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Keywords:

  • basal angiosperm;
  • floral odour;
  • mimicry;
  • pollination strategy;
  • scent ecology;
  • SPME

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. ECOLOGICAL AND EVOLUTIONARY ASPECTS OF FLORAL SCENT
  5. ANALYSIS AND CHARACTERIZATION OF FLORAL SCENT
  6. FLORAL SCENT CHEMISTRY AND POLLINATION IN ANNONACEAE
  7. FLORAL SCENT CHEMICAL DIVERSITY IN ANNONACEAE
  8. PERCEPTUAL DESCRIPTIONS OF FLORAL SCENT IN ANNONACEAE
  9. CONCLUSIONS
  10. ACKNOWLEDGEMENTS
  11. REFERENCES

Many species of Annonaceae are known for their distinctive, penetrating floral aromas. Numerous pollination studies have documented floral scents which probably play a key role in specialized pollination strategies. In particular, floral scents appear to play crucial roles in deceptive pollination strategies, contributing to floral mimicry of ripe or decaying fruits, fungi and, potentially, carrion or faeces. Occasionally, floral scent may advertise genuine floral rewards, as is the case for two species of Unonopsis pollinated by male euglossine bees. To date, ten studies have chemically characterized floral scent for 24 species representing 11 genera of Annonaceae. In this review, I discuss the chemical composition and diversity of the analysed floral scents in Annonaceae. I also summarize and discuss a wide range of (human) perceptual descriptions of floral scent found throughout the literature on Annonaceae. I have framed discussions of floral scent in Annonaceae in ecological and evolutionary contexts whenever possible. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 169, 262–279.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. ECOLOGICAL AND EVOLUTIONARY ASPECTS OF FLORAL SCENT
  5. ANALYSIS AND CHARACTERIZATION OF FLORAL SCENT
  6. FLORAL SCENT CHEMISTRY AND POLLINATION IN ANNONACEAE
  7. FLORAL SCENT CHEMICAL DIVERSITY IN ANNONACEAE
  8. PERCEPTUAL DESCRIPTIONS OF FLORAL SCENT IN ANNONACEAE
  9. CONCLUSIONS
  10. ACKNOWLEDGEMENTS
  11. REFERENCES

Flowers of Annonaceae are frequently noted to have strong, distinctive floral scents. Indeed, numerous studies have linked floral scent to specialized pollination syndromes in tropical Annonaceae. Although floral scent probably plays a key role in the reproductive ecology of many species of Annonaceae, relatively little work has been carried out to characterize scents within the family. This is not a shortcoming unique to Annonaceae research, however. A review by Knudsen et al. (2006) indicated that, at that time, the majority of angiosperm families had been subjected to little or no research on floral scent. Furthermore, studies of floral biology and pollination ecology, historically, have been biased towards visual aspects of floral phenotype, and most humans typically lack a reliable vocabulary with which to characterize odour and communicate its qualities (Raguso, 2008). Thus, characterizations of floral scent (or a lack thereof) are lacking from some studies focusing on floral biology or pollination ecology of Annonaceae, especially in work from previous decades. At best, floral scents are referred to colloquially (e.g. Gottsberger, 1988; Gottsberger, Meinke & Porembski, 2011).

Existing floral scent characterizations in Annonaceae, whether by chemical analysis or human perception, show scent to be a dynamic and diverse component of floral phenotype, warranting increased attention as a crucial component of pollination ecology in the family. In this article, I briefly review (in the context of early diverging angiosperms and, in particular, Annonaceae) the ecological and evolutionary importance of floral scent, its utility as a phylogenetic trait and current methods for its analysis. I then present an overview of the existing literature on floral scents in Annonaceae and suggest directions in which this research is headed.

ECOLOGICAL AND EVOLUTIONARY ASPECTS OF FLORAL SCENT

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. ECOLOGICAL AND EVOLUTIONARY ASPECTS OF FLORAL SCENT
  5. ANALYSIS AND CHARACTERIZATION OF FLORAL SCENT
  6. FLORAL SCENT CHEMISTRY AND POLLINATION IN ANNONACEAE
  7. FLORAL SCENT CHEMICAL DIVERSITY IN ANNONACEAE
  8. PERCEPTUAL DESCRIPTIONS OF FLORAL SCENT IN ANNONACEAE
  9. CONCLUSIONS
  10. ACKNOWLEDGEMENTS
  11. REFERENCES

The scent of a flower typically consists of a blend of volatile compounds emitted by floral tissues. Although floral scent is frequently studied as it relates to plant–pollinator interactions, the scent blend consists of volatiles acting as a ‘signal’ to other organisms in the environment (e.g. pollinators or herbivores) and volatiles which may represent by-products of biosynthetic pathways, neutral genetic variation or other environmental factors (Raguso, 2003). It is important to keep this in mind when considering ecological implications of complex floral scent blends, as is the case in most analysed species of Annonaceae. Certain scent compounds may be indicative of specialized pollination strategies, whereas other compounds may reflect phylogenetic constraints, plant defence or other evolutionary or ecological factors (Raguso, 2008; Junker & Blüthgen, 2010).

Studies of floral scent in early diverging angiosperms (angiosperms that belong to neither the monocots nor the eudicots) suggest that floral scent volatiles arose from compounds previously associated with plant defence (Pellmyr & Thien, 1986). Strong floral odours, with dull coloration, fleshy petals and, occasionally, thermogenesis, are traits common in extant lineages of these plants (Thien, Azuma & Kawano, 2000; Endress, 2010). These floral traits are typically linked to pollination by beetles and flies (Thien et al., 2000; Silberbauer-Gottsberger, Gottsberger & Webber, 2003; Endress, 2010), and diverse families of Coleoptera and Diptera were already present when early angiosperms underwent rapid radiation and diversification (Baker & Hurd, 1968; Ren, 1998; Thien et al., 2000). Thus, insect perception of and interaction with floral odour, colour and morphology are central to the rapid diversification of reproductive strategies seen within early diverging angiosperms (Thien et al., 2000). The study of floral scent in the extant lineages (such as Annonaceae) provides a unique and important perspective on interactions between the earliest flowering plants and potential insect pollinators (Pellmyr & Thien, 1986; Jürgens, 2009). Floral scent is of particular interest in Annonaceae, as many species across multiple genera share a similar floral bauplan (van Heusden, 1992), but exhibit a fascinating diversity of floral scent and diverging pollination strategies (e.g. Silberbauer-Gottsberger et al., 2003; Saunders, 2012).

If pollinators and herbivores exert strong selective pressures on floral volatile composition, we might expect floral scent to have low phylogenetic utility. Knudsen et al. (2006) reviewed 268 published papers on floral scent, concluding that, as a result of the high variability of floral scent composition between closely related individuals, floral scent is not particularly informative for the characterization of clades at or above the generic level. However, Knudsen et al. (2006) acknowledged that floral scent could provide a better fit to phylogenetic trees if particular biosynthetic scent pathways were to show notable phylogenetic constraints within currently under- or unstudied families or genera (see Knudsen & Ståhl, 1994; Levin, McDade & Raguso, 2003). At lower taxonomic levels, several authors have found floral scent composition to be useful in the elucidation of ecological or evolutionary patterns, especially between closely related species and within or between populations (e.g. Knudsen, 1999; Levin, Raguso & McDade, 2001; Raguso et al., 2003; Mant, Peakall & Schiestl, 2005; Majetic, Raguso & Ashman, 2008). In these studies, floral scent is linked to the pleiotropy of floral biochemistry, edaphic plasticity and potential incipient speciation, demonstrating the compelling role of floral scent in our understanding of floral ecology and evolution.

ANALYSIS AND CHARACTERIZATION OF FLORAL SCENT

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. ECOLOGICAL AND EVOLUTIONARY ASPECTS OF FLORAL SCENT
  5. ANALYSIS AND CHARACTERIZATION OF FLORAL SCENT
  6. FLORAL SCENT CHEMISTRY AND POLLINATION IN ANNONACEAE
  7. FLORAL SCENT CHEMICAL DIVERSITY IN ANNONACEAE
  8. PERCEPTUAL DESCRIPTIONS OF FLORAL SCENT IN ANNONACEAE
  9. CONCLUSIONS
  10. ACKNOWLEDGEMENTS
  11. REFERENCES

When analysing floral scent, whether by human perception or by chemical analysis techniques, it is important to keep several factors in mind. Volatiles emitted from flowers may vary spatially (from different floral organs or locations within organs), temporally (with diurnal, nocturnal or circadian rhythms), between different stages of floral ontogeny, in association with post-pollination changes or through the process of senescence (Moorherjee, Trenkle & Wilson, 1990; Knudsen & Tollsten, 1991; Schade, Legge & Thompson, 2001; Flamini, Cioni & Morelli, 2003; Raguso et al., 2003; Goodrich et al., 2006). Flowers of Annonaceae are typically protogynous, exhibiting dichogamy in their transition from female to male sexual stage. Existing studies characterizing floral scent in Annonaceae, whether by chemical analyses or human perception alone, show scent to be a highly dynamic character with potential variation between female and male stages of floral ontogeny and/or a potential link to diurnal rhythms, especially when in combination with floral thermogenesis (Armstrong & Marsh, 1997; Nagamitsu & Inoue, 1997; Momose, Nagamitsu & Inoue, 1998a; Gottsberger, 1999; Jürgens, Webber & Gottsberger, 2000; Silberbauer-Gottsberger et al., 2003; Webber & Gottsberger, 2003; Goodrich et al., 2006; Ratnayake et al., 2006, 2007; Teichert et al., 2008; Goodrich & Raguso, 2009; Silva & Neta, 2010; Braun, Dötterl & Gottsberger, 2011). Thus, time of day and floral ontogenetic stage are important factors when making scent ‘observations’ for species of Annonaceae.

Flower scent should also be differentiated from vegetative scents, ambient environmental scents and scents caused by plant wounding, especially when sampling cut flowers. In chemical analyses of floral scent, vegetative and ambient control samples can be used to distinguish between vegetative or ambient volatiles and floral volatiles. Some volatiles may be released from both floral and vegetative tissues, making it difficult to assess the importance of these volatiles in flower-specific functions of pollinator attraction and behavioural manipulation.

