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M. CHARTIER AND M. GIBERNAU, 2009 153 Size Variations of Flowering Characters in maculatum ()

Marion Chartier and Marc Gibernau* Universite Paul Sabatier ~boratoire d'Evolution & Diversite Biologique (UMR 5174) Bat.4R3·B2 31062 Toulouse cedex 9, France

ABSTRACT KEYWORDS For entomophilous , the size­ Size-advantage model, resources alloca­ advantage model predicts a bias to the tion, number, floral sex-ratio. female function with resource increase. This model has been shown to be ex­ INfRODUCTION pressed on Mill. (Araceae), Proposed by Ghiselin 0969, quoted in whose bigger or latest are Lloyd & Bawa, 1984), the size-advantage female-biased. Here, we characterise the reproductive-trait variations of Arum ma­ model postulates a sex change when an increase in body size is related to differen­ culatum 1., a closely related species that is tial abilities to produce or sire offspring. For smaller and produces a single per year. entomophilous species, such as Aroids, the size-advantage model predicts By measuring the different floral parts a female-biased gender expression with and counting the flower number of differ­ size increase (Klinkhamer et al., 1997). This ently-sized inflorescences, we showed that is expressed by a proportionally bigger (1) for A. maculatum, 34% of size is increase of the female function than the allocated to the appendix, 12% for female male function in bigger individuals. This and 7% for male flowers. Due to its topic has been mainly studied in Araceae size range, A. maculatum could in a on Arisaema species presenting an extreme manner be considered as a "small" A. reproductive variation with a gender mod­ italicum. (2) As for A. italicum, the ification according to size (Gusman & appendix size is the longest part of the Gusman, 2003). Apart from Arisaema, this inflorescence, and increases proportionally question has been mainly studied on Arum more than the male and female parts size italicum. It has been shown in this species with plant vigour. This is not surprising, as that there is a disproportionate allocation to the appendix is an essential attracting the appendix versus the floral parts, with a organ for pollinators. (3) There is no length representing 44% of the spadix size correlation in A. maculatum between the (Mendez, 1998; Gibernau & Albre, 2008), flowers number and the other floral char­ and a mass representing 29% of the total acters, and no bias for female part size in inflorescence weight (Mendez, 2001). Such bigger inflorescences. Thus, contrary to A. results are not surprising as the appendix is italicum, there is no expression of the size­ the inflorescence's attractive organ, pro­ advantage model for A. maculatum, whose ducing heat and volatile organic com­ range of sizes might be too small. Another pounds (Bermadinger-Stabentheiner & Sta­ explanation is selection for a high number bentheiner, 1995; Kite et al., 1998; Diaz & of male gametes that may counterbalance Kite, 2002). In general, fertile parts and the potential bias for female flowers. appendix weights increase with plant vigour, which is representative of an * e-mail: [email protected] increase of the reproductive effort when 154 AROIDEANA, Vol. 32 resources become more abundant (Men­ one diptera species, the midge Psychoda dez, 1998; Gibernau & Albre, 2008). In phalaenoides whereas A. italicum is polli­ Spanish A. italicum, Mendez (2001) nated by several diptera species (Lack & showed that the mass allocated to male Diaz, 1991; Diaz & Kite, 2002; Albre et al., flowers increases proportionally more than 2003). In a way, we can consider from a for female flowers with increase in the pollination point of view that A. macula­ inflorescence's weight, which is in contra­ tum may be a "specialist" and A. italicum diction with the size-advantage model rather an "opportunist" species. Another prediction. However, the same author difference is that mature of Arum (1998) found no significant difference maculatum generally produce only one between the proportional increase of male inflorescence whereas mature Arum itali­ and female flower number with spadix size cum produce an average of two inflores­ increase. On the contrary, in the South of cences (Albre & Gibernau, 2008). France, Gibernau & Albre (2008) found that The aim of this paper is to document the female flower number increased pro­ the reproductive characters of Arum portionally more than male flowers with maculatum in three different French spadix size increase in A. italicum, show­ populations, and to characterize its allo­ ing that a bias to female parts can exist, cation strategy. Does A. maculatum, which is in accordance to the size-advan­ which produces a single inflorescence tage model. Thus, A. italicum floral sex per year, express the size-advantage ratio, which is male-biased (mean = .74), model for big inflorescences? Does its decreases with spadix size increase (Giber­ higher pollinator-specificity result in a nau & Albre, 2008). Furthermore, the sex different resource allocation in terms of ratio from the last inflorescences (which are the relative appendix size or the numbers smaller) tends to be female-biased (Men­ of fertile flowers? dez, 1998) which is also in accordance with the sized-advantage model, as the more MATERIALS AND METHODS vigorous plants are the ones able to produce up to three inflorescences per 34 inflorescences of L. year. Then, when considering the floral were collected during the spring of 2008 in parts size and mass variations, the resourc­ 3 populations situated in Bagneres-de­ es allocation in A. italicum seems to be Bigorre (Midi-Pyrenees, France), La Louba­ different for female parts, for which an tiere (Languedoc-RoussilIon, France) and increase in size would rather be due to an Smarves (Poitou-Charentes, France). The increase in flower size, than it is for male inflorescences were collected before the parts, for which an increase in size may release of and preserved in 70% likely be due to an increase of flower alcohol. number (Mendez, 2001; Gibernau & Albre, The lengths of the different parts of the 2008). spadix, i.e. fertile male and female zones Here, we study the floral variations and and appendix, were measured with a the expression of the size-advantage model digital calliper. Moreover, male and female of Arum maculatum (L.). Its flowering flowers per inflorescence were counted on cycle is protogynous; female flowers being 13 inflorescences. receptive before stamens release the pol­ Data analyses consisting of linear regres­ len. Arum maculatum is pollinated by sions, Shapiro tests, Bartlett tests, ANCOVA deceived diptera attracted by the floral (for differences between regression odour mimicking the odour of their ovi­ slopes), as well as a Kruskal-Wallis test positing site (sapromyophily) (Gibernau et followed by a multiple comparison test (for al., 2004). The deceiving odour is pro­ inter populations differences of floral part duced by a sterile organ situated at the apex sizes) were performed using R 2.5.1 (2007) of the inflorescence called the appendix. software. Codes are available from M. Arum maculatum is mainly pollinated by Chartier. M. CHARTIER AND M. GIBERNAU, 2009 155

