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Floral costs in Nigella sativa (Ranunculaceae): compensatory responses to perianth removal¹

Plant Ecology and Systematics, Department of Ecology, Sölvegatan 37, S-223 62 Lund, Sweden

Received for publication April 16, 2004. Accepted for publication October 19, 2004.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Because internal resources are finite, it has been assumed that attractive, floral organs represent a significant drain on the energy and nutrient budget of a plant. Despite the broad significance of such trade-offs, in relatively few studies have investigators manipulated floral investments, then evaluated allocation to subsequently produced flowers, fruits, and seeds. In the present study of Nigella sativa, the cost of maturing and/or maintaining perianths was documented after all sepals and nectaries were removed at the bud stage and a significant increase in mean seed mass, the total amount of biomass allocated to seed production, and mean germination rate of the maternal seed crop were measured. The increased biomass, carbon, and nitrogen allocated to seeds were similar in magnitude to the reduction in biomass, carbon, and nitrogen invested in sepals and nectaries after perianth removal. Perianth removal did not significantly affect flower production, maternal fecundity, or progeny seed number. Taken together, these observations indicate the potential for selection—mediated through resource trade-offs with seed mass and time to germination—to cause, or at least facilitate, evolutionary reductions in flower size.

Key Words: floral evolution • Nigella sativa • Ranunculaceae • reproduction • resource allocation • trade-off

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Natural selection is an important force driving evolutionary change in floral morphology that involves not only pollinators, but also resource costs, flower enemies (e.g., nectar thieves, flower herbivores, seed predators), and correlated responses to evolutionary changes in nonfloral characters (Primack, 1987 ; Andersson, 1997 , 2001 ; Galen, 1999 ). In particular, the commonly assumed trade-off between allocation to floral advertising vs. fruit or seed production has long been invoked as a primary mechanism underlying the evolutionary reduction of flower size as plants become less dependent on outcrossing (Charlesworth and Charlesworth, 1987 ; Lloyd, 1987 ; but see Sakai, 1993 ). However, although substantial biomass may be invested in attractive floral organs (Lovett-Doust and Cavers, 1982 ; Southwick, 1984 ; Ashman, 1994a , b ; Ashman and Schoen, 1996 ), increased allocation to floral display must be demonstrated to entail reduced allocation to other functions ("opportunity costs," Gulmon and Mooney, 1986 ) before any broad generalizations can be made regarding the evolutionary significance of "advertising costs."

Several studies have reported negative genetic correlations between floral advertising and components of fitness (Mossop et al., 1994 ; Robertson et al., 1994 ; Campbell, 1997 ), but both nonsignificant and positive correlations have also been documented (Connor and Via, 1993 ; Eckhart, 1993 ; Andersson, 1996 ; Worley and Barrett, 2000 ). Furthermore, the importance of such trade-offs could be obscured or reduced by factors such as photosynthesis of the attractive structures themselves, resorption of resources prior to the abscission of the perianths (Ashman, 1994a ), or positive covariance generated by differences in resource acquisition as a consequence of age, genotype or local growth conditions (van Noordwijk and de Jong, 1986 ).

Confounding effects of resource status can be minimized in experiments involving random assignment of plants to different resource manipulation treatments. Regarding experimental studies of advertising costs, the most obvious approach is to remove the attractive floral parts so early that resources have not yet been invested in these structures, and then evaluate allocation to subsequently produced flowers, fruits, and seeds (Andersson, 1999 , 2000 , 2001 ; see also Pyke, 1991 ; Ashman and Schoen, 1997 ). Such experiments not only minimize the weaknesses associated with correlational analyses, but also enhance the power to detect trade-offs by expanding the variation in floral investment (Mitchell-Olds and Shaw, 1987 ).