Some of the most common scent collection techniques for floral volatiles include static headspace collection using solid-phase microextraction (SPME) and varied forms of dynamic headspace collection. The SPME methods allow for rapid field and laboratory sampling and broad qualitative analysis of floral scent; however, only relative quantities of volatile compounds can be inferred from these methods, and these data are influenced by several factors in addition to the abundance of a compound in the sample. Dynamic headspace collection techniques generally require longer times for scent collection, except when small scent traps are used in combination with direct thermal desorption (see Dötterl & Jürgens, 2005). Dynamic headspace methods are not as practical for cut flowers or dissected floral organs because the volatiles emitted from dissected tissue after several hours may not represent the floral volatiles emitted under normal physiological conditions. Dynamic headspace sampling provides a more accurate quantification of volatiles emitted and, with the addition of internal and external standards, scent emission rates can be calculated. Furthermore, several subsamples of the eluate can be injected on different gas chromatography (GC) columns under different conditions, which is minimally necessary for the identification of unknown compounds. A more detailed explanation of the techniques and considerations for their use is given in Agelopoulos & Pickett (1998), Raguso & Pellmyr (1998), Flamini et al. (2003) and Tholl et al. (2006).

Detailed chemical analyses of floral scent are not always practical because of technological constraints and the time and/or funding necessary for such analyses. Floral scent characterization based on human perception alone can provide valuable preliminary information. Human perceptions of scent may vary somewhat between individuals, as discussed by Goodrich et al. (2006) with regard to the floral scent of Asimina triloba (L.) Dunal (a temperate species of Annonaceae). The floral scent of A. triloba has been characterized as stinking or unpleasant with specific reference to fermentation (Delpino, 1874), putatively derived from decomposing albuminoid or nitrogenous compounds (Kerner von Marilaum, 1895) or foetid, similar to decaying meat (Kral, 1960). Chemical analysis has shown that the floral scent of A. triloba contains many of the same fermentation products as emitted by baker's yeast (Saccharomyces cerevisiae), including acetic acid, ethyl acetate, ethanol, 3-methyl-1-butanol, 3-hydroxy-2-butanone and butanediols (Goodrich et al., 2006). However, the floral scent lacks nitrogen- or sulphur-containing compounds typical of decomposing meat or the odour of carrion-mimicking flowers (Kite & Hetterscheid, 1997; Stensmyr et al., 2002; Jürgens, Dötterl & Meve, 2006).

Although descriptions, such as ‘fermented’ and ‘yeasty’, most accurately represent the chemical composition of A. triloba floral scent, all the descriptions listed above fall within a similar odour genre distinctly different from human perceptions of ‘sweet’, ‘fruity’ or ‘pleasant’. The simple distinction between pleasant and unpleasant floral scents (based on human perception) may yield some information regarding pollination strategy. Common floral compounds, such as linalool, geraniol and phenylacetaldehyde, are perceived by humans as ‘very pleasant’ and ‘sweet’, and are known to be highly attractive to butterflies, moths and bees (Knudsen & Tollsten, 1993; Andersson et al., 2002; Dobson, 2006). Common floral odours unpleasant to most humans may mimic scents of fermentation or protein decomposition, and these compounds (such as ethanol, indole or dimethyl disulphide) are more likely to attract saprophilous beetles and flies (Nout & Bartelt, 1998; Stensmyr et al., 2002; Jürgens et al., 2006). Further differentiation of floral odours, such as the distinction between ‘sour, fermenting fruits’ or ‘foetid, decomposing carrion’, may yield even more clues regarding distinct, if perhaps overlapping, pollinator fauna.

FLORAL SCENT CHEMISTRY AND POLLINATION IN ANNONACEAE

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. ECOLOGICAL AND EVOLUTIONARY ASPECTS OF FLORAL SCENT
  5. ANALYSIS AND CHARACTERIZATION OF FLORAL SCENT
  6. FLORAL SCENT CHEMISTRY AND POLLINATION IN ANNONACEAE
  7. FLORAL SCENT CHEMICAL DIVERSITY IN ANNONACEAE
  8. PERCEPTUAL DESCRIPTIONS OF FLORAL SCENT IN ANNONACEAE
  9. CONCLUSIONS
  10. ACKNOWLEDGEMENTS
  11. REFERENCES

Flowers of Annonaceae commonly exhibit characters typical of early angiosperms, including protogyny, distinctive floral scents, fleshy petals, formation of a chamber and, occasionally, thermogenesis (Thien et al., 2000; Silberbauer-Gottsberger et al., 2003). Most species studied in Annonaceae are pollinated by beetles and exhibit characteristics typical of small or large beetle pollination syndromes, including fleshy petals or food bodies, fruity, spicy or decaying scents and the formation of protective chambers (Momose et al., 1998b; Gottsberger, 1999; Silberbauer-Gottsberger et al., 2003; Webber & Gottsberger, 2003). Although fly pollination is less common in the family (Willson & Schemske, 1980; Norman, Rice & Cochran, 1992; Su et al., 2005), Silberbauer-Gottsberger et al. (2003) noted the occasional occurrence of characters consistent with this syndrome in Old and New World Annonaceae: spots of translucent tissue, unpleasant, sour or fermenting scents and nectar production. Thrips have been identified as either primary or secondary pollinators in a few species of Annonaceae (Momose et al., 1998a; Jürgens et al., 2000; Norman, 2003; Silberbauer-Gottsberger et al., 2003). In rare instances, male euglossine bees (Carvalho & Webber, 2000; Teichert et al., 2008) or cockroaches (Nagamitsu & Inoue, 1997) have been identified as pollinators.

In many of the published pollination studies of Annonaceae, including those described above, distinctive floral scents are thought to be crucial components of pollinator attraction. Many floral volatile compounds identified in Annonaceae (Ma et al., 1988; Jürgens et al., 2000; Goodrich et al., 2006; Ratnayake et al., 2007; Teichert, 2008; Teichert et al., 2008; Goodrich & Raguso, 2009; Braun et al., 2011; Pripdeevech, 2011; Teichert, Dötterl & Gottsberger, 2011) have been shown in other studies to attract known pollinator fauna. For example, floral scents for a number of nitidulid beetle-pollinated species contain aliphatic esters and alcohols attractive to species of nitidulid beetles (Phelan & Lin, 1991; Bartelt & Wicklow, 1999; Peña et al., 1999; Jürgens et al., 2000). The floral scent of euglossine bee-pollinated Unonopsis stipitata Diels contains trans-carvone oxide, a compound shown in field bioassays to be highly attractive to male euglossine bees (Whitten et al., 1986; Teichert et al., 2008). Clearly, floral scent should be expected to play a key role in the reproductive biology of many species of Annonaceae.

To date, ten studies (Ma et al., 1988; Jürgens et al., 2000; Goodrich et al., 2006; Ratnayake et al., 2007; Teichert, 2008; Teichert et al., 2008, 2011; Goodrich & Raguso, 2009; Braun et al., 2011; Pripdeevech, 2011) have described floral scent compounds for 24 species of Annonaceae, representing 11 genera, in North and South America and South-East Asia (see Table 2). Compounds identified in these species can be divided into five major compound classes: aliphatics, aromatics (benzenoids), isoprenoids (terpenes), nitrogen-containing compounds and sulphur-containing compounds. These categorizations are based on chemical structure and a broad understanding of plant secondary metabolic pathways, as described by Knudsen et al. (2006). The diversity of compounds in each of these categories varies widely between species, as indicated in Table 2. The major compound classes identified in Annonaceae are common to most angiosperm families sampled thus far, with the exception of nitrogen- and sulphur-containing volatiles, which are typically rare (Knudsen et al., 2006). However, the specific compounds produced and the predominance of certain compound classes over others in certain species may be more informative in an ecological or evolutionary context.

For example, all species included in the study of Jürgens et al. (2000) occurred in the Manaus region of Brazil, but are not closely related to one another based on several morphological and molecular phylogenetic studies of the family (Doyle & Le Thomas, 1996; Richardson et al., 2004; Couvreur et al., 2008; Chatrou et al., 2012). Five of the six species in this study [Anaxagorea brevipes Benth., Anaxagorea dolichocarpa Sprague & Sandwith, Duguetia asterotricha (Diels) R.E.Fr., Rollinia insignis R.E.Fr. (now Annona neoinsignis H.Rainer), Xylopia aromatica (Lam.) Mart. and Xylopia benthamii R.E.Fr.] have ‘fruity’ scents and cream or yellow petals, with Nitidulidae representing 94% or greater of the visitors observed (Table 1; Jürgens et al., 2000). However, these species achieve their ‘fruity’ scents using different volatile compounds. This shows potential convergent evolution towards small beetle pollination, and illustrates the significance of floral scent characterization in an ecological and phylogenetic context. Although Anaxagorea A.St.-Hil., Duguetia A.St.-Hil., Annona L. and Xylopia L. utilize different biochemical building blocks, they all produce floral scents characteristic of food substrates or brood sites of Nitidulidae (Phelan & Lin, 1991; Nout & Bartelt, 1998; Peña et al., 1999). Furthermore, the differences in compound class seen in the ‘fruity’ odours appear to group roughly by genus, suggesting that floral scent composition and the underlying biosynthetic pathways may have some phylogenetic utility in Annonaceae. The two Anaxagorea spp. have scents dominated by aliphatic compounds (primarily aliphatic esters). Both Xylopia spp. have floral scents dominated by aromatic compounds, primarily 2-phenylethyl alcohol (61.4%) in X. aromatica and methyl benzoate (38.6%) in X. benthamii. The floral scent of D. asterotricha is dominated by isoprenoid compounds and a number of unknown compounds not identified by class. The floral scent of Annona neoinsignis is dominated by naphthalene, although it was noted that naphthalene (the scent of moth-balls) might have been of anthropogenic origin (Jürgens et al., 2000).