RESULTS '3~-;'C; g ..... rv") ..... Morphology ~~t ~C\j""'; The mean sizes of the different parts of a ~ tI tI +1 ~=d-1 ,-... C"cc the inflorescences are shown in Table 1. ~C\j

Table 2. Mean numbers of male and female flowers of Arum maculatum inflorescences at La Loubatiere, Bagneres-de-Bigorre (BB) and Smarves. N = number of inflorescences measured. Loubatiere (N=5) BB(N=5) Smarves (N=3) Female flower number 26.8 ± 5.8 37.6 ± 13.1 27.3 ± 5.5 Male flower number 88.0 ± 19.3 128.6 ± 65.5 74.7 ± 19.1

DISCUSSION mean of 53% of spadix size is allocated to appendix and fertile zones for A. macula­ An important part of the spadix size of A. tum, against 67% for A. italicum. This (34%) was found to be allocat­ maculatum difference can be explained by the fact that ed to the appendix, against 11.9% for A. maculatum is on average smaller than A. female part and 7.2% for male part. italicum, with a mean A. maculatum Moreover, the appendix size increases spadix size of 64 mm (range 47-75) against proportionally more than fertile zones 102 mm (range 52-181) in A. italicum lengths (Fig. 1). This pattern is similar for (Gibernau & Albre, 2008). Then, the size A. italicum, whose appendix represents range of A. maculatum seems to corre­ 44% of the spadix size, against 16.5% for the spond to the smallest size range of A. female part and 6% for the male part italicum, and A. maculatum could be (Gibernau & Albre, 2008). However, a considered as a "small" A. italicum. An­ other explanation is that there may be a .. morphological constraint on the sterile ....0 flowers (as part of the floral trap) and stipe (as inflorescence sustaining organ) for their e- o minimal sizes. Thus, there might be a g '" threshold below which the stipe and the ic !!., sterile flower can't be decreased without c !il 1:1 affecting the reproductive success. 1! ~ ;!

