148 AROIDEANA, Vol. 27 Pollination in the -a Review

Marc Gibernau*, David Macquart, and Gilles Przetak Laboratoire d'Evolution & Diversite Biologique Unlversite de Toulouse m 118 Route de Narbonne, Bat. IV R 3-B 2 31062 Toulouse Cedex 4 *e-mail: [email protected]

ABSTRACT KEYWORDS , pollinators, inflorescence, ther­ The 28 of the genus Arum (Ar­ mogenesis, floral odor, morphology, Ara­ aceae) attract and temporarily trap ceae. (mainly , and beetles in a few cases) during a complex pollination process. At INTRODUCTION anthesis, the appendix of the inflorescence produces heat and emits a specific odor History which attracts insects. The lured insects Arum have been known since Antiquity are trapped within the floral chamber (, Pliny and Dioscorides). when stigmas are receptive. They will be The description "Arum oificinarum" ap­ released about 24h later after emis­ peared during the Middle-Ages because of sion, ensuring pollen dissemination. Stud­ their medicinal properties, but this term ies on the reproductive biology of the ge­ designated all kinds of aroids for about nus have shown some degree of variability four centuries (Prime,1960; Fridlender, in the pollination strategies: morphological 1999a). During this period several authors variations, flowering and heating periods, dealt with Arum (see Croat, 2000 for more odor types and the type of pollinating in­ details). The binomial name Arum macu­ sects. latum is attributed to Tabernaemontanus Most species of Arum have never been around 1590, but it has been used with a studied in depth but data available from taxonomic "value" only after the classifi­ the literature indicate quite a high diversity cation work of Linnaeus in 1753 (Boyce, of pollination strategy within this genus. 1993). Hundreds of species were given the name of Arum, most of them later to be Consequently, a general pollination model defined as new genera of , for ex­ is not valid at the level of the whole genus. ample Arum tenuifolium is the type spec­ The origin of this diversity certainly results imen for the genus Biarum described in from the biogeographic history of the ge­ 1832 by Schott (Boyce, 1993; Mayo et al., nus. The (Le. species) have devel­ 1997). Following , the oped adaptations in response to different second valid species was A. italicum, de­ climatic, ecological and biotic (i.e. ento­ scribed in 1768 by Miller (Table 1), and mofauna) constraints (Le. selective pres­ later Linnaeus f. described A. pictum in sures) according to the various habitats oc­ 1782. During the 19'h century, period of cupied in the different regions of Europe oriental expeditions, many species were and the Middle East. However, in the ab­ described from the East and the Mediter­ sence of phylogenetic data, it is actually ranean (Table 1). More recently, 7 new impossible to determine how these differ­ species have been described in the last 23 ent reproductive strategies have devel­ years (Boyce, 1993, 1994, 2004). Today, oped and evolved during the history of the genus Arum is considered to have 28 this genus. species (Boyce, 2004). M. GIBERNAU, D. MACQUART, G. PRZETAK, 2004 149

Table 1. History of species descriptions for the genus Arum (Boyce, 1993, 2004) Date Species Author Odor 1753 A. maculatum Linnaeus Faecal/urine 1768 A. italicum Miller Urine/faecal 1782 A.pictum Linnaeus fil. Dung/pungent 1808 A. orientale" Bieberstein Dung/urine Rotting/fermenting fruit 1816 A. dioscoridiS' Smith Dung/carrion I Ammonia? 1836 A. byzantinum Blume Urine/putrid% 1836 A. jacquemontii Blume No perceptible 1844 A. cylindraceum Gasparr Putrid23 1845 A.longispathum Reichenbach Dung 1853 A. rupicola Boissier No perceptible 1853 A. hygrophilum Boissier No perceptible (swee~) 1853 A. palaestinurrt Boissier Rotting/fermenting fruit Dung/carrion 1853 A. creticurrt Boissier & Heldreich Sweet-rotting ("Freesia") Naphthalene mothballs 1856 A. gratum Schott Sweet ("pear drops") 1857 A. nigrum Schott Dung 1857 A. elongatum Steven Dung 1858 A. besserianum Schott Fermenting fruit% 1859 A. concinnatum Schott Putrid/urine 1877 A. korolkowii Regel No perceptible 1912 A. cyrenaicum Hruby Dung 1917 A. idaeum Cousturier & Gandoger No perceptible/sweet% 1981 A. hainesii Agnew & Hadac ??? 1983 A. euxinum Mill No perceptible 1983 A. balansanum Mill "Acidic apple" 1984 A. apulum Bedalov Dung 1987 A. purpureospathum Boyce Dung 1994 A. sintenisii Boyce Rotting/fermenting fruit 2004 A. alpinariae Boyce Dung% • Several chemotypes exist each with different odors (Koach, 1985; Feibrun-Dothan, 1986; Boyce 1993; Drummond & Hammond, 1991, 1993). % Light odor perceptible close to the inflorescence. I Var. syriacum: odor not perceptible (Boyce, 1993). 2 As synonym of A. lucanum: odor of dung/plasticine (Drummond & Boorman, 2003). 3 As synonym of A. alpinum: odor not perceptible (Boyce, 1993).