Table 1.  Descriptions of floral scent, floral colour and pollinators for 93 species representing 30 genera of Annonaceae
Species (citation)LocationScent descriptionFloral colourPrimary pollinator(s)
Anaxagorea brevipes Benth.* (7)SAFruity, banana-likeCreamBeetles
Anaxagorea crassipetala Hemsl. (2)CAStrong spicy, fruity; detectable from several metresCreamy whiteFlies and beetles
Anaxagorea dolichocarpa Sprague & Sandwith* (7)SAFruity, banana-like, acetonicLight yellowBeetles
Anaxagorea manausensis A.Timmerman (14)SAFruity odoursNot reportedBeetles
Anaxagorea phaeocarpa Mart. (14)SAFruity odoursNot reportedBeetles
Anaxagorea prinoides St.Hil. & A.DC.* (21)SAStrong, fruity, banana-likeYellowBeetles
Annona ambotay Aubl. (27)SAFragrantDark red to yellowish redNot reported
Annona coriacea Mart. (6)SASomewhat unpleasant odourNot reportedBeetles
Annona cornifolia A.St.-Hil. (6)SAPleasant fruity odourYellow (purple)Beetles
Annona crassiflora Mart. (6)SASomewhat unpleasant odourNot reportedBeetles
Annona dioica A.St.-Hil. (6)SASomewhat unpleasant odourNot reportedBeetles
Annona glabra Forssk.* (6, 18)NA/SAHeavy acetonic scent; strongest at duskCream (red)Beetles
Annona monticola Mart. (6)SASomewhat unpleasant odourNot reportedBeetles
Annona neoinsignis H.Rainer (previously Rollinia insignis R.E.Fr.)* (7)SAFruity, sweetYellowBeetles
Annona tomentosa R.E.Fr. (6)SAPleasant fruity odourNot reportedBeetles
Asimina incana Exell* (4, 18, 8)NAStrong, pleasant, sweet, with slight acrid or waxy note as flowers enter male stageWhite/cream (yellow)Beetles
Asimina longifolia Kral* (4, 18, 8)NAFaint, sweet, slightly ‘green’, fragrantWhite/cream (purple)Beetles
Asimina obovata Nash* (12, 18, 8)NAPleasant, sweet, not very strongWhite/cream (purple)Beetles
Asimina reticulata Shuttlew. ex Chapm.* (4, 18, 19, 8)NAVery sweet and pleasantWhite/cream (purple)Beetles (bees observed)
Asimina pygmaea Dunal* (12, 18, 8)NAYeasty and cheesy; foetidMaroon (maroon)Beetles
Asimina tetramera Small* (18, 19, 8)NAYeasty, weak, slight rootbeer note; foetidMaroon (yellow)Beetles
Asimina parviflora Dunal* (18, 20, 8)NAYeasty, like baking bread, but slightly fruity; foetidMaroonFlies, beetles
Asimina triloba Dunal* (5, 15, 8)NAYeasty, like red wine or baking bread; foetidMaroon (yellow)Flies, beetles
Bocageopsis multiflora (Mart.) R.E.Fr. (6, 14)SAVariable – somewhat sweet or rancid; slight rancid-fruity odourWhitishThrips
Bocageopsis pleiosperma Maas (27)SASweet fragranceCreamy yellow (pinkish)Not reported
Cananga odorata (Lam.) Hook.f. & Thomson* (23)SEAIntensely sweet, similar to jasmineYellowish green to yellowNot reported
Cymbopetalum brasiliense Benth.* (32)SABalsamic; not fruit-likeYellowNone observed
Cymbopetalum torulosum G.E.Schatz (25)CASubtle odour reminiscent of linseed oilYellowish green to yellowBeetles
Deeringothamnus pulchellus Small* (11, 18)NAVery sweet and perfume-likeWhite/creamPossibly beetles or thrips
Deeringothamnus rugelii Small* (11, 18)NAVery faint, slightly rubbery or unpleasantYellowPossibly flies or thrips
Duguetia asterotricha (Diels) R.E.Fr. (7)SAFruity, pineapple-likeYellowishBeetles
Duguetia cadaverica Huber* (21)SAMouldy, cheesy, foetid scentRed (white)Beetles
Duguetia calycina Benoist (26)SAAgreeable and intensifying at night (with thermogenesis)Greenish-yellow to greenish-whiteBeetles
Duguetia flagellaris Huber (26, 27)SAOdour similar to fruit juice of Euterpe oleracea (acai palm); sweet scent of overripe pineapplesPink (red)Beetles
Duguetia furfuracea (A.St.-Hil.) Saff. (26)SAPleasant, fruity odourReddishBeetles
Duguetia lanceolata A.St.-Hil. (14)SAOnset of anthesis – pleasant fruity odour; later anthesis – change to rotting fruit odourDeep red petalsBeetles
Duguetia marcgraviana Mart. (30)SAFemale stage is similar to mango or caja (Spondias cytherea); male stage is similar to formaldehyde mixed with fruit (strong and repugnant)Brown to reddishBeetles
Duguetia neglecta Sandwith (26)SAInitially agreeable ripe fruit odour, changing to unpleasant rotten fruit odourCreamBeetles
Duguetia pycnastera Sandwith (26)SASmell of ripe peaches, changing to acetonic fruit ester odourPale yellowBeetles
Duguetia riparia Huber (26)SAAromaticYellowBeetles
Duguetia stelechantha (Diels) R.E. Fr. (26)SAOdour of ripe bananas, detectable from several metresYellow (wine-red)Beetles
Duguetia surinamensis R.E.Fr. (27)SAStrong smell or a slightly sweet aromaCream, maturing dull redNot reported
Duguetia trunciflora Maas & A.H.Gentry (27)SASmell of bananasCreamNot reported
Duguetia ulei (Diels) R.E.Fr. (26, 27)SAAromatic odour similar to squashed Myrtaceae leaves; mushroom-like odourCream-colouredBeetles
Enicosanthum cf. paradoxum Becc. (14)SEAAromatic odour of ripe fruitsYellowish-creamBeetles, some flies
Goniothalamus australis Jessup (14)AUSTStrong odour of fermented fruitsFrom green to yellow to deep brownish orange–redBeetles
Guatteria duodecima Maas & Westra (31)SAApple-like odourBrownish-yellowNot reported
Guatteria foliosa Benth. (14)SASlight fruity scent, similar to ripe bananasYellow, becoming reddish-brownBeetles
Guatteria megalophylla Diels (27)SAAromaticPinkish-orange to redNot reported
Guatteria meliodora R.E.Fr. (27)SAAromaticGreen, maturing yellowNot reported
Guatteria neglecta R.E.Fr. (6)SAHeavy, fruit-like odourYellowish, becoming brownBeetles
Guatteriopsis blepharophylla (Mart.) R.E.Fr. (27)SAPleasant smellWhitish-yellowNot reported
Guatteriopsis hispida R.E.Fr. (27)SAPleasant smellYellowNot reported
Haplostichanthus sp. F.Muell. (14)AUSTDid not detect any floral odourPale green (white, wine-red)Beetles
Isolona campanulata Engl. & Diels (28)AFFruit-like, fermentingYellow (dark purple)Beetles
Meiogyne sp. Miq. (14)AUSTStrong emission similar to mushrooms during female and male phasePale yellow (red)Beetles
Meiogyne virgata Miq. (14)SEAFemale stage slightly fruity odour; male stage stronger, penetrating odour of rotten fruitYellowishBeetles
Melodorum fruticosum Lour.* (29)SEAStrongly scentedPale yellowNot reported
Melodorum sp. Hook.f. & Thomson (14)AUSTSharp and acetone-likeBrown (cream)Beetles
Melodorum uhrii F.Muell. (14)AUSTFaint, aromatic, sweet, fruity, and apple-like noteNot reportedNo visitors observed
Monodora tenuifolia Benth. (28)AFSweetish, cabbage-like, similar to a rabbit hutch, mouldy, disagreeableYellowish with dark red spotsFlies, mostly dung flies
Oxandra euneura Diels (6)SASweet perfumed odour during female stageNot reportedBeetles and thrips
Piptostigma sp. Oliv. (28)AFFruity, apple-likeLight yellowBeetles
Polyalthia cf. cauliflora Hook.f. & Thomson (14)SEAVery slight peach-like or resinous odour; later, slight peach – and yet stronger, straw-like odourCarmin (cream white)Did not detect floral visitors – self-pollination is likely
Polyalthia coffeoides (Thwaites) Hook.f. & Thomson (16)SEAStrong alcoholic to fermented fruit-like scentYellowish greenBeetles
Polyalthia discolor Diels (13)SEAPleasing, strong, like Cananga odorataYellowBeetles
Polyalthia glauca Boerl. (13)SEAPleasing, strong, like Cananga odorataYellowBeetles
Polyalthia hypoleuca Hook.f. & Thomson (13)SEAPleasing, strong, like Cananga odorataYellowBeetles
Polyalthia korinti (Dunal) Hook.f. & Thomson (16)SEAStrong alcoholic to fermented fruit-like scentVivid greenBeetles
Polyalthia multinervis Diels (13)SEANo odour detectedYellowBeetles
Polyalthia sumatrana King (13)SEAPleasing, strong, like Cananga odorataYellowBeetles
Popowia pisocarpa Endl. (9)SEAStrong odour throughout female and male phase; ‘different’ from other AnnonaceaeNot reportedThrips
Pseuduvaria froggattii (F.Muell.) Jessup (14)AUSTUnpleasant scent reminiscent of old dishwater or vomitCream (wine-red, dark purple)Flies and beetles
Rollinia mucosa Baill. (7)SAFruity, sweet odourCreamNot reported
Sapranthus isae J.G.Vélez & Cogollo (24)SAFragrantGreen (purple, black)Not reported
Sapranthus sp. Seem. (14)SAExhales an unpleasant odourDark purple or brownBeetles, bees, possibly flies
Sapranthus viridiflorus G.E.Schatz (24)SALingering, strong foetid scent of carrion, similar to stapelias and aristolochiasGreen (purple, white)Not reported
Tetrameranthus duckei R.E.Fr. (6, 27)SAMusky odours (during the night); musky odour or strong fragrance of aniseYellowBeetles
Unonopsis duckei R.E.Fr. (27)SASweet scentCreamNot reported
Unonopsis guatterioides (A.DC.) R.E.Fr. (3, 27)SASimilar to lemongrass or vanilla, strongest in morningCreamEuglossine bees
Unonopsis stipitata Diels* (22)SAStrong, spearmint-like odourCreamEuglossine bees
Uvaria elmeri Merr. (10)SEAOdour like decayed wood or a mushroom, stronger during the male phaseCreamy white or brownCockroaches, flies
Uvariodendron calophyllum R.E.Fr. (28)AFFruity, spicy, aromatic and sweetPale yellow (red)Beetles
Uvariodendron connivens (Benth.) R.E.Fr. (28)AFStrong, aromatic and fruityGreyish magentaBeetles
Uvariopsis bakeriana (Hutch. & Dalziel) Robyns & Ghesq. (28)AFFaint, with sharp notes, pungent, spicy, nutmeg-likeViolet brownRare visitors, dung flies
Uvariopsis congolana (De Wild.) R.E.Fr. (28)AFSharp, pungent, fungus-like, sulphur-likeYellowishSporadic dung fly visitors
Xylopia amazonica R.E.Fr. (27)SAAromaticCreamNot reported
Xylopia aromatica (Lam.) Mart.* (7)SASweet, aromaticWhiteThrips
Xylopia benthamii R.E.Fr.* (7)SAFruity, similar to ripe fruit of Spondias luteaYellowishBeetles
Xylopia brasiliensis Spreng. (1)SAFruity odoursPale colourBeetles
Xylopia championii Hook.f. & Thomson* (17)SEAStrong, fruity odourYellowish-creamBeetles
Xylopia emarginata var. duckei R.E.Fr. (27)SAFruity odourYellowNot reported
Xylopia spruceana Benth. ex Spruce (27)SAScentedYellow (white)Not reported

