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(American Journal of Botany. 2001;88:1419-1423.)
© 2001 Botanical Society of America, Inc.

Reproductive Biology

A rare continual flowering strategy and its influence on offspring quality in a gynodioecious plant1

Lorne M. Wolfe2,4 and Janet L. Burns3

2Department of Biology, Georgia Southern University, Statesboro, Georgia 30460 USA 3Zach S. Henderson Library, Georgia Southern University, Statesboro, Georgia 30460 USA

Received for publication October 26, 2000. Accepted for publication January 25, 2001.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The majority of angiosperms have a single annual bout of reproduction; species that flower continually throughout the year are rare. Ochradenus baccatus is a gynodioecious, desert shrub whose principal flowering period is associated with the winter rains, although large individuals also remain in flower during the hot, dry summer. The goal of this study was to examine the reproductive consequences of continual flowering in a large population of O. baccatus in Israel. Over the two years of this study, 60% of individuals flowered continuously. The number of fruit and seeds per fruit were greater in winter. Winter seeds were ~12% heavier than summer seeds and had significantly higher germination rates (80 vs. 60%, respectively). Although summer seeds were smaller and less likely to germinate, we propose that the benefit derived from their production lies in their ability to capitalize on the first winter rains. These early rain events provide a head start on establishment and growth in the hostile desert environment. Plants that delay reproduction until the onset of rains risk having their offspring face the dry conditions of spring and summer.

Key Words: flowering phenology • germination • gynodioecious • hermaphrodite • Israel • Ochradenus baccatus • seed size


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The flowering phenology is an important property of a species' life history (Rathcke and Lacey, 1985 ; Ollerton and Lack, 1992 ; Kelly, 1993 ). While the most common pattern of flowering among angiosperms is a single annual bout of flower production (McClure, 1966 ; Frankie, Baker, and Opler, 1974 ; Rathcke and Lacey, 1985 ), several other phenological patterns exist (Newstrom et al., 1994 ). For example, a number of species display multiple episodic bursts of reproduction in a calendar year (Bawa, 1983 ; Bullock, Beach, and Bawa, 1983 ), while others have flowering periods interrupted by long nonreproductive intervals (e.g., bamboo; Janzen, 1976 ). Yet, except for anecdotal reports, few species exist in which individuals produce flowers and fruit all year (Newstrom et al., 1994 ).

Ultimately, the importance of a particular flowering strategy should be evaluated in light of its effect on the number and quality of offspring produced. It is known for a variety of species that there are reproductive consequences of intrapopulation variation in flowering time and synchrony (Augspurger, 1981 ; Marquis, 1988 ; Kelly and Levin, 2000 ). Individuals coming into bloom at the tails of the flowering season will have a potentially smaller pool of available mates than individuals that flower during the middle of the phenology (Thomson, 1980 ), and this can affect outcrossing rates (Wolfe and Shore, 1992 ). The influence of flowering behavior can also be detected within individuals. For a number of plant species, seed size declines through the flowering season (Cavers and Steel, 1984 ; Kang and Primack, 1991 ; Wolfe, 1992 ; Vaughton and Ramsey, 1997 ) suggesting that there is a diminishing pool of available resources through the flower phenology (Lloyd, 1980 ; Lee, 1988 ; Wolfe, 1992 ). The importance of seasonal shifts in offspring size results from the fact that parental provisioning plays an important role in the eventual success of those progeny (Harper and Obeid, 1967 ; Gross, 1984 ; Stanton, 1984 ; Parrish and Bazzaz, 1985 ; Waller, 1985 ; McGinley, Temme, and Geber, 1987 ; Mazer and Wolfe, 1998 ).

Ochradenus baccatus is a Middle Eastern desert shrub with a principal flowering period in the December–March rainy season (Zohary, 1966 ). However, a large fraction of the adult population remains in anthesis all year and the ability to flower continually is positively correlated with plant size (Wolfe and Shmida, 1995, 1997 ). As a result, there are effectively two flowering patterns exhibited in populations—large plants flower continually and smaller plants are reproductive only during the winter. The continual flowering behavior of O. baccatus raises the issue of whether this pattern has repercussions for offspring production and quality. It might be expected that offspring traits would be affected because environmental differences between the two seasons in the desert could affect a maternal plant's ability to provision seeds. Thus, the specific objective of this study was to address whether the quality and number of offspring produced by female and hermaphrodite O. baccatus differ between the winter and summer flowering seasons.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
The plant
Ochradenus baccatus (Resedaceae; hereafter Ochradenus) is a semideciduous shrub common in Middle Eastern deserts (Miller, 1984 ). In Israel, where this study was conducted, the plant occurs throughout the Judean Desert and Arava Valley (Zohary, 1966 ). The unspecialized flowers of Ochradenus are small (2 mm), borne on spikate inflorescences, and bees, beetles, wasps, and flies visit the flowers to collect pollen and/or nectar (Wolfe and Shmida, 1995 ). Individual flowers remain in anthesis for 2–3 d, and male flowers fall off the inflorescence immediately after. Populations of Ochradenus are gynodioecious and contain hermaphrodites and females in ~50 : 50 ratios (Wolfe and Shmida, 1997 ).