Plants of Nigella sativa L. (Ranunculaceae) have large, robust flowers that allow early removal of both sexual and accessory organs, and therefore provide a useful model for experimental studies of allocation costs. For example, previous stamen and style removal experiments have verified the existence of a resource-based trade-off between male and female reproductive effort in this species (Andersson, 2003 ). In the study presented here, I extend the experimental analyses to explore the costs of maturing and/or maintaining the outer, accessory parts of the flowers, the perianths. Specifically, I ask (1) Does reduced expenditure of resources on the perianths, mediated through early perianth removal, lead to compensatory increases in subsequent flower and seed production? (2) Is there a quantitative agreement between the "saved" resources after perianth removal and the increase in resources allocated to seeds in the removal group? I emphasize that my study is focused on resource costs, not on how the removal of sepals and nectaries affects the functioning of the perianths (which will be the subject of future studies).

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Plant material
Nigella sativa is an annual, hermaphroditic species with a more or less branched stem, pinnately dissected leaves, and a determinate flowering pattern, starting with the flower terminating the main shoot and ending with the flowers on the lower-most branches. The perianths are differentiated into an outer whorl of five, 15–20 mm long, whitish, petaloid sepals, and an inner whorl of eight, 7–8 mm long, nectariferous petals (hereafter referred to as "nectaries"). The androecium comprises a large number of stamens, which shed their pollen as the filaments curve outward during the male phase. The gynoecium consists of up to five completely united follicles, each with a long, indehiscent style. The male phase is initiated a few days before the stigmas become receptive; however, the maturing styles often become twisted around the last dehiscing anthers, which results in self-pollination (delayed selfing; Lloyd, 1979 ). Fertilized flowers develop into 2- to 3-cm-long capsules with numerous seeds. Due to slow sepal development, all perianth parts are exposed during the early bud stage. Nigella plants flower once and then die; therefore, all resources accumulated prior to flowering are devoted to reproduction.

This study is based on the same plant material (provided by the Botanical Garden of the Martin-Luther-Universität at Halle, Germany) as were used in the previous study of sex allocation trade-offs (Andersson, 2003 ). The study plants represent the type variety sativa, a widely cultivated form in the southern parts of Eurasia. This form differs from putatively wild populations, N. sativa var. hispidula Boiss., in having longer leaves, fewer branches, and larger flowers (Zohary, 1983 ).

Perianth removal experiment
In March 2003, ca. 200 seeds from a bulked population sample were sown individually into 25-cm² cells with standard peat soil (Kronmull; Weibulls, Hammenhög, Sweden) in a series of plug trays on a bench in a greenhouse. Water was supplied daily or as needed, but no extra fertilizer was applied. Following the initiation of the first flower buds, I assigned 70 randomly selected individuals to each of two resource manipulation treatments—removal of all perianths at the bud stage (removal group) vs. perianths left intact (control group)—and outcrossed all flowers by hand at the onset of female receptivity with pollen from freshly dehisced anthers in flowers on other plants in the experiment. The perianths were removed with a pair of tweezers when they had reached 1/4 of their final size. Based on phenological data from 10 randomly chosen plants in the experiment, the perianths were removed 10 to 11 d before the onset of anther dehiscence and 14 to 16 d before the onset of stigma receptivity. The stamens and pistils appeared to develop normally after perianth removal (S. Andersson, personal observation). Hand pollination of all flowers enhanced the power to detect trade-offs by increasing the number of resource sinks (increased fruit production) and the range of response variables.

After the flowering season (June), I measured the following response variables on each plant: total fruit number, total seed number, total seed mass (measured to the nearest mg), and mean seed mass (total seed mass divided by total seed number). All plants were dead at the final harvest. In September, I planted five seeds per plant in random positions (one seed per cell) in the same type of plug trays as were used in the parent generation, to examine progeny quality, quantified as the number of days to germination and progeny seed number. The latter variable was estimated from the length of each fruit using a predictive equation generated from a separate data set (seed number = –30.81 + 6.84 fruit length (mm); Pearson r = 0.98, N = 20, P < 0.001). Any increase in these parameters after perianth removal, relative to the control group, would indicate that perianths are costly to mature and/or maintain.