Floral scent composition in Asimina Adans. also demonstrates the potential utility of scent composition in evolutionary and ecological contexts. Floral scents of Asimina are qualitatively quite different from the ‘fruity’ scents described by Jürgens et al. (2000), with half the genus emitting ‘yeasty’ floral odours and the other half emitting ‘sweet’, ‘pleasant’ and ‘waxy’ scents (Table 1). Flowers with yeasty scents share a small size and maroon pigmentation and probably mimic food or brood sites of local pollinating insects (Goodrich & Raguso, 2009; K. Goodrich, unpubl. data). Alternatively, flowers with pleasant, sweet scents share white coloration and relatively larger floral dimensions, and probably represent a genuine advertisement of copious floral tissues, pollen and liquid exudates (Goodrich & Raguso, 2009; K. Goodrich, unpubl. data). On a finer scale, the floral scent of yeasty maroon flowers shows potential diversification of mimicry types. Two species [A. triloba (L.) Dunal and A. parviflora (Michx.) Dunal] occur in mesic woodlands of temperate North America (Kral, 1960), and their scents are dominated by small aliphatic alcohols and esters associated with rotting fruits or fermenting sugars (Table 2; Goodrich et al., 2006; Goodrich & Raguso, 2009). The other two species with yeasty scents contain many of the same aliphatic compounds, with the addition of dimethyl disulphide in A. pygmaea (W.Bartram) Dunal and indole in A. tetramera Small (Table 2; Goodrich & Raguso, 2009). Dimethyl disulphide and indole are characteristic of the scents of carrion and faeces, respectively. Both A. pygmaea and A. tetramera occur in dry, sandy pine scrub habitats in Florida, USA (Kral, 1960), and the addition of dimethyl disulphide or indole may represent a transition towards mimicry of food sources more common to these habitats. This diversification of mimicry types has been demonstrated previously in Araceae and several stapeliads (Apocynaceae; Stensmyr et al., 2002; Jürgens et al., 2006). Evolutionarily, the two broad scent types of Asimina may represent a single divergence or multiple transitions between suites of floral traits. In addition, the visual displays of white-flowered Asimina spp. are strikingly similar, whereas the species-specific scent blends are quite distinct. It will be interesting to examine the role of floral scent in reproductive isolation of sympatric taxa, potentially through odour-mediated floral constancy (see Wright & Schiestl, 2009).

Table 2.  Floral scent chemical diversity by broad biosynthetic class for 24 species representing 11 genera of Annonaceae
Species (citation)LocationAliph hcAliph alcohAliph est & ethAliph ald & ketBenz hcOxy benzMono hcOxy monoSesqui hcOxy sesquiN-cmpdsS-cmpds
  1. Values reported as number of different compounds within each compound class, with compounds unique to each species in parentheses. Locality abbreviations: NA, North America; SA, South America; SEA, South-East Asia. Chemical class abbreviations: Aliph hc, aliphatic hydrocarbons; Aliph alcoh, aliphatic alcohols; Aliph est & eth, aliphatic esters and ethers; Aliph ald & ket, aliphatic aldehydes and ketones; Benz hc, benzenoid hydrocarbons; Oxy benz, oxygenated benzenoids; Mono hc, monoterpene hydrocarbons; Oxy mono, oxygenated monoterpenoids; Sesqui hc, sesquiterpene hydrocarbons; Oxy sesqui, oxygenated sesquiterpenoids; N-cmpds, nitrogen-containing compounds; S-cmpds, sulphur-containing compounds.

Asimina triloba (2)NA04 (0)3 (0)1 (0)008 (0)1 (0)8 (0)08 (4)0
Asimina parviflora (3)NA03 (0)9 (2)3 (2)01 (1)3 (0)017 (0)000
Asimina tetramera (3)NA1 (0)4 (0)1 (0)1 (0)02 (1)7 (0)1 (0)8 (0)02 (0)0
Asimina pygmaea (3)NA3 (0)3 (0)1 (0)2 (0)02 (0)5 (0)1 (0)14 (0)01 (0)1 (1)
Asimina obovata (3)NA3 (0)01 (0)1 (0)1 (1)1 (0)7 (0)9 (1)12 (0)1 (0)00
Asimina incana (3)NA5 (1)01 (0)3 (0)06 (0)7 (0)12 (2)13 (0)1 (0)1 (0)0
Asimina reticulata (3)NA4 (1)001 (0)04 (0)5 (0)3 (0)11 (0)01 (0)0
Asimina longifolia (3)NA4 (1)2 (1)1 (0)1 (0)003 (0)6 (0)9 (0)01 (0)0
Deeringothamnus rugelii (3)NA1 (0)01 (0)2 (1)01 (0)4 (0)3 (1)6 (0)1 (0)2 (0)0
Deeringothamnus pulchellus (3)NA003 (1)006 (1)2 (0)3 (0)6 (0)1 (0)3 (0)0
Annona glabra (3)NA/SA03 (2)1 (0)1 (1)009 (0)2 (0)2 (0)000
Anaxagorea brevipes (4)SA1 (0)08 (7)0004 (0)1 (0)4 (0)000
Anaxagorea dolichocarpa (4)SA1 (0)011 (4)1 (0)3 (0)2 (0)3 (0)03 (0)01 (1)0
Anaxagorea prinoides (8)SA01 (0)6 (2)000000000
Annona neoinsignis (previously Rollinia insignis) (4)SA1 (0)001 (0)6 (0)1 (0)3 (0)09 (0)000
Unonopsis stipitata (9)SA00000012 (2)8 (6)0000
Cymbopetalum brasiliense (1)SA000002 (1)000000
Duguetia asterotricha (4)SA2 (1)0001 (0)03 (0)06 (0)000
Duguetia cadaverica (8)SA04 (4)1 (1)000000002 (2)
Xylopia aromatica (4)SA1 (0)001 (0)3 (0)6 (1)6 (0)2 (2)9 (0)01 (0)0
Xylopia benthamii (4)SA1 (0)0006 (0)2 (0)3 (0)1 (0)5 (0)000
Xylopia championii (7)SEA008 (7)0005 (3)4 (3)7 (4)1 (1)00
Cananga odorata (5)SEA004 (3)003 (1)01 (0)0000
Melodorum fruticosum (6)SEA005 (3)005 (3)14 (4)6 (5)20 (10)4 (4)00

The remaining scent studies of Annonaceae are of more isolated taxa and generally illustrate the role of scent in highly specialized pollination systems (Ma et al., 1988; Ratnayake et al., 2007; Teichert, 2008; Teichert et al., 2008, 2011; Braun et al., 2011; Pripdeevech, 2011). Four other New World species of Annonaceae were studied [Duguetia cadaverica Huber, Anaxagorea prinoides (Dunal) A.DC., Unonopsis stipitata and Cymbopetalum brasiliense (Vell.) Benth. ex Baill.; Teichert, 2008; Teichert et al., 2008, 2011; Braun et al., 2011], with scent playing a central role in at least three distinctly different and specialized pollination syndromes. Anaxagorea prinoides has a relatively simple scent blend (only seven compounds) described as strong and banana-like (Teichert et al., 2011). The pollination strategy of this species appears to conform to the small beetle pollination observed for Anaxagorea dolichocarpa and several other species, described by Jürgens et al. (2000). Unonopsis stipitata emits high levels of several monoterpenes, including limonene and carvone and their oxides, found to be highly attractive to male euglossine bees (Teichert et al., 2008), and these bees have been documented as the main floral visitors. One other species of Annonaceae, Unonopsis guatteroides (A.DC.) R.E.Fr., has been shown to be pollinated by male euglossine bees (Carvalho & Webber, 2000). No floral scent analyses have been performed on this species, but the scent has been described as similar to lemon grass or vanilla (Table 1; Carvalho & Webber, 2000).