Interestingly, in parallel with the taxo­ anists discovered that the "Farina Fecun­ nomic work of species description, there denS' produced by the stamens and the was a progressive discovery of insect pol­ stigma were necessary to set seeds, and lination. In their 1996 book, Proctor, Yeo the first cross hand-pollinations were per­ & Lack describe the work of Camerarius, formed. During the second half of the 18th Bradley, Miller, Logan and others during century biologists such as Dobbs and K61- the first half of the 18th century, when bot- reuter discovered that insects, and partic- 150 AROIDEANA, Vol. 27 ularly bees, visited flowers in search of The Genus Arum nectar and incidentally were carrying the The genus Arum is composed of 28 spe­ "Farina", and thus were pollinating agents cies, largely distributed in Europe, North for numerous flowering species Africa, Middle East and Central Asia (Boy­ (Proctor et al., 1996). During this period, ce, 1993; Mayo et at., 1997). It is divided Lamarck (1778) discovered the heat pro­ into two sub-genera: the sub-genus Arum duced by spadices of Arum italicum. which contains all the species except one, Sprengel (1793) produced the first system­ Arum pictum, which belongs to the sub­ atic study of insect pollination on about genus Gymnomesium due to the timing of 500 plant species and described several its flowering (autumn instead of spring) pollination mechanisms, in particular flow­ and morphological characters of its sterile ers which temporarily trap insects (e.g. flowers and leaves. Aristolocbia). Many Arum species are pollinated, or at Sixty years later (1857-1876), Darwin least visited, by saprophilous or coproph­ studied the plant variation and insect pol­ ilous insects, mainly flies and beetles lination systems (particularly self-pollina­ (Boyce, 1993; Kite et at., 1998; Gibernau, tion avoidance) within the frame of his 2003). Arum inflorescences attract and theory of natural selection. At this time, trap the insects by mimicking the odor of Hildebrand (1867) wrote the first book on their laying site (e.g. decaying organic floral biology, followed by Delpino (1868) matter or faeces). Thus the insects are who proposed a flower classification (two lured by the inflorescence when pollinat­ volumes) based on different floral types in ing and gain no reward from this interac­ relation to pollination. Delpino studied nu­ tion (Proctor et at., 1996). merous pollination mechanisms, including those of Arum italicum and in 1870 of A. Inflorescence Morphology macutatum. In the same way, Muller The morphology of the Arum inflores­ (1873) wrote three books on plant-polli­ cence is characteristic, made up of a nator-insect relationships, describing many spathe and a spadix. The spathe is the fo­ pollination mechanisms, including Arum liar organ around the spadix. The spadix macutatum. In 1883, Arcangeli described is the central axis bearing the small uni­ the pollinating fauna of Arum italicum sexual flowers. and in 1886 he studied Arum pictum. The spathe is a modified . Its basal Knuth (1898--1905) wrote a handbook (3 part forms a tube around the fertile part of volumes) on flower pollination in which the spadix, called the floral chamber, Arum italicum, A. maculatum, A. pictum which is closed at its top by hairs derived and A. dioscoridis are cited. The under­ from sterile male flowers (Barabe et al., standing of the insect trap mechanism was 2003). The upper part of the spathe opens at anthesis and looks like a limb above a elucidated 40 years later thanks to exper­ constriction zone. After pollination, the imental studies of the pollination of Arum spathe wraps around the spadix protecting maculatum and A. nigrum (Schmucker, the developing fruit (Le. the infructesc­ 1925; Knoll, 1926). These studies showed ence). the role of the appendix, the hairs and the The spadix is divided in two zones, the floral chamber in attracting and capturing basal fertile zone where the flowers are lo­ the insects, and also in seed production. cated within the floral chamber and the During the last 60 years, only the pollina­ upper sterile zone, the appendix. Within tion of Arum macutatum has been stud­ the fertile zone, fertile female flowers (i.e. ied, and this only in England. Nevertheless ovaries) are situated at the bottom, above the genus Arum is the most documented them are sterile female flowers looking among Araceae in relation to pollination like hairs (Le. pistillodes), still higher are (Gibernau, 2003). the fertile male flowers (i.e. stamens), and M. G IB ERNAU, D. MACQUART, G. PRZETAK, 2004 151

finally male sterile fl ower also looking like Day Night hairs (i. e. staminodes). The appendix is a sterile organ situated at the apex of the spadix. It can develop heat and emits the cf A pendix volatile compounds attracting the pollin at­ ing insects. In Aru.m italieu:m, the longer the appendix, the more insects it w ill at­ ~Feilemal C tract (Mendez & Obeso, 1992), and the higher w ill be the numbe r of fruits initiated (Mendez & Diaz, 2001). In A. maeulatwn, Time if the appendix is removed, few Psyehoda Fig. l. Thermogenic pattern on Arum are caught and o nl y 20% of the infl ores­ maeulatum and A. italicum with four pe­ cences are visited (Lack & Diaz, 1991). The ri ods of heat. Two heating events occur same result had been fo und in infl ores­ before the spathe unfolding by the male cences of A. hygmpbilum with no appen­ fl owers (D - 1 & D), another on the first dix (Koach , 1985).The appendix loss (i.e. day of anthesis by the appendix (D even­ by predation) diminishes the fruit and ing), and the last on the second day of seed productions in A. italleum and A. anthesis, again by the male fl owers (D + maeulatum (Lack & Diaz, 1991; Mendez 1). & Obeso, 1992). On the other hand, the appendix is not absolutely necessary sin ce 40% of the A. italieum with no appendix phase) starts and finishes before pollen produce seeds (Mendez & Obeso, 1992), liberation (male phase). This trait implies and in A. maculatum, inflorescences still that inflorescences ca nnot self-pollinate produce a reduced seed set (Lamb, 1956; (i. e. with their own po llen). Insects are Lack & Diaz, 1991). trapped w ithin the fl oral chamber during the time between the two sexual phases Cryptic and Flag Species Each inflorescence produces four peri­ ods of heat during anthesis (Fig. 1). The Boyce (1993) distinguished two inflores­ first two are due to the male fl owers. The cence types w ithin the genus Antm. The first occurs on the day before the spathe species in which the inflorescence is o pens (Albre et al., 2003), the second on borne on a short peduncle and in this way the day of the spathe opening (S kubatz et is situated amid or below the leaves, are al., 1990; Bermadinger-Stabentheiner & called "Clyptic" species. On the other Stabenthe iner, 1995). A temperature in­ hand, species where the inflorescences are crease is perceptible at 9 A.M., several above the leaf level at the end of long pe­ hours before the opening of the inflores­ duncles are call ed "fl ag" species. We w ill cence in A. italicum (Arcangeli, 1886). see later that these two kinds of species These two heating events are not related have different re productive biology. to insect attraction but may rather be in­ Among the most studied species, Arum volved in the actu al unfo lding of the macula tum, A. italicum, A. dioscoridis, A. spathe (Fig. 1). palaestinum, and A. idaeum are all "cryp­ On the day of spathe opening, a third tic" species, w hile Aru.m rupicola, A . by­ heating event occurs during the evening, gmphilum and A. cretieum are "fla g" spe­ but it is produced by the appendix (Fig. cies. 1). This heating event is related to the phase of insect attracti on and enhances POLLINATION CYCLE the volatilisation of the odoriferous volatile compounds (Kno ll , 1926; Bermadinger­ Cycle Steps Sta bentheiner & Stabentheiner, 1995; Kite, Arum inflorescences are protogynous: 1995). Insects are mainly attracted by the the period of stigma receptivity (female scent, and visual cues of the spadix con- 152 AROIDEANA, Vol. 27

