1677 Variable patterns of seed maturation and abortion in Alliaria petiolata (Brassicaceae) David J. Susko and Lesley Lovett-Doust Abstract: We investigated variation in ovule development within and among fruits in garlic mustard, Alliaria petiolata (M. Bieb.) Cavara & Grande. Individuals were sampled at 14 sites in North America. On average, 94% of ovules showed evidence of fertilization and development. The majority of ovules (mean 68%; range 53.2–82.5%) reached seed maturity. Patterns of seed maturation and abortion varied nonrandomly within and among fruits. In sites in Tennessee, Kentucky, and Ontario, resource limitation seemed to be an important determinant of seed production, as fruits initiated nearest the base of an infructescence were significantly more likely to produce mature seeds than distally located fruits. Also the probability of seed maturation within individual fruits decreased significantly from the pedicellar to the stylar ends. In contrast, for individuals from Ohio sites, the probability of maturing seeds was greatest for centrally located fruits within an infructescence as well as for centrally located ovules within fruits, indicating a greater influence of pollen limitation in addition to resource limitation. We conclude that it could be misleading to infer traits of a species as a whole based on observed patterns of seed maturation in a single site or region. Rather such patterns may reflect prevailing conditions and selection pressures at a local, or regional, scale. Key words: Alliaria petiolata, Brassicaceae, garlic mustard, ovule abortion, seed maturation, patterns. Résumé : Les auteurs ont examiné la variation du développement de l’ovule à l’intérieur et entre les fruits de l’Alliaria petiolata (M. Bieb.) Cavara & Grande (ail-moutarde). Ils ont échantillonné des individus provenant de 14 sites en Amérique du Nord. Globalement, 94% des ovules montraient des signes de fécondation et de développement. La majorité des ovules ont atteint (en moyenne 68%; écart 53,2 à 82,5%) la maturité. Les patrons de maturation des graines et d’avortement varient de façon non-aléatoire à l’intérieur et entre les fruits. Sur les sites du Tennessee, du Kentucky et de l’Ontario, la limitation en ressources semble être un important facteur déterminant pour la production des graines, puisque les fruits se formant tout près de la base de l’infructescence sont significativement plus enclins à produire des graines mûres que les fruits se formant en position distale. De plus, la probabilité de maturation des graines à l’intérieur du fruit individuel diminue significativement de l’extrémité pédicellaire en allant vers celle du style. Au contraire, chez les individus provenant des sites de l’Ohio, la probabilité que les graines mûrissent est plus élevée pour les fruits localisés au milieu, à l’intérieur de l’infructescence, aussi bien que pour les ovules localisées centralement à l’intérieur du fruit, ce qui indique une plus grande influence d’une pollinisation limitée en plus de la limitation en ressources. Les auteurs concluent qu’il pourrait être trompeur de déduire les caractères d’une espèce dans son ensemble en ne se basant sur les patrons de maturation des graines, à partir d’une seule station ou région. De tels patrons peuvent au contraire refléter les conditions et les pressions sélective prévalant à l’échelle locale ou régionale. Mots clés : Alliaria petiolata, Brassicaceae, ail-moutarde, avortement ovulaire, maturation des graines, patrons. [Traduit par la Rédaction] Susko and Lovett-Doust 1686 tions is the period from ovule fertilization to seed matura- tion. Ovules may or may not be fertilized, and not all fertil- Plant population studies typically trace individual fates ized ovules reach maturity as viable, fully developed seeds. over time from seed germination and the emergence of seed- The period of seed ontogeny between fertilization and seed lings to reproductive maturity and the eventual death of the maturity is likely to be important in determining the even- individual. Mating systems and methods of seed dispersal, tual reproductive output of a plant and the vigour of its off- as agents driving ecological dynamics, have been studied in- spring. tensively (Howe and Smallwood 1982; Marshall and Folsom 1991; Venable and Brown 1993). However, a significant Several studies have shown that early initiated fruits life-history stage often neglected in demographic investiga- and seeds have a greater probability of reaching maturity than later initiated ones (Lovett-Doust and Eaton 1982; Nakamura 1986; Guitian 1994; Emms 1996). Early fertiliza- Received December 19, 1997. Accepted June 12, 1998. tion may provide a temporal advantage in subsequent inter- and intra-ovary competition for maternal resources. In addi- D.J. Susko and L. Lovett-Doust.1 Department of Biological tion to the timing of fertilization, the spatial arrangement of Sciences, University of Windsor, 401 Sunset Avenue, ovaries and ovules within a plant may also affect the