The floral scent of D. cadaverica is described as ‘mouldy’, ‘cheesy’ and ‘mushroom-like’, with (E)-2-octen-1-ol and (Z)-1-octen-5-ol as the main compounds (Table 1; Teichert, 2008). These eight-carbon alcohols are typical of mushroom odour (Picardi & Issenberg, 1973) and, with the fleshy red and white petals and occurrence of flowers along flagelliform twigs at ground level, yield convincing mushroom mimics. This mimicry observation is supported by the attraction of mycetophagous beetles as pollinators (Teichert, 2008). An odour similar to mushrooms has also been described for two Asian species (Uvaria elmeri Merr. and an unidentified species of Meiogyne Miq.; Nagamitsu & Inoue, 1997 and Silberbauer-Gottsberger et al., 2003, respectively), the African species Uvariopsis congolana (De Wild.) R.E.Fr. (Gottsberger et al., 2011) and the South American species Duguetia ulei (Diels) R.E.Fr. (Maas, Maas & Miralha, 2007), suggesting that this type of mimicry has evolved at least several times in the family. It will be interesting to see whether eight-carbon alcohols or ketones dominate the floral scent of these other species characterized as having ‘mushroom’ or ‘fungus-like’ odours.

Finally, flowers of Cymbopetalum brasiliense emit a ‘balsamic’ scent which is ‘not reminiscent of fruit’ (Braun et al., 2011). The scent of C. brasiliense is uncharacteristically simple for Annonaceae, consisting mostly of p-methyl anisol (> 99% relative scent composition), with small quantities of p-cresol (Braun et al., 2011). Braun et al. (2011) observed few floral visitors and agamospermic fruit production in C. brasiliense, providing the first documented case of probable apomixis in Annonaceae. p-Methyl anisol, however, is also a key floral scent component (> 99% relative scent composition) for several species of Phytelephas Ruiz & Pav. (Ervik, Tollsten & Knudsen, 1999) and, in field bioassays, Ervik et al. (1999) found that numerous insects were attracted to filter paper soaked in p-methyl anisol. These contradictory results may reflect variation in pollinator communities, or a product of the forest fragmentation surrounding populations of C. brasiliense documented by Braun et al. (2011).

Only three Old World species of Annonaceae have had their floral scent composition analysed: Xylopia championii Hook.f. & Thomson (Ratnayake et al., 2007), Cananga odorata (Lam.) Hook.f. & Thomson (Ma et al., 1988) and Melodorum fruticosum Lour. (Pripdeevech, 2011). Ratnayake et al. (2007) described the scent of X. championii as strong and fruity, dominated by caproic acid, an ethyl ester of hexanoate and ethyl decadienoate. In this case, floral odour emission is strongly correlated with floral reproductive phase and floral thermogenesis. These traits, in combination with small floral dimensions, indicate that this species is specialized for its observed curculionid beetle pollinators (Ratnayake et al., 2007). The studies of Cananga odorata (Lam.) Hook.f. & Thomson and Melodorum fruticosum Lour. do not present the data in the context of pollination strategies. Cananga odorata (commonly known as ylang-ylang) is highly valued for its floral essential oils (Manner & Elevitch, 2006) which yield a heavy, sweet scent, but little is known about its reproductive biology. Ma et al. (1988) reported the floral volatiles of Cananga odorata to include ethyl, propyl, butyl and pentyl acetates, several benzenoid compounds and linalool (a monoterpene alcohol). A number of studies have documented bioactive constituents from bark, leaves, branches and flowers of M. fruticosum (Jung et al., 1990; Tuchinda et al., 1991; Pripdeevech & Chukeatirote, 2010), but little work has been carried out on its pollination biology. Pripdeevech (2011) characterized the floral scent for M. fruticosum using three types of SPME fibres to illustrate the variation that this technique may potentially yield (as discussed earlier in this article). Although the relative percentages of floral compounds varied by fibre type, all fibre types showed the floral scent of M. fruticosum to contain relatively large quantities of p-methyl anisol (a benzenoid compound discussed for C. brasiliense, above) and the monoterpenes β-phellandrene, trans-β-ocimene and linalool, with each of these compounds representing > 5% relative scent composition for most or all of the sampling techniques used (Pripdeevech, 2011).

FLORAL SCENT CHEMICAL DIVERSITY IN ANNONACEAE

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. ECOLOGICAL AND EVOLUTIONARY ASPECTS OF FLORAL SCENT
  5. ANALYSIS AND CHARACTERIZATION OF FLORAL SCENT
  6. FLORAL SCENT CHEMISTRY AND POLLINATION IN ANNONACEAE
  7. FLORAL SCENT CHEMICAL DIVERSITY IN ANNONACEAE
  8. PERCEPTUAL DESCRIPTIONS OF FLORAL SCENT IN ANNONACEAE
  9. CONCLUSIONS
  10. ACKNOWLEDGEMENTS
  11. REFERENCES

A summary of the diversity of floral scent composition for all sampled species of Annonaceae is provided in Table 2. Several conclusions can be drawn from the diversity of floral scent composition in species of Annonaceae studied to date. First, it is interesting to compare scent composition and diversity between genera, although this comparison is limited by the number of species sampled within each genus. For example, the three Anaxagorea spp. sampled show relatively high diversity in aliphatic esters compared with the other genera, and these compounds are probably responsible for the strong ‘fruity’ aromas characteristic of these species. Asimina shows relatively high frequency and diversity of aliphatic hydrocarbons, aldehydes and ketones compared with all other genera sampled. Finally, oxygenated benzenoid compounds occur with almost complete absence of benzenoid hydrocarbons in Asimina and Deeringothamnus Small, whereas they are frequently associated with benzenoid hydrocarbons in Anaxagorea, Annona and Xylopia spp.

This comparison of floral scent diversity and composition may also be indicative of shared ecology and/or pollination strategy. For example, relatively high proportions of aliphatic alcohols are found in maroon-flowered Asimina spp. and D. cadaverica and, in combination with the red or maroon pigmentation of these species, may be linked to specialized food mimicry pollination strategies (Teichert, 2008; Goodrich & Raguso, 2009). Furthermore, the dimethyl oligosulphides, found only in A. pygmaea and D. cadaverica (Teichert, 2008; Goodrich & Raguso, 2009), may represent specialization towards specific mimicry of protein decomposition typical of carrion or faeces. The eight-carbon alcohols of D. cadaverica are highly indicative of mushroom mimicry (see discussion above), but the oligosulphides may mimic substrates on which mushrooms may occur. Finally, the relatively high number of aliphatic hydrocarbons found in six Asimina spp. may be linked to adaptations preventing desiccation (see Hadley, 1981), as these species occur in xeric pine scrub habitats (Kral, 1960), unlike most other sampled Asimina spp. from mesic tropical or temperate forests.

The absence of certain compound classes may also be evolutionarily or ecologically informative. For example, sesquiterpene hydrocarbons appear to be relatively diverse and ubiquitous (high numbers and low ‘unique’ representation in Table 2) in the floral scent of many species, and it is therefore interesting that this class of compounds is not reported for four species. This result, however, may be an artefact of the differing interpretations of floral scent data by individual researchers. Sesquiterpenes are frequently associated with leaf odours in Annonaceae (Oguntimein et al., 1989; Fekam Boyom et al., 1996; Maia et al., 2005; K. Goodrich, unpubl. data). Their absence in floral scent analyses by Ma et al. (1988), Teichert (2008), Teichert et al. (2008) and Braun et al. (2011) may reflect the absence of these compounds from floral scent altogether, their absence in concentrations or proportions above those of vegetative odours, or the authors' decision to report only compounds unique to floral tissue. Perhaps more informative is the almost complete absence of oxygenated monoterpenes from sampled species of Anaxagorea and Duguetia, and the absence of both oxygenated and hydrocarbon benzenoid compounds from Old World Xylopia championii, compared with their relative abundance in the two New World Xylopia spp. There is also a notable lack of nitrogenous compounds in tropical species sampled compared with the temperate species of Asimina and Deeringothamnus. However, given the nested phylogenetic position of Deeringothamnus in Asimina (R. Abbott, Department of Biological Sciences, Eastern Illinois University, Charleston & K. Neubig, Department of Biology, University of Florida, Gainesville, pers. comm.), the presence of nitrogenous compounds in this clade is a result of shared ancestry. Whether this is a result of differences between temperate and tropical habitats is difficult to test as the AsiminaDeeringothamnus clade is the only temperate group in Annonaceae, and therefore no further comparisons of tropical and temperate sister groups can be made.

As a final point, it is interesting and informative to compare the similarities and differences between entire scent datasets. Jürgens (2009) illustrated the potentially strong link between overall floral scent composition and pollination strategy by conducting a multivariate analysis of 150 identified compounds across 21 species of Annonaceae. Jürgens (2009) then demonstrated how species which group by similarity of scent composition also group roughly by pollination strategy. This type of meta-analysis becomes increasingly informative as scent studies are performed across additional species and genera.