Measurements
Plant material used in this study was from a population of 134 permanently marked individuals (64 females, 70 hermaphrodites) at Nahal Hever, Israel (31°20' N, 35°20' E). This site is a wadi located ~5 km south of Ein Gedi in the Judean Desert (for details on this site, see Wolfe and Shmida, 1997 ). We censused the population for flowering seven times during this study (December 1993–August 1994). During each census we counted the standing crop of mature fruit on each plant and collected a random sample of ripe fruit from those individuals bearing fruit. The white fleshy fruits were air-dried for several days and stored in seed envelopes at room temperature until 1998 when we recorded the number of seeds per fruit and individual seed mass. These data were taken on the 53 families (28 females and 25 hermaphrodites) that flowered continually and produced fruit in both winter and summer seasons. The data in this paper are derived from measurements on 783 fruits and 4404 seeds.

Germination trials were conducted in the laboratory using seeds from 12 hermaphrodite and 12 female plants. From each plant we randomly selected ten seeds that were produced in each season. Seeds were weighed in groups of ten, placed in bags made of nylon parachute material that were then fixed under a slow-running faucet for 3 d. This protocol was designed to simulate the heavy rainfalls that seem to stimulate germination in the field. The majority of Ochradenus germination occurs in the first 3 d using this method (Wolfe and Shmida, 1997 ). The trials yielded virtually identical germination rates to those obtained immediately after seed collection in 1993–1994 (Wolfe and Shmida, 1997 ); therefore, the storage of seeds for 5 yr did not appear to affect germination.

Data analysis
All analyses were conducted with JMP 3.1.5 (SAS, 1995 ). Repeated-measures analysis of variance (ANOVA) (Zar, 1999 ) was used to partition the variance in fruit production, seed number per fruit, seed mass, and percentage germination into the following sources of variation: individual plant, sex (female vs. hermaphrodite), season (summer vs. winter), and the interaction between season and sex. All effects in the ANOVA model were considered as fixed effects except for individual plant, which was random. Values for germination were arcsine square-root transformed to achieve normality. To avoid potential problems of pseudoreplication, the average number of seeds per fruit and seed mass were calculated for each census for each plant, and these were the values used in ANOVAs.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Virtually all plants flowered in the large population of O. baccatus at Nahal Hever during the winter months (Fig. 1). Yet, of particular interest for this study, ~60% of the plants remained in flower continually, even during the summer.



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  		Fig. 1. Flowering phenology of Ochradenus baccatus at Nahal Hever, Israel throughout the duration of this study

 
The pattern of fruit production in Ochradenus varied between the two sexes and the two seasons (Fig. 2, Table 1). During the summer, males and females did not differ in fruit production. However, in winter, the standing crop of fruit was much greater in females than males. The highly significant interaction between sex and season resulted because hermaphrodites had relatively constant fruit production through the year, while females produced more fruit in winter compared to summer (Fig. 2). Although there was no significant difference between the two sex morphs in seed number per fruit (Fig. 3A), seeds produced by females were significantly heavier and germinated at a higher rate than seeds produced by hermaphrodites (Fig. 3B, C, Table 1).



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  		Fig. 2. Total fruit production by hermaphrodite and female Ochradenus baccatus in winter and summer flowering seasons. Open circles are female; closed circles are hermaphrodite. Values are means ± 1 SE

 

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  		Table 1. Repeated-measures ANOVAs partitioning the variance in reproductive traits on Ochradenus baccatus

 


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  		Fig. 3. The number, mass, and germination of seeds produced by hermaphrodite and female parents in the summer and winter flowering seasons in Ochradenus baccatus. Open circles are female, closed circles are hermaphrodite. Values are means ± 1 SE

 
There were significant differences in the packaging and provisioning of seeds between seasons. Winter fruit contained about twice the number of seeds as summer fruit (Fig. 3A, Table 1), and winter seeds were heavier than those produced during the summer months (Fig. 3B, Table 1). Germination success of seeds also varied seasonally with the highest percentage germination occurring in winter-produced seeds (Fig. 3C, Table 1).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Summer in Middle Eastern deserts is a difficult period for plants and as a result most growth and reproduction occurs during or immediately following the winter (Evenari, Shanan, and Tadmor, 1982 ). In fact, lack of water for physiological activity is thought to be the main factor limiting summer flowering in Mediterranean (Johnson, 1992 ) and desert environments (Fox, 1990 ). The combination of extremely high temperatures and complete lack of rainfall is likely responsible for the fact that virtually no plant species are active during this 6-mo period. Therefore, while true continual flowering appears to be rare among angiosperms, perhaps the last habitat we would expect to find it in would be a highly seasonal desert.