o Male 40 50 60 70 60 90 100 ~ J------~_,._--~ Spadix length (mm) I Figure 1. Relationships between the C til lengths of the spadix and the appendix, J the male flower zone, and the female ------o ______• .0.. ______0 0 _ flower zone. Each of the measured parts 000 Female increases with spadix length (appendix: R2 9 = .72, F1,32 = 79.99, P < 10- ; female o zone: R2 = .2 4, F1,32 = 11. 4 5, P < 10 -2; L-~---,----._--._--_r--_,r 60 65 70 75 male zone: R2 = .53, F1,32 = 37.81, P < 50 55 Spadix length (mm) 10-6). Female and male zone increase in the same proportions (slopes are not Figure 2. Relationship between the significantly different: F1,32 = .11, P length of the spadix and the male and =.75). The slope of the appendix regres­ female flower number. No significant sion is higher than for the other zones correlation was found (male: F1,1l = .03, (F2,96 = 18.5, P < 10-5). P = .86; female: F1,ll = .07, P = .80). M. CHARTIER AND M. GIBERNAU, 2009 157

For both species, the appendix consti­ flower number and the spadix size. Anoth­ tutes the biggest spadix part. The appendix er explanation is that we masked any is crucial for pollination achievement as it relationship by pooling inflorescences from attracts insects by heating and producing several populations. This has to be tested volatiles organic compounds (Bermadin­ by measuring the flowers size and gamete ger-Stabentheiner & Stabentheiner, 1995; number against the spadix size in A. Kite et al., 1998; Diaz & Kite, 2002; A1bre & maculatum and A. italicum from a broader Gibernau, 2003), especially for these Arum sampling in the same populations. species, which are obligatory allogamous The expression of the size-advantage (Lack & Diaz, 1991; Albre et al., 2003). model in A. italicum results in a propor­ Thus, the more important investment made tionally bigger increase of the female part by the plant when more resources are vs. male part sizes with the spadix length available concerns the pollinator attraction increase (Gibernau & Albre, 2008) and in a function. In A. italicum, it has been shown bias to female part in the last inflorescence that appendix length was positively corre­ (Mendez, 1998). On the contrary, A. ma­ lated with the number of insects caught by culatum, which produces a single inflores­ the inflorescence (Mendez & Obeso, 1992), cence per year, doesn't show any expres­ which is likely also to occur in A. macula­ sion of the size-advantage model. We tum. For A. maculatum, one single Psy­ found no difference between the increase choda phalaenoides is supposed to be of the female and male part size against the sufficient to ensure fructification, but more spadix size increase, and no correlation pollinators might be necessary for A. between the floral sex-ratio and any other italicum, that bears 2.4 times more flowers floral character. This can be explained by and produces 4.6 times more seeds (Lack & the combination of different factors. (1) Diaz, 1991; Albre & Gibernau, 2008). In The range of spadix sizes of this species both cases, it seems that attracting a great may be too small to see the expression of number of pollinators increases the chanc­ the model. It has been shown on A. es (1) to ensure efficient pollen dispersal, italicum that plant size, and a fortiori (2) to attract at least one pollinator bearing spadix sizes are dependent on bulb size fresh allogamous pollen (Lack & Diaz, (Mendez & Obeso, 1993). The sizes of A. 1991; A1bre et al., 2003). maculatum represent the lower range of Male and female parts sizes increase size distribution of A. italicum, and its proportionally with spadix size for A. mean sex-ratio (.74) corresponds to A. maculatum, traducing a reproductive ef­ italicum smallest inflorescences sex-ratio fort when more resources are available, (.75) (Gibernau & Albre, 2008). In fact, A. even when pooling different populations. maculatum inflorescences appear to be However, their male and female flower equivalent (in terms of floral number and number is not significantly correlated to sex-ratio) to small A. italicum. The resourc­ spadix size. Thus, an increase of these parts es the bulbs of A. maculatum can accu­ may be due to an increase of flowers sizes mulate might be limited, leading to a for both genders, which is different than for constraint on the maximal inflorescence A. italicum, whose male part size increase size the plant can produce without affect­ is more due to an increase of the flower ing its seed survival and/or production number (Gibernau & Albre, 2008). Consid­ capacity. (2) In the studied populations, A. ering the small size range of A. maculatum, maculatum attracted 2 to 10 times more an increase of the flower number with pollinators than A. italicum (data non spadix increase might be more costly than published), so pollinators might not be a an increase of the size and number of limiting factor. A greater pollen disperSion gametes. On the contrary, reducing too and selection for a big number of male much the flower number may compromise gametes (i.e. male flowers) may counter­ the reproductive success. This may explain balance the potential bias for female the absence of correlation between the flowers. 158 AROIDEANA, Vol. 32

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