PERCEPTUAL DESCRIPTIONS OF FLORAL SCENT IN ANNONACEAE

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. ECOLOGICAL AND EVOLUTIONARY ASPECTS OF FLORAL SCENT
  5. ANALYSIS AND CHARACTERIZATION OF FLORAL SCENT
  6. FLORAL SCENT CHEMISTRY AND POLLINATION IN ANNONACEAE
  7. FLORAL SCENT CHEMICAL DIVERSITY IN ANNONACEAE
  8. PERCEPTUAL DESCRIPTIONS OF FLORAL SCENT IN ANNONACEAE
  9. CONCLUSIONS
  10. ACKNOWLEDGEMENTS
  11. REFERENCES

Several scent ‘types’ are clearly recognizable in Annonaceae, including several variations of ‘fruity’, ‘aromatic’, ‘sweet (but not fruit-like)’ and ‘mushroom-like’, even without extensive chemical analyses. Scent descriptions from the literature have been compiled in Table 1. I then subjectively categorized the scent descriptions (based on the descriptions provided for 93 species) to provide a more general overview of the frequency of scent types currently described in the family (Fig. 1). Although these perceptual depictions are subjective and may vary somewhat by author, these depictions of floral scent give some clues to the possible chemical composition of the scent. One of the most common scent descriptions mentioned in the existing literature for the family is ‘fruity’ (Fig. 1), which is often further qualified as ‘fruity and sweet’, ‘ripe fruit’ or ‘rancid/rotting fruit’. Typical fruit odours are usually associated with ripe fruits, close to or at an early stage of decay. Although the smell of ripe fruit from different families and genera varies, common ripe fruit odours consist of a blend of branched aliphatic esters, alcohols and lactones (Macku & Jennings, 1987; Horvat et al., 1990; Shiota, 1991; Augusto et al., 2000; Carasek & Pawliszyn, 2006). As a fruit becomes more rotten, its scent noticeably becomes more fermented or alcoholic (a sharper, unpleasant odour). Several protogynous species of Annonaceae [Meiogyne virgata (Blume) Miq., Duguetia lanceolata A.St.-Hil., D. marcgraviana Mart., D. neglecta Sandwith and D. pycnastera Sandwith] are described as having pleasant or slight ‘fruity’ odours during their female phase, which change to more ‘rotten’ or ‘rancid’ fruit odours as they progress through the male stage (Silberbauer-Gottsberger et al., 2003; Webber & Gottsberger, 2003; Silva & Neta, 2010). Studies of fermentation volatiles typically show the presence of ethanol, ethyl acetate, 3-methyl-1-butanol and 3-hydroxy-2-butanone (Lee et al., 1997; Goodrich et al., 2006; Gürbüz, Rouseff & Rouseff, 2006), and these compounds may potentially be found in floral odours mimicking rotten fruits, as they are also seen in the ‘yeasty’ odour of some Asimina spp. (Goodrich & Raguso, 2009).

image

Figure 1. Annonaceae scent ‘types’ based on descriptions of 93 species.

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The most common specific ‘fruity’ odour in Annonaceae is ‘banana-like’, often found in combination with descriptions of an ‘alcoholic’ or ‘acetonic’ scent (Table 1). The odour of ripe bananas was described for Anaxagorea dolichocarpa, A. brevipes, A. prinoides, Duguetia stelechantha (Diels) R.E.Fr., D. trunciflora Maas & Gentry and Guatteria foliosa Benth. (Jürgens et al., 2000; Silberbauer-Gottsberger et al., 2003; Webber & Gottsberger, 2003; Maas et al., 2007). Existing data on the odour composition of ripe bananas show it to be dominated by esters of acetic, butanoic and 3-methylbutanoic acid, alcohols and one ketone (Macku & Jennings, 1987). Chemical odour analysis for the above Anaxagorea spp. shows that their scents are, in fact, dominated by the same or similar esters (Jürgens et al., 2000; Teichert, 2008). Floral scent analyses for Guatteria foliosa, Duguetia stelechantha and D. trunciflora have not yet been published.

Other descriptions of ‘fruity’ Annonaceae floral scents include comparisons to ripe cajá (Spondias lutea L.), pineapple [Ananas comosus (L.) Merr.], peaches [Prunus persica (L.) Stokes] and apples (Malus domestica Borkh.). Jürgens et al. (2000) compared the scent of X. benthamii flowers to the scent of ripe fruit of S. lutea (Anacardiaceae). The chemical analysis of X. benthamii shows the scent to be dominated by methyl benzoate (38.6%), a heavy, sweet scent (Jürgens et al., 2000). A chemical analysis of the scent of ripe S. lutea fruit has shown that its scent also contains methyl benzoate, with a number of other esters, alcohols and terpenoid compounds (Augusto et al., 2000). Duguetia asterotricha and D. flagellaris Huber both have odours described as similar to ripe pineapple (Jürgens et al., 2000; Webber & Gottsberger, 2003). The floral scent composition of D. asterotricha has a relatively high concentration of terpenoid compounds, including the monoterpenes limonene, p-cymene and α-pinene, but lacks oxygenated aliphatic compounds which are prevalent in the odour of fresh pineapple (Tokitomo et al., 2005). In this case, human perception may not indicate chemical similarities between the floral scents of D. asterotricha and pineapple. However, there are a number of unidentified compounds in the floral scent of D. asterotricha (28% of the relative scent composition; Jürgens et al., 2000), and thus a comprehensive comparison of the two scent blends is not possible.

Polyalthia cf. cauliflora Hook.f. & Thomson and Duguetia pycnastera are both described as having peach-like odours, whereas Uvaria uhrii (F.Muell.) L.L.Zhou, Y.C.F.Su & R.M.K.Saunders, Guatteria duodecima Maas & Westra and an unidentified Piptostigma spp. are all described as having an ‘apple-like’ odour (Silberbauer-Gottsberger et al., 2003; Erkens, Westra & Maas, 2008; Gottsberger et al., 2011). The scent of ripe peaches is dominated by lactones (Horvat et al., 1990), and the scent of a ripe apple is dominated by α-farnesene (Matich, Rowan & Banks, 1996). It will be interesting to determine whether or not these compounds are major (or minor) components of the floral scent for these species.

CONCLUSIONS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. ECOLOGICAL AND EVOLUTIONARY ASPECTS OF FLORAL SCENT
  5. ANALYSIS AND CHARACTERIZATION OF FLORAL SCENT
  6. FLORAL SCENT CHEMISTRY AND POLLINATION IN ANNONACEAE
  7. FLORAL SCENT CHEMICAL DIVERSITY IN ANNONACEAE
  8. PERCEPTUAL DESCRIPTIONS OF FLORAL SCENT IN ANNONACEAE
  9. CONCLUSIONS
  10. ACKNOWLEDGEMENTS
  11. REFERENCES

Many of the points discussed above can only be supported with additional extensive testing, especially of species closely related to those already sampled. Currently, most genera of Annonaceae lack published descriptions of floral scent. Of the genera with some scent characterization, most have scent descriptions (chemical or perceptual) for fewer than four species. In addition, I have found no studies documenting floral scent variation within or between populations of Annonaceae. Only two genera (Asimina and Deeringothamnus) have had their floral scent analysed for all species (Goodrich & Raguso, 2009), and these genera demonstrate the potential utility of floral scent in closely related taxa when assessing shared phylogenetic history versus (or in combination with) shared ecological contexts, including pollination strategies. Future work may also focus on evolutionarily divergent taxa in shared ecological contexts. For example, the convergence of fruity, sweet scents and light floral coloration associated with beetle pollination in a common habitat type (tropical rainforest near the Manaus region of Brazil) demonstrates the ecologically informative potential of floral scent analysis (Jürgens et al., 2000). In this case, the varied composition, but similar quality, of floral scent represents the potential for convergent evolution of the same pollination syndrome in Annonaceae in evolutionarily divergent genera (Jürgens et al., 2000).

In conclusion, floral scent in Annonaceae can be highly dynamic, with variation between floral organs or ontogenetic stage (as described by Goodrich & Raguso, 2009 and Ratnayake et al., 2007, respectively), indicating the necessity for detailed spatial and temporal floral scent analyses within individual species and broad surveys across closely related species and genera. Advances in sampling and analytical techniques described earlier in this article have made it possible for such comprehensive studies. As more studies link distinctive floral scents to specialized pollination strategies in Annonaceae, it will become increasingly important to have detailed analyses of these scents; it will also become important to consider floral scent in contexts beyond pollinator attraction, including its potential role in herbivore and microbial inhibition, crypsis, pleiotropy and shared ancestry. The growing literature of floral scent analyses should lead to a better shared vocabulary of floral scent. At the very least, authors may note the presence or absence of floral scent as a potentially important component of floral display. Beyond presence/absence, it is becoming more common for authors to note qualities of floral odour, from simple descriptions of either ‘pleasant’ or ‘unpleasant’, to more detailed comparisons with commonly known scents, such as ‘bananas’, ‘pineapple’, ‘mushrooms’ or ‘carrion’. Subjective descriptions, although potentially variable and imprecise, offer extremely valuable information about overall floral display and the potential for future scent analyses. The knowledge to be gained from floral scent analyses in Annonaceae is phenomenal. All that remains is the time and enthusiasm to pursue such studies.

ACKNOWLEDGEMENTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. ECOLOGICAL AND EVOLUTIONARY ASPECTS OF FLORAL SCENT
  5. ANALYSIS AND CHARACTERIZATION OF FLORAL SCENT
  6. FLORAL SCENT CHEMISTRY AND POLLINATION IN ANNONACEAE
  7. FLORAL SCENT CHEMICAL DIVERSITY IN ANNONACEAE
  8. PERCEPTUAL DESCRIPTIONS OF FLORAL SCENT IN ANNONACEAE
  9. CONCLUSIONS
  10. ACKNOWLEDGEMENTS
  11. REFERENCES