The present study is the first to examine how offspring attributes and production vary within individuals in a species that flowers all year. Seed size in Ochradenus was highly dependent on when during the year they were produced. Since the data were based on winter and summer seed from the same set of genotypes, the observed interseasonal differences are due to environmentally induced maternal effects. Presumably, plants are water stressed during the long dry summer, and the amount of resources available to be invested in offspring is less than in winter. Furthermore, it is well established that seed size in a variety of species is controlled largely by nongenetic maternal effects (Antonovics and Schmitt, 1986 ; Roach and Wulff, 1987 ; Mazer and Wolfe, 1992 ; Wolfe, 1995 ). Additional evidence that plants are stressed, or that some resource is limiting, is that the number of seeds per fruit also declined in summer. An alternative explanation for the decrease in seed output is that pollen is limiting due to lower pollinator densities in summer (Wolfe and Shmida, 1995 ). However, because seed number per fruit also declined in hermaphrodites, which are capable of producing seeds in the absence of pollinators (L. M. Wolfe, unpublished data), it is unlikely that pollen limitation is the cause of seasonal differences in seed number.

Owing to its unique summer flowering in the desert, it is reasonable to ask what selective forces favor continual flowering in Ochradenus. One could imagine that it would be preferable to cease flowering during the summer and save resources until the more favorable winter season. Perhaps the simplest way to explain summer flowering is that plants do it because they can. In other words, once plants attain some critical threshold size, they are better able to handle severe conditions. This proximate explanation could be true if, for example, larger plants had longer taproots that were able to exploit sources of water unavailable to smaller plants. An alternative, and more adaptive explanation, is that the benefit of summer flowering results from its effect on seed and seedling ecology. Individuals that flower during the summer contribute relatively early to the seed bank. In the Judean Desert, heavy rains typically fall for a short period causing local flooding. However, the water rapidly percolates into the sand or evaporates and the time available for germination and establishment is restricted to a few days. Thus, the seeds that have the best chance of surviving the seedling stage and first year of growth are those that were produced prior to the rainy season and are able to take advantage of the first rains. Also, germinating early in the winter means that the probability of additional rain events in that year is still high (Clauss and Venable, 2000) . On the other hand, individuals that delay flowering until the onset of winter rains will not have offspring ready for germination until later in the rainy season. Given the high variance among years in total rainfall in this region (Aronson and Shmida, 1992 ), it is possible that no further rains will occur, dooming the winter-produced seeds to a long period of dormancy. Lying dormant in a seed bank can be a costly strategy as there are various sources of attrition (Baker, 1989 ). For example, Israeli deserts support large numbers of granivorous animals (Brown, Kotler, and Mitchell, 1997 ; Wilby and Shachak, 2000 ). In addition to predation pressure, abiotic factors such as sunlight may result in a loss of viability in seeds under natural conditions (Kigomo, Woodell, and Savill, 1994 ). We therefore propose that selection for early germination in the next generation has been the prime force selecting for the rare continual flowering phenology of Ochradenus. A similar argument was forwarded by Clauss and Venable (2000) who suggested that reproductive traits in desert annuals evolved in response to selection to increase the predictability of success following germination. Furthermore, Burtt (1970) argued that conditions for seed germination in some Israeli desert monocots have selected for flowering time in the adults. By monitoring experimental arrays of seeds under natural conditions, it would be feasible to evaluate the importance of seed bank ecology and early germination in the evolution of flowering schedules in Ochradenus.


   FOOTNOTES
 
1 The authors thank Avi Shmida and ROTEM for providing logistic support during the fieldwork portion of this study; Ori Fragman and Gato Hatool for help in the field; Katrina Motes and Susan Sellers for weighing and counting seeds; and Ray Chandler, Danny Gleason, Alan Harvey, Lissa Leege, Rob Slotow, Allison Snow, and the GSU Evolution & Ecology Discussion Group for providing comments that improved the manuscript; and the Lady Davis Fellowship Trust for financial support. Back

4 Author for reprint requests (wolfe{at}gasou.edu , Phone: 912-681-0848, Fax: 912-681-0845). Back


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