimulus, with theflower providing the exact sensory cues needed for optimalattraction.

4. Concluding remarks

Evolution has shaped amazingly complicated systems aimed atfilling the senses of the duped insect to such an extent that, in themind of the dupe, the mimic ‘‘is’’ the model. That this has suc-ceeded in many cases manifests itself in the fact that the deceptivesystems indeed seem to be stable strategies. For a deceptive sys-tems to be stable, the energetic or fitness costs to pollinators whenthey visit rewardless flowers must be balanced by rewards ob-tained from other sources (Renner, 2006). Carrion/dung flowersare (1) found (often) either confined in small populations or inscattered specimens (e.g., Stapelia) with a prolonged odor/attrac-tion (more then 1 week), or (2) occur in a bigger populations witha very short time-window (less then 24 h) of odor production andthus attraction (e.g., Helicodiceros). Thus the energy losses encoun-tered by pollinators by being duped and (in some instances) layingeggs on the wrong substrate are balanced by the low probability ofencounting these cheating systems in comparison to the naturalresource (Roy and Raguso, 1997). At the same time we observehigh degrees of dynamics, where the deceiving flowers seem tobe undergoing fast and constant evolution. We are thus dealingwith a system characterized by both present perfection and evolu-tionary readiness. This combination is very likely what is needed toremain a successful deceiver.

Although plants exploiting brood-site mimicry for pollinationshow a strong diversity in shape, structure, color and emitted odor,the underlying mechanism necessary to deceive the intended tar-gets into pollination thus remains the same, namely to be irresist-ible. More often than not, this means producing an irresistiblesmell. Of the brood-site deceptive systems discussed here the odormimicry appears to be of main importance; in line with the criticalrole olfaction plays in the life of most insects. Although the odorsdiffer between different strategies, the fundamental principle bywhich these odors interact with the deceived insects remains sim-ilar, irrespective of insect species. The emitted odors of the plantsare detected by critically important odorant receptors, the trigger-ing of which induce activity in neuronal circuits mediating innateand obligate attraction. Olfaction is, however, not always sufficient.

Another striking feature of the deceptive systems is how differentsensory cues during evolutionary time have been tuned to enhanceeach other’s attractivity. The dead horse arum will, e.g., not accom-plish its deception without the interplay of several sensory cues.The ‘‘co-evolution’’ of unrelatedly produced cues is a highly inter-esting question that calls for further study. There are naturallymany more questions left unanswered with respect to brood-sitemimicry systems. For example, how are the volatiles emitted bythe plants produced, are these de novo generated by the plants,or produced by microbes residing within the plants? How preciseor un-precise is the mimicry in these systems? Do, e.g., dung-mimicking plants copy the fecal smell of certain species, or do theyalways reproduce a general dung smell? What influence has colorand shape to the success of the deception? In addition, there arecertainly more brood deceptive systems, with strategies fallingoutside those outlined here left to be discovered and explored. Po-tential novelties are likely found in, e.g., Orchidaceae. The orchidsof South and Central American are an extremely diverse group, interms of species numbers but also with respect to colors, shapesand smells. Although the pollination mechanisms of several spe-cies have been studied, the deceptive systems of most still remainto be investigated (see, e.g., Borba and Semir, 2001; Damon et al.,2002). Given that these diverse groups of orchids grow in an envi-ronment housing an extraordinary diversity of insects, the condi-tions for novel peculiar deceptive pollination syndromes to haveevolved is naturally favorable. In short, the future will certainly re-veal new, striking and surprising examples of plant trickery andevolutionary ‘‘ingenuity’’, extending our list of mimicked oviposi-tion substrates.

Acknowledgement

The writing of this review was funded by the Max-PlanckSociety.

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Isabella Urru received her master’s degree in Biologywith Chemical Ecology as major subject at the Univer-sity of Cagliari (Italy), in collaboration with the Uni-versity of Lund (Sweden), where she spent one year.During her Ph.D. at the University of Cagliari herresearch focused on the pollination system of theendemic Helicodiceros muscivorus (Araceae) and thephysiology of the olfactory system of Protophormiaterranovae in this plant–insect interaction. After herPh.D. she moved to Germany and joined the Departmentof Evolutionary Neuroethology at the Max Plank Insti-tute for Chemical Ecology as a PostDoc and focused her

research on the pollination systems of the Mediterranean genus Arum by combiningmolecular, chemical and electrophysiological methods. Her general researchinterest is on pollination systems built on deception, particularly the chemosensory

cues involved in this complex plant–insect interaction.

M.C. Stensmyr obtained his degree in ecology at LundUniversity. He did his Ph.D. in the group of Bill S.Hansson at the Swedish University of Agricultural Sci-ences (SLU), in Alnarp, followed by a postdoc with PeterMombaerts at the Rockefeller University, New York.He’s interested in how olfactory systems evolve andadapt, and particularly so in drosophilid flies.

Bill Hansson defended his Ph.D. in animal ecology atLund University, Sweden in 1988. After an 18 monthpostdoc period at the University of Arizona he took upan assistant professorship in Lund, where he alsobecame associate (1992) and full (2000) professor. In2001, he was offered a full professorship at the SwedishUniversity of Agricultural Sciences at Alnarp and wasinstalled as head of the division of chemical ecology.Between 2003 and 2006 he was also associate dean inAlnarp. In 2006 Hansson was recruited as Director to theGerman Max Planck Society, where he presently headsthe department of evolutionary neuroethology at the

Max Planck Institute for Chemical Ecology in Jena. Since 2011 he is also managingdirector of the institute. He is a member of the Royal Swedish Academy of Sciences,the Royal Swedish Academy of Agriculture and Forestry and of the Saxonian

Academy of Sciences.