The author would like to thank Jette Knudsen, Robert Raguso, Boris Schlumpberger and Lars Chatrou for review and helpful comments on the manuscript. She would also like to thank all of the authors who have worked to describe the floral scent of Annonaceae, whether through chemical analyses or colourful language.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. ECOLOGICAL AND EVOLUTIONARY ASPECTS OF FLORAL SCENT
  5. ANALYSIS AND CHARACTERIZATION OF FLORAL SCENT
  6. FLORAL SCENT CHEMISTRY AND POLLINATION IN ANNONACEAE
  7. FLORAL SCENT CHEMICAL DIVERSITY IN ANNONACEAE
  8. PERCEPTUAL DESCRIPTIONS OF FLORAL SCENT IN ANNONACEAE
  9. CONCLUSIONS
  10. ACKNOWLEDGEMENTS
  11. REFERENCES
  • Agelopoulos NG, Pickett JA. 1998. Headspace analysis in chemical ecology: effects of different sampling methods on ratios of volatile compounds present in headspace samples. Journal of Chemical Ecology 24: 11611172.
  • Andersson S, Nilsson LA, Groth I, Bergstrom G. 2002. Floral scents in butterfly-pollinated plants: possible convergence in chemical composition. Botanical Journal of the Linnean Society 140: 129153.
  • Andrade BM, Oliveira-Filho AT, Soares AR. 1996. Pollination and breeding system of Xylopia brasiliensis Sprengel (Annonaceae) in south-eastern Brazil. Journal of Tropical Ecology 12: 313320.
  • Armstrong JE, Marsh D. 1997. Floral herbivory, floral phenology, visitation rate, and fruit set in Anaxagorea crassipetala (Annonaceae), a lowland rain forest tree of Costa Rica. Journal of the Torrey Botanical Society 124: 228235.
  • Augusto F, Valente ALP, Tada EdS, Rivellino SR. 2000. Screening of Brazilian fruit aromas using solid-phase microextraction-gas chromatography-mass spectrometry. Journal of Chromatography A 873: 117127.
  • Baker HG, Hurd PD Jr. 1968. Intrafloral ecology. Annual Review of Entomology 13: 385414.
  • Bartelt RJ, Wicklow DT. 1999. Volatiles from Fusarium verticillioides (Sacc.) Nirenb. and their attractiveness to nitidulid beetles. Journal of Agricultural Food Chemistry 47: 24472454.
  • Braun M, Dötterl S, Gottsberger G. 2011. Absence of pollinators and apomictic fruit production in an Atlantic rainforest population of Cymbopetalum brasiliense (Annonaceae). Plant Systematics and Evolution 296: 265273.
  • Carasek E, Pawliszyn J. 2006. Screening of tropical fruit volatile compounds using solid-phase microextraction (SPME) fibers and internally cooled SPME fiber. Journal of Agricultural and Food Chemistry 54: 86888696.
  • Carvalho R, Webber AC. 2000. Biologia floral de Unonopsis guatterioides (A. D. C.) R. E. Fr., uma Annonaceae polinizada por Euglossini. Revista Brasileira de Botânica 23: 421425.
  • Chatrou LW, Pirie MD, Erkens RHJ, Couvreur TLP, Neubig KM, Abbott JR, Mols JB, Maas JW, Saunders RMK, Chase MW. 2012. A new higher-level classification of the pantropical flowering plant family Annonaceae informed by molecular phylogenetics. Botanical Journal of the Linnean Society 169: 540.
  • Couvreur TLP, Richardson JE, Sosef MSM, Erkens RHJ, Chatrou LW. 2008. Evolution of syncarpy and other morphological characters in African Annonaceae: a posterior mapping approach. Molecular Phylogenetics and Evolution 47: 302318.
  • Cox A. 1998. Comparative reproductive biology of two Florida pawpaws Asimina reticulata Chapman and Asimina tetramera Small. DPhil Thesis, Florida International University.
  • Delpino F. 1874. Ulteriori osservazioni e considerazioni sulla dicogamia nel regno vegetale. 2(IV). Delle piante zoidifile. Atti della Società Italiana di Scienze Naturali 16: 151349.
  • Dobson HEM. 2006. Floral fragrance composition and type of pollinator. In: Dudareva N, Pichersky E, eds. Biology of floral scent. Boca Raton, FL: CRC Press, 147198.
  • Dötterl S, Jürgens A. 2005. Spatial fragrance patterns in flowers of Silene latifolia: lilac compounds as olfactory nectar guides? Plant Systematics and Evolution 255: 99109.
  • Doyle JA, Le Thomas A. 1996. Phylogenetic analysis and character evolution in Annonaceae. Bulletin Muséum Nationale d'Histoire Naturelle, Paris, 4e Série, Section B, Adansonia 18: 279334.
  • Endress PK. 2010. The evolution of floral biology in basal angiosperms. Philosophical Transactions of the Royal Society B 365: 411421.
  • Erkens RHJ, Westra LYT, Maas PJM. 2008. Increasing diversity in the species-rich genus Guatteria (Annonaceae). Blumea 53: 467514.
  • Ervik F, Tollsten L, Knudsen JT. 1999. Floral scent chemistry and pollination ecology in phytelephantoid palms (Arecaceae). Plant Systematics and Evolution. 217: 279297.
  • Fekam Boyom F, Amvam Zollo PH, Menut C, Lamaty G. Bessiere JM. 1996. Aromatic plants of tropical central Africa. Part XXVII. Comparative study of the volatile constituents of five Annonaceae species growing in Cameroon. Flavour and Fragrance Journal 11: 333338.
  • Flamini G, Cioni PL, Morelli I. 2003. Use of solid-phase micro-extraction as a sampling technique in the determination of volatiles emitted by flowers, isolated flower parts and pollen. Journal of Chromatography A 998: 229233.
  • Goodrich KR, Raguso RA. 2009. The olfactory component of floral display in Asimina and Deeringothamnus (Annonaceae). New Phytologist 183: 457469.
  • Goodrich KR, Zjhra ML, Ley CA, Raguso RA. 2006. When flowers smell fermented: the chemistry and ontogeny of yeasty floral scent in pawpaw (Asimina triloba: Annonaceae). International Journal of Plant Sciences 167: 3346.
  • Gottsberger G. 1988. The reproductive biology of primitive angiosperms. Taxon 37: 630643.
  • Gottsberger G. 1999. Pollination and evolution in neotropical Annonaceae. Plant Species Biology 14: 143152.
  • Gottsberger G, Meinke S, Porembski S. 2011. First records of flower biology and pollination in African Annonaceae: Isolona, Piptostigma, Uvariodendron, Monodora and Uvariopsis. Flora 206: 498510.
  • Gürbüz O, Rouseff JM, Rouseff RL. 2006. Comparison of aroma volatiles in commercial Merlot and Cabernet Sauvignon wines using gas chromatography-olfactometry and gas chromatography-mass spectrometry. Journal of Agricultural Food Chemistry 54: 39903996.
  • Hadley NF. 1981. Cuticular lipids of terrestrial plants and arthropods: a comparison of their structure, composition, and waterproofing function. Biological Reviews 56: 2347.
  • van Heusden ECH. 1992. Flowers of Annonaceae: morphology, classification, and evolution. Blumea Supplement 7: 1218.
  • Horvat RJ, Chapman GW, Robertson JA, Meredith FI, Scorza R, Callahan AM, Morgens P. 1990. Comparison of the volatile compounds from several commercial peach cultivars. Journal of Agricultural and Food Chemistry 38: 234237.
  • Jung JH, Pummangura S, Chaichantipyuth C, Patarapanich C, McLaughlin JL. 1990. Bioactive constituents of Melodorum fruticosum. Phytochemistry 29: 16671670.
  • Junker RR, Blüthgen N. 2010. Floral scents repel facultative flower visitors, but attract obligate ones. Annals of Botany 105: 777782.
  • Jürgens A. 2009. The hidden language of flowering plants: floral odours as a key for understanding angiosperm evolution? New Phytologist 183: 240243.
  • Jürgens A, Dötterl S, Meve U. 2006. The chemical nature of fetid floral odours in stapeliads (Apocynaceae–Asclepiadoideae–Ceropegieae). New Phytologist 172: 452468.
  • Jürgens A, Webber AC, Gottsberger G. 2000. Floral scent compounds of Amazonian Annonaceae species pollinated by small beetles and thrips. Phytochemistry 55: 551558.
  • Kerner von Marilaum A. 1895. The natural history of plants; their forms, growth, reproduction and distribution. London: Blackie.
  • Kite GC, Hetterscheid WLA. 1997. Inflorescence odours of Amorphophallus and Pseudodracontium (Araceae). Phytochemistry 46: 7175.
  • Knudsen JT. 1999. Floral scent chemistry in geonomoid palms (Palmae: Geonomeae) and its importance in maintaining reproductive isolation. Memoirs of the New York Botanical Garden 83: 141168.
  • Knudsen JT, Eriksson R, Gershenzon J, Ståhl B. 2006. Diversity and distribution of floral scent. The Botanical Review 72: 1120.
  • Knudsen JT, Ståhl B. 1994. Floral odours in the Theophrastaceae. Biochemical Systematics and Ecology 22: 259268.
  • Knudsen JT, Tollsten L. 1991. Floral scent and intrafloral scent differentiation in Moneses and Pyrola (Pyrolaceae). Plant Systematics and Evolution 177: 8191.
  • Knudsen JT, Tollsten L. 1993. Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth-pollinated taxa. Botanical Journal of the Linnean Society 113: 263284.
  • Kral R. 1960. A revision of Asimina and Deeringothamnus. Brittonia 12: 233278.
  • Lee C, DeMilo AB, Moreno DS, Mangan RL. 1997. Identification of the volatile components of E802 Mazoferm steepwater, a condensed fermented corn extractive highly attractive to the Mexican fruit fly (Diptera: Tephritidae). Journal of Agricultural Food Chemistry 45: 23272331.
  • Levin RA, McDade LA, Raguso RA. 2003. The systematic utility of floral and vegetative fragrance in two genera of Nyctaginaceae. Systematic Biology 52: 334351.
  • Levin RA, Raguso RA, McDade LA. 2001. Fragrance chemistry and pollinator affinities in Nyctaginaceae. Phytochemistry 58: 429440.
  • Ma L, Zeng Y, Sun Y, Wu Z, Liu M. 1988. Studies on the aroma volatile constituents of Ylang-Ylang flowers by gas chromatography and gas chromatography/mass spectrometry. Sepu 6: 1118.
  • Maas PJM, Maas H, Miralha JMS. 2007. Floral da Reserva Ducke, Amazonas, Brasil: Annonaceae. Rodriguésia 58: 617662.