Stigma receptivity

\ Female phase ------,- - -- Male

Pollen

Fruit maturation

Fig 2. Biological cycle of Psychoda midges (left side of the vertical line), pollination of Arum cycle with capture of lured midges (right side of the vertical line). trast against the spathe are secondary until the male phase on the next day when (Knoll, 1926; Lamb, 1956; Prime, 1960; pollen release occurs. The chamber wall is Lack & Diaz, 1991; Kite et al., 1998). Once constituted of a spongy mesophyll (Le. attracted, the insects fall or enter into the loosely packed cells) coupled with nu­ floral chamber where they are trapped merous stomata on the external wall sur­ (Fig. 2). The upper hairs, which are mod­ face (Knoll, 1926; Beck, 1983; Bermadin­ ified sterile male flowers, located at the en­ ger-Stabentheiner & Stabentheiner, 1995). trance of the floral chamber, are supposed This structure of the wall tissue may facil­ to prevent the insects from escaping out itate the oxygen transfer necessary for in­ and "huge" invertebrates from entering in, sect respiration, but also may be of value and/or to reduce light entrance (Knoll to respiration of the male flowers of the 1926; Dormer, 1960; Lack & Diaz, 1991; spadix during heating events, particularly Fridlender, 1999b). Large dung flies have when the spathe is still closed. Moreover, been observed to alight on the spadix of in particular dry conditions, the relative A. maculatum and A. nigrum, but not go humidity of the floral chamber can remain further down (Church, 1908; Knoll, 1926; high independent of the external condi­ Dormer, 1960). tions (Knoll, 1926). In Israel, the mortality During their stay in the floral chamber, of Psychoda cinerea, pollinator of A. hy­ insects may deposit pollen on the stigma, grophilum, is limited thanks to the humid­ if they already carry some. Female flowers ity of the floral chamber, thus this may be are receptive at this time and their stigmas of adaptive value in arid habitats (Koach, have a drop of secretion, enhancing pol­ 1985). len collection. The conditions within the During the second day of anthesis, the floral chamber allow the insect to survive fourth heat event is produced by the sta- M. GIBERNAU, D. MACQUART, G. PRZETAK, 2004 153 mens (Fig. 1) and may be related to the captured in the floral chamber, which are anther opening and pollen release (Ber­ not necessarily efficient pollinators (Giber­ madinger-Stabentheiner & Stabentheiner, nau, 2003). For example Arum macula­ 1995; Albre et al., 2003). At this stage, the tum inflorescences captured many insect cells of the appendix, the epidermis of the species, 56 recorded in and at floral chamber and the spadix are no lon­ least 13 in England but the main pollinator ger turgid and slippery, and the hairs have is only Psychoda phalaenoides (Grensted, wilted. Insects are able to walk up the flo­ 1947; Beck, 1983; Diaz & Kite, 2002). In ral chamber and to escape loaded with the same way in A. italicum, at least 9 in­ pollen (Knoll, 1926; Prime, 1960; Beck, sect species are captured but only two are 1983; Bermadinger-Stabentheiner & Sta­ efficient pollinators and two others may be bentheiner, 1995). If these insects are cap­ opportunist secondary pollinators (Albre tured again by a female stage inflores­ et al., 2003). In Crete, at least 21 species cence, they may deposit pollen on the re­ of insects visited inflorescences of A. cre­ ceptive stigma, but the insect capture must ticum, but only the bruchid beetles (5 spe­ occur in the two days following their es­ cies) seemed to be active enough and cape, as Arum pollen qUickly loses its vi­ coated with enough pollen to be pollina­ ability (Gibernau et al., 2003). In A. ma­ tors (Drummond & Hammond, 1993). The culatum, about 25% of the Psychoda cap­ larger scarabs were coated with much tured are attracted for the first time and more pollen, but remained quiescent at thus carry no pollen (Lack & Diaz, 1991). the bottom of the spathes (Drummond & Moreover, a Psychoda can only visit one Hammond, 1993). In A. nigrum, 50 spe­ inflorescence on a given day because of cies of insect are attracted by the inflores­ the trap mechanism. Thus, an inflores­ cences but only 4-5 species may be effi­ cence must attract a maximum of insects cient pollinators (Knoll, 1926). in order to have a high probability of pol­ lination and thus set seed, and conse­ Thermogenesis quently will have a "good" pollen dissem­ ination on the following day. On the other This question has been reviewed by Bay hand, the fruiting success of A. macula­ (995): in summary the thermogenic pro­ tum did not appear to be related to the cess is triggered by the alternation of light number of insects trapped, as if just one and dark, which stimulates the primordia midge carrying pollen was necessary for a of the male flowers. As a result, the male full fruit set (Lack & Diaz, 1991). flowers produce salicylic acid, which act as a calorigen hormone by stimulating The Pollinators thermogenic reactions. In Arum, there are two spadix zones (the male flowers and Pollinators are documented for 15 spe­ the appendix) which produce heat at dif­ cies in their natural habitats, about half the ferent moments of anthesis. In summary genus, plus three species in culture out of (see the previous section "cycle step"), the their distribution (Table 2). Arum species thermogenic pattern in Arum is tetra phasic are mainly pollinated and visited by flies: (Fig. 1). Two heating events occur before Nematocera (Psychodidae, Ceratopogoni­ the spathe unfolding, by the male flowers, dae, Chironomidae) and also Brachycera another on the first day of anthesis by the (Sphaerocerldae, Drosophilidae, Scato­ appendix, and the last on the second day phagidae). Visiting insects can also be of anthesis, again by the male flowers. beetles (Staphylinidae, Bruchideae, Scara­ If temperature increases have been ob­ baeideae) for a few species (Table 2). served in many Arum species, in fact few Except for four species, namely A. ma­ actual temperature measurements are culatum, A. italicum, A. nigrum and A. available. The heat production by the ap­ hygrophilum, data on pollination are ac­ pendix appears to be the most spectular tually observations or samples of insects of the four heating events. In A. italicum 154 AROIDEANA, Vol. 27