proba- Windsor, ON N9B 3P4, Canada. bility of fruit and seed maturation. Seed mass, fruit mass, 1Author to whom all correspondence should be addressed. and the probability of maturing fruits and seeds have been e-mail: [email protected] shown to be greater in fruits located nearest the main rachis Can. J. Bot. 76: 1677–1686 (1998) © 1998 NRC Canada 1678 Can. J. Bot. Vol. 76, 1998 compared to those situated at more distal positions within a (siliques) are fully mature by early to middle July, at which time plant for a number of species (Lee and Bazzaz 1986; dehiscence begins. Cavers et al. (1979) determined that this species Matthies 1990; Guitian 1994). It is well established that was self-compatible and self-pollinated. plant fecundity is dependent on the ability to acquire poten- tially limiting resources. Thus, fruits and seeds that develop Stages of ovule development closer to maternal resources should have a spatial advantage Like most mustards, garlic mustard has two-loculed, bicar- in inter- and (or) intra-ovary competition (Solomon 1988; pellate, linear fruits. Individual siliques contain 8–24 ovules, gen- Siemens 1994; Navarro 1996). Two physiological models erally arranged alternately on the two sides of the sinus. A useful have been proposed to explain the success of early initiated feature of these fruits for the purpose of this study is that the and proximally located fruits and seeds (see Lee 1988 for re- ovules retain a persistent connection to the wall of the ovary. Thus, view). The source–sink model suggests that early or proxi- if fruits are collected with appropriate care prior to dehiscence, the mal fruits act as stronger sinks for attracting resources. An relative position of every ovule or developing seed within a fruit alternative model suggests that developing early or proximal can be recorded. Four major stages of ovule development could be identified readily. Some ovules showed no apparent signs of devel- fruits actively inhibit later or distal fruits through the pro- opment whatsoever; these ovules were small, shrivelled, and pre- duction of phytohormones. sumably unfertilized (though they could have been fertilized and Variation in ovule fates associated with ovule positions then aborted at such an early stage that they showed no visible within and between infructescences have been observed in a morphological signs of fertilization). Three subsequent stages were number of species (Wyatt 1981; Bawa and Webb 1984; recognized. Some ovules were expanded in size and had begun Rocha and Stephenson 1990). Although the existence of po- some development of the embryo but had not formed a seed coat. sitional effects on ovule development has been recognized These were termed early aborted ovules. Ovules that had pro- for a long time, few studies have addressed whether these ceeded through further expansion and embryo development but patterns of seed maturation vary among individuals, sites, or had not matured were called late-aborted ovules. These did have a seed coat but were characterized by malformations and were still geographical regions (but see Hossaert and Valero 1988). much smaller than a fully mature seed. Mature seeds were recog- Rather, it is implied that an observed pattern for a given site nized as the fourth and final stage of ovule development. These is representative of the species as a whole, regardless of ge- seeds were brown-black in colour and plump, with a completely netic differentiation or differing abiotic site conditions formed seed coat. Mean mass (± SE) of a mature seed was 1.723 ± among sites. The objective of this study was to examine spa- 0.005 mg and ranged from 0.466 to 3.652 mg (D.J. Susko, unpub- tial patterns in ovule development within and among fruits lished data). of garlic mustard, Alliaria petiolata (M. Bieb.) Cavara & Grande (Brassicaceae), which possesses relatively linear Sampling procedure and ovule standardization multiseeded fruits. To test for variation in the probability of Fourteen sites containing garlic mustard were sampled over a 3- seed maturation and abortion, we compared positional pat- week period from July 8 to July 29, 1994 (Table 1). Sites were se- terns both among plants and among sites across a large por- lected from four sampling regions across a >700 km latitudinal tion of this introduced species’ range in North America. transect of the species’ distribution in North America (Table 1). Factors that may contribute to the observed pattern of seed Annual precipitation, temperature, and the number of frost-free maturation and abortion are then discussed. days varied clinally among the regions (Table 1). Each site was lo- cated in a closed woodland or forest. Nearly all were associated with a river or creek, suggesting that garlic mustard seed dispersal via waterways may contribute to gene flow and the invasion of previously uncolonized communities. Garlic mustard was a domi- Study species nant understorey herb at all sites. Garlic mustard is a biennial herb native to northern Europe.