  • Macku C, Jennings WG. 1987. Production of volatiles by ripening bananas. Journal of Agricultural Food Chemistry 35: 845848.
  • Maia JGS, Andrade EHA, da Silva ACM, Oliveira J, Carreira LMM, Araújo JS. 2005. Leaf volatile oils from four Brazilian Xylopia species. Flavour and Fragrance Journal 20: 474477.
  • Majetic CJ, Raguso RA, Ashman T-L. 2008. The impact of biochemistry vs. population membership on floral scent profiles in colour polymorphic Hesperis matronalis. Annals of Botany 102: 911922.
  • Manner HI, Elevitch CR. 2006. Cananga odorata (ylang-ylang), ver. 2.1. In: Elevitch CR, ed. Species profiles for Pacific Island agroforestry. Hōlualoa, Hawai'i: Permanent Agriculture Resources (PAR), 111. Available at: http://www.traditionaltree.org (Accessed June 2009).
  • Mant J, Peakall R, Schiestl FP. 2005. Does selection on floral odor promote differentiation among populations and species of the sexually deceptive orchid genus Ophrys? Evolution 59: 14491463.
  • Matich AJ, Rowan DD, Banks NH. 1996. Solid phase microextraction for quantitative headspace sampling of apple volatiles. Analytical Chemistry 68: 41144118.
  • Momose K, Nagamitsu T, Inoue T. 1998a. Thrips cross-pollination of Popowia pisocarpa (Annonaceae) in a lowland dipterocarp forest in Sarawak. Biotropica 30: 444448.
  • Momose K, Yumoto T, Nagamitsu T, Kato M, Nagamasu H, Sakai S, Harrison RD, Itioka T, Hamid AA, Inoue T. 1998b. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant–pollinator community in a lowland dipterocarp forest. American Journal of Botany 85: 14771501.
  • Moorherjee BD, Trenkle RW, Wilson RA. 1990. The chemistry of flowers, fruits and spices: live vs. dead a new dimension in fragrance research. Pure and Applied Chemistry 62: 13571364.
  • Nagamitsu T, Inoue T. 1997. Cockroach pollination and breeding system of Uvaria elmeri (Annonaceae) in lowland mixed-dipterocarp forest in Sarawak. American Journal of Botany 84: 208213.
  • Norman EM. 2003. Reproductive biology of Deeringothamnus rugelii and D. pulchellus (Annonaceae). Taxon 52: 547555.
  • Norman EM, Clayton D. 1986. Reproductive biology of two Florida pawpaws: Asimina obovata and A. pygmaea (Annonaceae). Bulletin of the Torrey Botanical Club 113: 1622.
  • Norman EM, Rice K, Cochran S. 1992. Reproductive biology of Asimina parviflora (Annonaceae). Bulletin of the Torrey Botanical Club 119: 15.
  • Nout MJR, Bartelt RJ. 1998. Attraction of a flying nitidulid (Carpophilus humeralis) to volatiles produced by yeasts grown on sweet corn and a corn-based medium. Journal of Chemical Ecology 24: 12171239.
  • Oguntimein B, Ekundayo O, Laakso I, Hiltunen R. 1989. Volatile constituents of Uvaria chamae leaves and root bark. Planta Medica 55: 312313.
  • Pellmyr O, Thien LB. 1986. Insect reproduction and floral fragrances: keys to the evolution of the angiosperms? Taxon 35: 7685.
  • Peña JE, Castiñeiras A, Bartelt R, Duncan R. 1999. Effect of pheromone bait stations for sap beetles (Coleoptera: Nitidulidae) on Annona spp. fruit set. Florida Entomologist 82: 475480.
  • Phelan PL, Lin H. 1991. Chemical characterization of fruit and fungal volatiles attractive to dried-fruit beetle, Carpophilus hemipterus (L.) (Coleoptera: Nitidulidae). Journal of Chemical Ecology 17: 12531272.
  • Picardi SM, Issenberg P. 1973. Investigation of some volatile constituents of mushrooms (Agaricus bisporus): changes which occur during heating. Journal of Agricultural and Food Chemistry 21: 959968.
  • Pripdeevech P. 2011. Analysis of odor constituents of Melodorum fruticosum flowers by solid-phase microextraction-gas chromatography-mass spectrometry. Chemistry of Natural Compounds 47: 292294.
  • Pripdeevech P, Chukeatirote E. 2010. Chemical compositions, antifungal and antioxidant activities of essential oil and various extracts of Melodorum fruticosum L. flowers. Food and Chemical Toxicology 48: 27542758.
  • Raguso RA. 2003. Olfactory landscapes and deceptive pollination: signal, noise and convergent evolution in floral scent. In: Blomquist GJ, Vogt RG, eds. Insect pheromone biochemistry and molecular biology. The biosynthesis and detection of pheromones and plant volatiles. Amsterdam: Elsevier Academic Press, 631650.
  • Raguso RA. 2008. Wake up and smell the roses: the ecology and evolution of floral scent. Annual Review of Ecology, Evolution and Systematics 39: 549569.
  • Raguso RA, Levin RA, Foose SE, Holmberg MW, McDade LA. 2003. Fragrance chemistry, nocturnal rhythms and pollination ‘syndromes’ in Nicotiana. Phytochemistry 63: 265284.
  • Raguso RA, Pellmyr O. 1998. Dynamic headspace analysis of floral volatiles: a comparison of methods. Oikos 81: 238254.
  • Ratnayake RMCS, Gunatilleke IAUN, Wijesundara DSA, Saunders RMK. 2006. Reproductive biology of two sympatric species of Polyalthia (Annonaceae) in Sri Lanka. I. Pollination by curculionid beetles. International Journal of Plant Sciences 167: 483493.
  • Ratnayake RMCS, Gunatilleke IAUN, Wijesundara DSA, Saunders RMK. 2007. Pollination ecology and breeding system of Xylopia championii (Annonaceae): curculionid beetle pollination, promoted by floral scents and elevated floral temperatures. International Journal of Plant Science 168: 12551268.
  • Ren D. 1998. Flower-associated Brachycera flies and fossil evidence for Jurassic angiosperm origins. Science 280: 8588.
  • Richardson JE, Chatrou LW, Mols JB, Erkens RHJ, Pirie MD. 2004. Historical biogeography of two cosmopolitan families of flowering plants: Annonaceae and Rhamnaceae. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 359: 14951508.
  • Rogstad S. 1994. The biosystematics and evolution of the Polyalthia hypoleuca species complex (Annonaceae) of Malesia. III. Floral ontogeny and breeding systems. American Journal of Botany 81: 145154.
  • Saunders RMK. 2012. The diversity and evolution of pollination systems in the basal grade and ‘long-branch clade’ of the Annonaceae. Botanical Journal of the Linnean Society 169: 222244.
  • Schade F, Legge RL, Thompson JE. 2001. Fragrance volatiles of developing and senescing carnation flowers. Phytochemistry 56: 703710.
  • Schatz GE. 1985. A new Cymbopetalum (Annonaceae) from Costa Rica and Panama with observations on natural hybridization. Annals of the Missouri Botanical Garden 72: 535538.
  • Shiota H. 1991. Volatile components of pawpaw fruit (Asimina triloba Dunal.). Journal of Agricultural and Food Chemistry 39: 16311635.
  • Silberbauer-Gottsberger I, Gottsberger G, Webber AC. 2003. Morphological and functional flower characteristics of New and Old World Annonaceae with respect to their mode of pollination. Taxon 52: 701718.
  • Silva CA, Neta AMD. 2010. Aspectos reprodutivos e visitantes florais de Duguetia marcgraviana Mart. (Annonaceae) na região sudoeste de Mato Grosso. Biotemas 23: 6976.
  • Stensmyr MC, Urru I, Collu I, Celander M, Angioy A-M. 2002. Rotting smell of dead-horse arum florets. Nature 420: 625626.
  • Su YCF, Mols JB, Takeuchi W, Kessler PJA, Saunders RMK. 2005. Reassessing the generic status of Petalolophus (Annonaceae): evidence for the evolution of a distinct sapromyophilous lineage within Pseuduvaria. Systematic Botany 30: 494502.
  • Teichert H. 2008. Pollination biology of cantharophilous and melittophilous Annonaceae and Cyclanthaceae in French Guiana. DPhil Thesis, Universität Ulm.
  • Teichert H, Dötterl S, Gottsberger G. 2011. Heterodichogamy and nitidulid beetle pollination in Anaxagorea prinoides, and early divergent Annonaceae. Plant Systematics and Evolution 291: 2533.
  • Teichert H, Dötterl S, Zimma B, Ayasse M, Gottsberger G. 2008. Perfume-collecting male euglossine bees as pollinators of a basal angiosperm: the case of Unonopsis stipitata (Annonaceae). Plant Biology 11: 2937.
  • Thien LB, Azuma H, Kawano S. 2000. New perspectives on the pollination biology of basal angiosperms. International Journal of Plant Sciences 161 (Suppl): S225S235.
  • Tholl D, Boland W, Hansel A, Loreto F, Röse USR, Schnitzler J. 2006. Practical approaches to plant volatile analysis. The Plant Journal 45: 540560.
  • Tokitomo Y, Steinhaus M, Büttner A, Schieberle P. 2005. Odor-active constituents in fresh pineapple (Ananas comosus [L.] Merr.) by quantitative and sensory evaluation. Bioscience, Biotechnology and Biochemistry 69: 13231330.
  • Tuchinda P, Udchachon J, Reutrakul V, Santisuk T, Taylor WC, Farnsworth NR, Pezzuto JM, Kinghorn AD. 1991. Bioactive butenolides from Melodorum fruticosum. Phytochemistry 30: 26852689.
  • Vélez-Arango JG, Cogollo-Pacheco A. 2007. Primer registro del género Sapranthus (Annonaceae) y una nueva especie para suramérica. Caldasia 29: 229233.
  • Webber AC, Gottsberger G. 2003. Floral biology and pollination. In: Maas PJM, Westra LYT, Chatrou LW, eds. Duguetia (Annonaceae) monograph, flora neotropica, Vol. 88. New York: New York Botanical Garden Press, 5053.
  • Whitten WM, Williams NH, Armbruster WS, Battiste MA, Strekowski L, Lindquist N. 1986. Carvone oxide: an example of convergent evolution in euglossine pollinated plants. Systematic Botany 11: 222228.
  • Willson MF, Schemske DW. 1980. Pollinator limitation, fruit production, and floral display in pawpaw (Asimina triloba). Bulletin of the Torrey Botanical Club 107: 401408.
  • Wright GA, Schiestl FP. 2009. The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signaling of floral rewards. Functional Ecology 23: 841851.