Table 2. Major insect taxa found in inflorescences of different species of Arum (in bold most abundant taxa). Unless noted, the insects are mainly fe- males. (=) indicates that caught insects are about half males and half females . .. plants in culture out of their natural distribution area. Species Country Main pollinators A. maculatum England Psychoda phalaenoides, P. grisescens, P. brevicornis Smitt pratorum (Piophila vulgaris) A. maculatum Germany Psychoda phalaenoides, P. grisescens A. italicum neglectum England Psychoda phalaenoides, Smittia pratorum A. italicum italicum England Psychoda phalaenoides, P. grisescens A. italicum italicum Psychoda nervosa, Limosina pygmaea, Ceratopog pictellum, Chironomus byssi- nus, Drosophila junebris A. italicum italicum France Psychoda crassipenis, P. pusilla A. italicurrt' Israel· Psychoda cinerea A.pictum Italy Sphaerocera equinus, Aphodius melanos- tictus A. orientale (named petten) Yugoslavia Coproica jerruginata, clunipes A. orientale Atheta trinotata, Atheta sp (D, Drosophila subobscura (=), busckii (=), D. hydei (=) A. dioscoridis Turkey Anotylus clypeonitens, A. inustus, Atheta atramentaria A. dioscoridis Cyprus Coproica vagans, C. jerruginata, Anotylus inustus A. dioscoridis Lebanon Scatophaga stercoraria, S. maculipes, Phi- lonthu intermedius, Oxytelus sculptura- tus, Onthophagus ovatus, ... A. dioscoridis Israel , Staphylinidae, Scarabaei- deae A. dioscoridis" England" Dung insects A. concinnatum Crete Coproica jerruginata, Spelobia sp., Anoty- Ius inustus, Athe coriaria A. concinnaturrt' England" Psychoda phalaenoides, Smittia sp. A. nigrum Croatia Aphodius tristis, Sphaerocera subsultans, S. pusilla, equinus Coprophila pusilla A. creticum Crete Bruchidius spp., Tropinota hirta, Aplo- cnemus spp. Heteroptera, Melyridae A. idaeum Crete Bruchidae, Melyridae, Mordellidae Heter- optera A. rupicola (named elonga- Israel Culicoides circumscriptus, C. cataneii tum) A. rupicola (named cono- " Culicoides aricola, Odagmia ornata phalloides)" A. rupicola* England" Culicoides brunnicans, C. vexans, C. punctatus, C. pulicaris A. hygrophilum Israel Psychoda cinerea CD, Tinearia alternata (D A. hygrophilum Lebanon Sciria advena M. GIBERNAU, D. MACQUART, G. PRZETAK, 2004 155

Table 2. Continued. Species Country Main pollinators A. jacquemontii" England· Culicoides brunnicans, C. obsoletus, Simu- lium ornatum A. palaestinum1 Israel Drosophila phalerata (=), D. immigrans (=), D. hydei (=), melanogaster(=), D. simulans (=) A. palaestinurJi2 Israel Flies & beetles A. purpureospathurrt England" Copromyza equina, Smittia sp., C. similes, P. phalaenoides A. gratum Turkey Psychodidae A. apulum Italy Sphaeroceridae, Chironomidae A. apulum* England" Psychodidae, Chironomidae, Sphaeroceri- dae A. cylindraceurrt (named England" Psychodidae, Culicidae lucanum) A. cyrenaicurrt England" Nematocera A.euxinum Turkey Psychodidae, Sphaeroceridae

1 Ecotype with fermenting fruit odor. 2 Ecotype with dung/carrion scent.

and A. maculatum, the appendix be­ batz et al., 1990). By contrast, male flowers comes as much as 15-25°C warmer than and the appendix of A. dioscoridis are the surrounding air (Lamarck, 1783; Kraus, highly thermogenic, 9-10°C above ambi­ 1882; Arcangeli, 1886; Church 1908; Prime, ent, some spadix part reaching 40°C 1960; Skubatz et al., 1990; Bermadinger­ (Koach, 1985; Skubatz et al., 1990). Stabentheiner & Stabentheiner, 1995; Albre The hypothesis of pollinator attraction et al., 2003). During anthesis, and partic­ by the heat production has been tested in ularly during the heat production by male Arum nigrum. Heated artificial inflores­ flowers, the floral chamber of A. italicum cences did not capture significant number and A. maculatum is about I-3°C warmer of pollinating insects, whereas artificial in­ than the external air (Church, 1908; Sow­ florescences with a smell were attractive ter, 1949; Prime, 1960; Bermadinger-Sta­ (Knoll, 1926 ; Dormer, 1960). A second ex­ bentheiner & Stabentheiner, 1995; Albre et periment on Psychoda phalaenoides, the al., 2003). main pollinator of Arum maculatum, was Apart from A. italicum and A. macula­ performed more recently. Glass tubes lOoC tum, incomplete data are available for a warmer than ambient air simulated warm few species. In Arum rupicola, the spadix inflorescences, but no insects were attract­ maintained a temperature of around 40°C, ed (Kite et al., 1998). about 15-20°C above ambient air from 17h Thus, the main role of the thermogenic to 23h and then began to fall (Koach, process (at least for the appendix) appears 1985; Drummond & Hammond, 1993). In to be the dispersion in the air of the scent­ A. jacquemontii, the spadix temperature ed compounds, rather than to attract the was 36.4°C at 18h 40 compared to an am­ insects because of the warmth. In addition, bient of 15.2°C and gave no discernible the thermogenic activities of the male odor (Drummond & Hammond, 1993). flowers are not linked with pollinator at­ Arum palaestinum and A. creticum are traction, but may be related to spathe un­ weakly thermogenic with just a few de­ folding, physiological processes such as grees above ambient (Koach, 1985; Sku- pollen maturation, insect warming or pol- 156 AROIDEANA, Vol. 27 len release (Barabe et al., 2002; Albre et (where the female flowers are located). al., 2003). In fact, this is because the floral cham­ ber wall is bicoloured: dark purple in its VARIATIONS IN THE REPRODUCTION upper part (opaque) and pale green BIOWGY (translucent) in its lower part. This floral chamber wall characteristic is also ob­ According to the species of Arum, dif­ served in A. orientale, A. rupicola, A. ferences in the pollination mechanism are purpureospathum and A. elongatum, of greater or lesser importance. Those dif­ but not in A. maculatum, A. italicum, ferences are related to the inflorescence A. concinnatum or A. cylindraceum. morphology, the thermogenesis, the inflo­ rescence odor, the type of pollinators but Arum creticum and A. idaeum, two these variations may also occur within a closely related species native to Crete, are species. The geographical variation in A. the only species with no hairs blocking the maculatum is a well known, for example, entrance of the floral chamber (Boyce, in the presence of spots, the plant size, 1993). Interestingly, A. idaeum and A. cre­ dextrallsinestral spathes or the yellow ap­ ticum have similar, if not the same, polli­ pendices, even if there is not always a nators; and are the only Arum species to "logical" pattern (Prime, 1960). be pollinated principally by beetles (Drummond & Hammond, 1993; Drum­ Modes of Capture mond & Boorman, 2003). This lack of "closing hairs" may be related to the pol­ Differences exist in the capture method linators. Beetles are relatively strong in­ between Arum maculatum and A. nigrum sects, able to sneak in through small open­ (Knoll, 1926; Dormer, 1960; Boyce, 1993). ings thanks to their smooth body and such Both species attract several different in­ hairs would be, in fact, inefficient in hold­ sects including Psychoda, but these insects ing them. Interestingly, A. diosocoridis, in do not behave similarly. In A. maculatum, Lebanon, is mainly visited by 7 species of insects in a spiral around the appendix beetles and two species of flies (Scatopha­ and the spadix and then land on the spa­ ga). All the beetles were able to move eas­ dix or the staminodes (hair modified male ily up and down from the floral chamber, sterile flowers), before they walk down only the Scatophaga flies seemed to be into the floral chamber. In A. nigrum, on held inside the floral chamber by the hairs the other hand, pollinators try to land on (modified sterile flowers) (Kullenberg, the spathe which is slippery due to oily 1953). secretions, and fall down into the floral It has been suggested that in general the chamber. pollinating insects collect the stigma secre­ Insects are hypothesized to remain cap­ tion and from this get some kind of food tured in the floral chamber of A. nigrum (Prime, 1960). But Lack & Diaz (1991) stat­ for three reasons (Knoll, 1926): ed that such behaviour was never ob­ • The upper part of the floral chamber served in Psychoda phalaenoides, polli­ and the spadix epidermis are slippery nator of Arum maculatum. These authors preventing insects from walking up­ suggest that the stigmatic secretions were wards the exit. not nectar (Le. produced to feed the in­ • The insects do not try to fly because the sects) but a fluid favourable for the adher­ volume of the floral chamber is not suf­ ence and the germination of the pollen. ficiently large to stimulate flying behav­ Moreover, such secretion is produced on iour. the second day of anthesis even if female • The main light source coming from be­ flowers are no longer receptive and, by low and the insects being positively getting onto the trapped insects, may en­ light sensitive, they might remain near hance pollen adhesion to their bodies the lower part of the floral chamber (Lack & Diaz, 1991). However, in A. itali- M. GIBERNAU, D. MACQUART, G. PRZETAK, 2004 157 cum, the stigmas are devoid of such se­ days with inflorescences already open cretion during the second day of anthesis (Mendez & Diaz, 2001). In the same way, (Albre et al., 2003). In any case, it has it appears that A. maculatum flowering at been suggested that Psychoda species are the beginning or the end of the flowering not known to feed during their short adult period, when few other inflorescences are life (Withers cited in Lack & Diaz, 1991), open, have a lower probability to fructify which is up to 7 days for P. phalaenoides than those flowering at the flowering peak (Prime 1960; Withers, 1988), and about 5 (allerton & Diaz, 1999). Consequently, se­ days for P. cinerea, P. trinodulosa and P. lection tends to synchronize flowering in parthenogenetica (Lachmann et al., 2000). A. maculatum, but the "mean" date fluc­ It is worth noting that adult P. trinodulosa tuates every year due to variable weather died when deprived of sugary water conditions (allerton & Diaz, 1999). In a whereas P. cinerea and P. parthenogene­ year with "good" weather conditions, tica survived but had a lesser reproductive flowering of A. maculatum is generally success (Lachmann et al., 2000). In Arum synchronised with Psychoda flight abun­ hygrophilum, the stigmatic fluid helps the dance and a high fruit set occurs; whereas pollinators (Psychoda cinerea) to survive with "bad" weather the flowering may be longer when in the floral chamber (Koach, delayed, the Psychoda flight activity re­ 1985). This fluid may help in maintaining duced and few fruits are produced (Kite et a humidity rate appropriate for the insects al., 1998). Hence, the reproductive suc­ and also represent a food source. Psycho­ cess of A. maculatum and A. italicum ap­ da cinerea fed with an aqueous solution pears to be pollen and pollinator limited. (5% sucrose) which is similar in composi­ The flowering phenology is unimodal tion to the stigmatic fluid, survive twice as (Le. a peak) in A. italicum and in A. ma­ long as those fed with only water (Koach, culatum, with inflorescences lasting a few 1985). In comparison, the fluid produced days (Le. anthesis of about 24h) and with­ by stigmas from A. maculatum, had a con­ ering quickly after anthesis (Mendez & centration of sucrose eqUivalent of 9- Obeso, 1992; allerton & Diaz, 1999; Men­ 12.5%, which was slightly more concen­ dez & Diaz, 2001). Two exceptions are trated than 8% sucrose equivalent of the known for which inflorescences do not fluid exuded from the phloem of cut stems fade and wither rapidly, but retain their (Lack & Diaz, 1991). Finally, during the fresh appearance for several days after the rearing of Psychoda captured in inflores­ spathe fully opened: about 7 days in A. cences of Arum italicum, the individuals creticum (Drummond & Hammond, 1993) were regularly observed to feed on 5% and 9-10 days in A. hygrophilum (Koach, sugary water (Albre, pers. comm.). 1985). Once again, a long inflorescence duration in A. creticum may be related to Reproduction beetle pollination. In A. italicum, it has been shown that The reproductive system has been in­ the sexual reproduction has a somatic tensively studied in only two species, cost, as tubers of reproductive plants grow namely A. maculatum and A. italicum. 30% less than non-reproductive plants. The reproductive success depends on the This cost can be lower by temporal coin­ flowering and pollination contexts: num­ cidence between leaves and inflorescenc­ ber of individuals, their density, the weath­ es/infructescences (Mendez, 1999). Arum er, the phenology, the pollinator abun­ italicum with tubers lighter than 2.5g do dance (allerton & Diaz, 1999; Mendez & not reproduce, whereas those with a tuber Diaz, 2001). Inflorescences which opened over 109 will reproduce each year (Men­ on days with no other inflorescences al­ dez & Obeso, 1993). In A. maculatum, a ready open (Le. potential pollen donors) size factor also exists since the tuber will have a probability up to 45% lower to fruc­ not flower until they reach a weight of ap­ tify than inflorescences which opened on proximately 109 (Prime, 1960). When its 158 AROIDEANA, Vol. 27 vigour increases (Le. the mass), a plant conditions. Thus cross-pollination by in­ tends to produce more inflorescences sects is necessary in order to set seeds. But which are bigger and bear more flowers self-compatibility allows geitonogamous (Mendez & Obeso, 1993; Mendez, 1998). pollination, that is pollination between in­ An individual of A. italicum with several florescences of a same individual or clone, inflorescences has a higher probability to to be successful in A. maculatum and A. fructify than plants with only one inflores­ italicum (Diaz & Gibernau, unpubl. data), cence (Mendez & Obeso, 1992; Mendez & even though the contrary was previously Diaz, 2001). In the same way, the inflores­ reported (Lack & Diaz, 1991). cence size (Le. mass) is positively related to the size of the appendix and the num­ Pollinators bers of flowers (Mendez, 1998; Mendez, 2001). On the other hand, the rank of de­ The type of the main pollinator/visitor velopment of the inflorescence (e.g. order varies according to the species (Table 2). of inflorescence appearance) appears to There are five main types of pollination be important, since inflorescences with a agents: Psychodids (5 Arnm species), higher rank (e.g. second or third inflores­ Sphaerocerids (2 Arnm species plus 5 in cences) tend to be smaller and to bear less association with Staphylinids), Drosophil­ flowers (Mendez, 1998). ids (2 Arnm species), Ceratopogonids (2 In A. italicum, it seems that two func­ Arnm species) and Bruchids/Melyrids (2 tional reproductive strategies occur (Men­ Arnm species). The three first types of pol­ dez, 1998). In fact, the reproductive out­ lination systems mimic the laying sites of come of individuals producing only one their pollinators, respectively decaying inflorescence is, on one hand abortion matter, dung and rotting fruit. In the fourth with no seed set but pollen dispersion, pollination system (Ceratopogonids), the and on the other hand seed production but with a low pollen dispersion. The re­ inflorescences imitate the insect host/prey. sult is like a gender specialisation of the Due to the lack of data, it is unclear if the inflorescence as functionally male or fe­ last pollination system mimics a reproduc­ male. On the contrary, plants producing tive or an alimentary site. two inflorescences do not tend to be male/ Recently, a study showed that Arnm female specialised, but are relatively as maculatum is frequently visited by fe­ successful in pollen dispersion (Le. male) males of Smittia pratornm, a terrestrial as in seed production (i.e. female) (Men­ chironomid whose larvae develop in wet dez, 1998). soil (Diaz & Kite, 2002). Nevertheless, this Another important reproductive charac­ species is not a major pollinator because ter is self-compatibility. Self-pollination is they carry very few pollen grains, proba­ rare in Arnm, inflorescences bagged be­ bly because of their less pubescent bodies. fore their opening abort in A. italicum (Al­ They may be attracted not by the faeces/ bre et al., 2001), A. maculatum (Lamb, urine odor but by the stigma exudates on 1956; Prime, 1960; Lack & Diaz, 1991), A. which they feed (Diaz & Kite, 2002). In nigrnm (Knoll, 1926; Dormer, 1960) and Germany, 56 insects species were trapped A. bygropbilum (Koach, 1985). In contrast in floral chambers of A. maculatum of Fridlender (1999b) report that in A. cylin­ which 94% were psychodid midges (Beck, draceum, individuals from small popula­ 1983; Rohacek et al., 1990). The main pol­ tions were self-fertile whereas individuals linators are females of Psycboda pbalae­ from big populations were unable to self­ noides (93.5%) and of P. grisescens (5.3%). pollinate. According to Ollerton & Diaz It's worth noting that even if P. grisescens (1999), Arnm maculatum is self-compati­ globally represents a small portion of the ble, but because of the delay between the total midges trapped, in some populations female and male phases (Le. protogyny), this species constitute up to half of the self-pollination is extremely rare in natural psychodids (Beck, 1983). Such variation M. GIBERNAU, D. MACQUART, G. PRZETAK, 2004 159 has also been observed in England (Proc­ licoides was also trapped in rare occasions tor et al., 1996). in A. maculatum (Beck, 1983) Pollinator variations can also occur These different kinds of interactions un­ among years. In A. maculatum, a popu­ derline different mechanisms and adapta­ lation normally pollinated by Psychoda tions of Arum species in order to achieve phalaenoides, flowered three weeks later their sexual reproduction by trapping local during a year with bad weather conditions insects. and was visited by Piophila vulgaris but had a low fruit set (Kite et al., 1998). Thermogenesis In England, A. maculatum and A. ital­ While almost all the species studied are icum subsp neglectum both attracted known to produce some heat, this char­ mainly female Psychoda phalaenoides and acter varies among species. The main Smittia pratorum; whereas A. italicum heating event can occur during the first subsp italicum attracted mainly P. phalae­ evening or night after the spathe has noides and P. grisescens (Diaz & Kite, opened as in: A. italicum, A. maculatum, 2002). On the other hand, A. italicum A. rupicola, A. jacquemontii. On the other (subsp italicum) is pollinated by different hand, A. dioscoridis, A. creticum and A. species, namely P. crassipenis and P. pus­ palaestinum produce heat during the early illa, in Toulouse (Albre et al., 2001). In­ morning until midday (Koach, 1985; Sku­ terestingly, P. crassipenis, a rare species in batz et al., 1990; Drummond & Hammond, England, has been recorded as a pollinator 1993; Bermadinger-Stabentheiner & Sta­ of British A. italicum (Withers, 1988). Con­ bentheiner, 1995; Albre et al., 2003). Fi­ sequently geographic variations of the pol­ nally, no rise in temperature was found in linators of a same species might be fre­ A. hygrophilum (Koach, 1985). Another quent. Some other examples of such var­ variable parameter is the intensity of heat iations are detailed in the next section (see production. The difference of temperature in the next paragraph "intraspecific varia­ between the spadix and ambient can be tion"). high (15-20°C) as in A. italicum, A. ma­ In Israel, Arum hygrophilum is also pol­ culatum, A. rupicola, A. jacquemontii, linated by a Psychoda species, namely P. medium (9-100 C) in A. dioscoridis, low cinerea, but only the males are attracted (3°C) in A. palaestinum and A. creticum, (Koach, 1985). In this case, the inflores­ or null as in A. hygrophilum (Koach, 1985; cence may not mimic the laying site of the Skubatz et al., 1990; Drummond & Ham­ pollinator as in A. maculatum or A. itali­ mond, 1993; Bermadinger-Stabentheiner & cum. Interestingly, females of P. cinerea Stabentheiner, 1995; Albre et al., 2003). were caught by inflorescences of A. itali­ cum cultivated in a botanical garden Odors (Koach, 1985). In Lebanon, Arum hygro­ This paragraph is mainly based on the philum is pollinated by another Psychod­ data presented in a major work done on id, Sciria advena (Kullenberg, 1953). 11 Arum species (Kite et at., 1998). Arum rupicola (misidentified as A. elon­ Odors of Arum species have been re­ gatum; [Boyce, 1993]) attracts Culicoides corded (Table 1) and with a few excep­ (Ceratopogonidae), an avian hematopha­ tions are congruent among observers gous parasite in Israel (Braverman & (Koach, 1985; Drummond & Hammond Koach 1982). This species cultivated in 1991, 1993; Boyce, 1993; Kite et al., 1998; Austria or England also attracts other Cu­ Drummond & Boorman, 2003; Boyce, licoides or Simulium species, which are 2004). According to Boyce (1993), "cryp­ rather mammalophilic (Knoll, 1926; Drum­ tic" species, except Arum idaeum pro­ mond & Boorman, 2003). The inflores­ duce odors, whereas "flag" species, except cence may mimic the fly host by its smell A. creticum are scentless, at least for a hu­ and heat and trap them once attracted. Cu- man nose. 160 AROIDEANA, Vol. 27

Faeces/urine Arum species Type of pollinator

A. maculatum Psychodidae

A. italicum Psychodidae

L..-_____ A. purpureospathum Sphaeroceridae 100 dung A. nigrum Sphaeroceridae Staphylinidae A. cyrenaicum 100 ??? A. apulum Sphaeroceridae Chironomidae Rotten A. dioscoridis Sphaeroceridae fruit A. palaesttnum Staphylinidae DrosophiJidae Freesia A. crettcum Bruchidae I Melyridae A. idaeum Bruchidae I Melyridae A. rupicola Ceratopogonidae

Fig. 3. Consensus strict tree ("chemogram") based on the relative abundances of the volatile compounds that composed the odor of various Arum species (data from Kite et at., 1998; Table 3).

The odors of many Arum species have chemogram, has been produced (Fig. 3). been studied (Kite, 1995; Kite et at. 1998; On this "tree", Arum odors are grouped Diaz & Kite, 2002), in which about 36 by chemical similarity. The integrity of one compounds have been found (see Table group, the 5 species with a dung odor plus 3). The volatile compounds emitted by the A. italicum, is very well supported. Inter­ appendix are variable among the species, estingly, A. maculatum and A. ttalicum but in general their foul odor smells like which are close species with similar fae­ faeces or decaying matter. Common com­ cal/urine odor are not in the same group, pounds are butanoIc acid esters, I-decene, indicating certainly an odor convergence terpenes (citronellene and its derivatives), (Kite et al., 1998). Arum maculatum has p-cresol, methyl salicylate, indole, 2-hep­ a different odor from the "dung group" by tanone (Table 3). Some species appear the absence of I-decene, f3-citronellene clearly different like A. creticum or A. pa­ and its derivatives: dimethyl-octadiene and taestinum, whose rotten fruit odor is due trimethyl-heptadiene (Table 3, Fig. 3). to benzyl alcohol and ethyl acetate. Arum Thus the faeces/urine odor of these two rupicola var. rupicola is also different be­ species have different biosynthetic origins, cause of a mixture of various sesquiter­ the one of A. italicum been chemically de­ penes even if p-cresol is abundant (Table rived from a dung odor. But despite these 3). odoriferous differences, both species are Based on the composition of Arum mainly pollinated by the same insect psy­ odors published by Kite et al. (1998), a choda phalaenoides in England (Diaz & phylogenetic tree, that may be called a Kite, 2002). Set apart from all others are M. GIBERNAU, D. MACQUART, G. PRZETAK, 2004 161 the two species with no apparent odor ferences were not Significant as they were (but which do emit volatile compounds!) in the insects trapped by A. maculatum. and the two species with sweet odors sim­ Arum palaestinum is an atypical "cryp­ ilar to rotten fruit or Freesia. But the chem­ tic" species, since its appendix emits main­ ical relationships among these groups are ly ethyl acetate, producing a smell of rot­ not fully resolved. ten fruit. Consequently, the insects attract­ Odors are also produced in the floral ed are not coprophilous insects but rather chamber, which are emitted by the fertile different species of Drosophila (Koach, part of the spadix and not the chamber 1985; Kite et al., 1998). wall (Kite, 1995). Contrary to the odor Finally, A. idaeum emits p-cresol and emitted by the appendix, the floral cham­ two derivatives (p-methyl anisole and 2- ber is highly homogeneous as 95% of the nitro-p-cresol) but in low quantities. This blend are bicyc10germacrenes for all the species is supposed to be scentless, but species studied. The exception is A. cre­ this suggests that it was never observed ticum, the only Arum species principally during the period of volatile production, pollinated by beetles which emits a-far­ or that the odor is not perceptible for the nesene (Kite et aI., 1998). human nose. A sweet odor akin to violet Pollinator attraction in Arum is mainly and hyacinth has also been reported for olfactory, thus odor change often implies this species by Drummond (in Kite et al., different visiting/pollinating insects. 1998). Flag species-These species are sup­ Cryptic species-Three compounds in posed to be non-smelling, except Arum particular are responsible for the faeces/ creticum, whose odor recalls Freesia (Iri­ urine odor in Arum maculatum: indole, p­ daceae) (Boyce, 1993). Nevertheless, these cresol and 2-heptanone (Kite, 1995). But species do emit volatile compounds that p-cresol is a major volatile compound of can be detected by insects. Also, the ap­ cow dung, which may explain why A. ma­ pendix of Arum rupicola var. rupicola culatum is pollinated 95% by females of produces numerous sesquiterpenes, traces Psychoda phalaenoides, since this midge of p-cresol, various alcohols, esters and lays its eggs in cow dung. Thus the midges ketones (Kite et al., 1998). These different searching by smell for a laying site may be compounds constitute a blend which at­ attracted by p-cresol emitted by the ap­ tracts biting midges (Ceratopogonidae) of pendix, and trapped by deceit. A field ex­ the genus Culicoides which are vertebrate periment showed that Psychoda species parasites (Braverman & Koach, 1982; were attracted to traps containingp-cresol, Koach, 1986; Drummond & Boorman, 2-heptanone, indole, or any combination 2003). (Kite et al., 1998). The most attractive Intraspecific variations-The odor in odors were p-cresol alone or the mixture some species may vary among popula­ of the three compounds. Since p-cresol is tions, particularly in species with large or present in most odors studied (Table 3), fragmented geographical distribution, and this molecule is suspected to be a general the types of pollinators attracted may also attractant for coprophilous insects (Kite et vary. Arum maculatum is described as al., 1998). having a foul and urinous scent in Eng­ The odor of A. dioscoridis var. dioscor­ land, whereas on continental Europe, it idis seems to confirm the attractive prop­ smells like a mixture of mouse, lemon and erties of 2-heptanone and p-cresol, since rotting plant material (Prime, 1960). this species emitting these two com­ Arum palaestinum has two different pounds, attracts coprophilous staphylinid ecotypes, the first type emits the odor of beetles and sphaerocerid flies (Drummond rotting fruit and attracts Drosophila; & Hammond, 1991). Apparently females whereas the second type produces a smell were more numerous than males but dif- of carrion which attracts necrophilous 162 AROIDEANA, Vol. 27

Table 3. Relative abundances of volatile compounds· present in the odors emitted by the appendix or the floral chamber in 11 species of Arum (data from Kite et aL, 1998). A. Chemical class italicum compound names A. spp. A. A. (or type) maculatum Italicum apulum cyrenaicum APPENDIX Fatty acid Derivatives I-decene +++ +++ +++ f3-citronellene +++ ++ +++ (dimethyl-octadiene) ++ +++ +++ (trimethyl-heptadiene) + Ethyl acetate Methyl butyrate + +++ ++ Methyl isobutyrate ++ ++ 2-methyl methyl butyrate + ++ + 2-heptanone +++ + + ++ 3-methyl butan-2-one + ++ 3-methyl pentan-2-one ++ 6-methyl heptan-2-one 2-nonanone ++ Ethanol + +++ + ++ Propanol Acetic acid Benzenics Benzeyl alcohol Benzaldehyde Methyl benzoate Methyl salicylate + + + p-cresol ++ + +++ +++ p-methyl anisole Nitrogen compounds Indole +++ ++ + Skatole + 2-nitro-p-cresol Phenylpropanoids Eugenol Terpenoids a-pinene ++ Myrcene ++ Limonene ++ ++ Sabinene ++ f3-pinene ++ Terpinolene ++ Geraniol Geranial Citronellol + (unidentified sesquiterpene) +++ ++ ++ +++ Sesquiterpenes (various) +++ ++ ++ + FLORAL CHAMBER Terpenoids Bicyclogermacrene ++++ ++++ ? ++++ a-farnesene ? • ++++: >90%; +++: 10-90%; ++: 1-10%; +: <1%; ?: not analysed. M. GIBERNAU, D. MACQUART, G. PRZETAK, 2004 163

Table 3. Extended.

A. A. A. rupicola A. purpureo- A. palaes- A. A.' var. nigrum spathum dioscorldis Unum creUcum idaeum rupicola

+++ +++ +++ +++ +++ ++ +++ +++ ++ ++ +++ ++ ++ + ++ ++ ++ ++ + ++

++ ++ ++ ++ ++ ++ ++ ++ ++ +++ ++ ++ ++ ++ ++ +++ +++ +++ ++ ++ ++ ++ + ++ ++

++ + ++ ++ ++ ++ ++ ++ ++ + +++

++++ ++++ ++++ ++++ ? ? ++++ ? ? 164 AROIDEANA, Vol. 27 scarabs and flies (Koach 1985, 1986; tions where the percentage of yellow spa­ Drummond & Hammond, 1993). In the dices is high (up to 50%) have been re­ same way, A. orientale, in Cyprus, is ported also in England but no data related known to have a fruit-scented form attract­ to pollination exist (Prime, 1960). ing Drosophila, whereas a faecal-scented form attracts Atheta staphylinids (Drum­ CONCLUSION mond & Hammond, 1991). Arum dioscor­ idis has been collected frequently and rep­ Even if the inflorescence morphology is resents the best documentation on geo­ basically very similar among the different graphical pollinator variation. In Turkey, species of Arum (i.e. a spadix surrounded this species traps coprophilous beetles by a spathe which forms a floral chamber (Staphylinidae: Anotylus and A theta) at its base), pollination systems appear to whereas in Cyprus it is mainly coprophi­ be diverse. Pollinator types attracted are in lous flies (Sphaerocerid: Coproica) with fact very different: beetles (Bruchidae, some Anotylus and Atheta (Drummond & Scarabaeideae, Staphylinidae), flies (Dro­ Hammond, 1991). In Lebanon, A. dioscor­ sophilidae, Sphaeroceridae, Psychodidae). idis is pollinated by other coprophilous So are the floral odors produced (sweet, beetles (Staphylinidae, Scarabaeideae) and faeces, urine, foetid, carrion, or none scatophagid flies (Kullenberg, 1953), but perceptible). Actually, the complete ther­ none of the Lebanese species are the same mogenic pattern is known for only a few as those from Turkey or Cyprus (Drum­ species, studying this character on new mond & Hammond, 1991). In Israel the species may reveal variations of thermo­ visitors are coprophilous flies (Sphaero­ genesis through the genus. Consequently, ceridae, Sepsidae) and beetles (Staphylin­ a general pollination model is clearly not idae, Scarabaeideae) (Koach, 1985; Papp valid for the whole genus, particularly & Rohacek, 1987). The odor variation has since A. creticum shows several peculiar­ not been studied between these locations, ities. These differences are probably relat­ but distinct odor profiles apparently exist ed to the biogeographical history of the between A. dioscoridisvar. dioscoridisand genus. The species have, during their evo­ A. dioscoridis var. philistaeum (Kite et al., lution, colonised various habitats in the 1998). These different ecotypes may be an different regions of Europe and Middle adaptation to a differential availability of East in which they had experienced dif­ pollinators among the localities. ferent climatic, ecological and fauna con­ Differences in volatile compounds have straints and may have developed particu­ been found between the odor of the two lar adaptations. However, in the absence English sub-species of Arum italicum of phylogenetic data, it is actually impos­ (Diaz & Kite, 2002). In particular; 2,6-di­ sible to determine how these different re­ methyl-2,6-octadiene and one derivative productive strategies have developed and are present in the odor of A. italicum evolved during the history of this genus. subsp. neglectum and absent in A. itali­ It is important to bear in mind that this cum subsp. italicum. Moreover, p-cresol is review is based on data available on just more abundant in this latter sub-species. a few species, with numerous species still This odor difference may be related to the to be studied. Such studies would allow fact that A. italicum subsp. italicum at­ testing different hypotheses on the evolu­ tracts P. phalaenoides and P. grisescens tion of plant-pollinators, for which the ge­ whereas it is P. phalaenoides and Smittia nus Arum appears to be a good system. pratorum in A. italicum subsp. neglectum (Diaz & Kite, 2002). Finally, an atypical ACKNOWLEDGMENTS French population of A. maculatum with yellow appendices may attract not only We wish to thank Peter Boyce for shar­ Psychoda but also domestic flies (Fridlen­ ing much information and personal data der, 1999b). Arum maculatum popula- and also for correcting the manuscript, and M. GIBERNAU, D. MACQUART, G. PRZETAK, 2004 165

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