Data on total fruit number, total seed number, total seed mass, and mean seed mass were subjected to one-way analyses of variance (ANOVA) to assess the effect of perianth removal on each response variable. Analysis of progeny quality (germination date and seed number) also included maternal parent (nested within treatment) as an additional group variable. These analyses were followed by analyses of covariance (ANCOVA) based on family means to detect (and remove) any confounding effects of seed mass and/or emergence date on measures of progeny quality. The residuals of all ANOVAs and ANCOVAs approached normality, so no transformations were necessary.

Analysis of biomass, carbon, and nutrient allocation
To quantify the reduction in floral investment after early perianth removal, I obtained a bulked sample of removed perianths from 50 randomly selected flowers in the removal group, and a corresponding sample of fully developed perianths from plants in the control group (collected immediately before perianth abscission). These bulk samples provided data on perianth biomass—recorded to the nearest mg after drying for 3 wk at room temperature, then divided by 50 to obtain per-flower estimates—and the investment of energy and nutrients, quantified as the product of perianth biomass and the concentration of carbon and nitrogen in each sample of perianths. The amounts of biomass, carbon, and nitrogen allocated per perianth, multiplied by total flower number (Table 1) to obtain per-plant estimates, were compared between treatment groups to assess the amount of saved resources after perianth removal. These data were compared with the total amount of resources allocated to seeds, estimated from data on mean seed biomass (Table 1) and the content of carbon or nitrogen in a bulked sample of seeds from each treatment group. A close agreement between the amount of resources not spent on perianths and the amount of extra resources invested in seeds after perianth removal would verify the existence of a resource-based trade-off between perianth and seed development.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Plants subjected to early perianth removal produced 12.5% heavier seeds (P < 0.001) and allocated 15.8% more biomass to seed production (P < 0.01) than plants on which all perianths were left intact, whereas differences in flower production and total seed number were not significant (Table 1). Perianth removal did not significantly affect the proportion of seeds that germinated (ca. 95% in both treatment groups; ² = 0.04, P = 0.84, data pooled across progeny families), but caused a shift toward earlier germination dates (P < 0.01; Table 1). Collapsing the germination dates into family means and including maternal seed mass as a covariate reduced the F value for treatment (Tables 1, 2), but perianth removal continued to have a significant effect on germination date (P < 0.05). Progeny seed number varied positively with seed mass (regression coefficient b = +0.62, P < 0.01) and negatively with germination date (b = –2.45, P < 0.001; multiple regression analysis on family means based on data pooled over treatments, N = 135), but was not significantly affected by the presence or absence of perianths on the maternal parent, regardless of whether covariates were included or excluded (Tables 1, 2).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
With a fixed amount of resources, increased expenditure of resources on floral structures necessarily entails reduced allocation to subsequently produced flowers, fruits, and seeds, especially in short-lived, monocarpic species (which require no allocation of resources to future growth and longevity). Despite the broad significance of such resource trade-offs (Charlesworth and Charlesworth, 1987 ; Lloyd, 1987 ), in relatively few studies have investigators documented genetically based correlations between floral display and other plant functions (Mossop et al., 1994 ; Robertson et al., 1994 ; Campbell, 1997 ) or manipulated floral investments to determine costs of allocation to attractive floral structures (Ashman and Schoen, 1997 ; Andersson, 1999 , 2000 , 2001 ). In the present study, I explored the floral costs of N. sativa, an annual plant whose flower structure allows early removal of all sepals and nectaries without deleterious effect on subsequent flower development. As well as testing for significant treatment effects on reproductive effort, I looked for quantitative agreement between the resources saved after perianth removal and the subsequent resources allocated to seeds after the removal.

Removal of immature perianths had no detectable effect on the number of flowers and seeds produced, but significantly increased seed mass and the total biomass allocated to seed production, presumably by using resources that became available after the perianths were removed. In agreement with the latter interpretation, the increases in seed biomass and two additional measures of allocation, the amount of carbon and nitrogen allocated to seeds, were similar in magnitude to the amount of biomass, carbon, and nitrogen not spent on perianths in the removal group. These observations corroborate the assumption that accessory floral structures represent an important sink for assimilates (Charlesworth and Charlesworth, 1987 ; Lloyd, 1987 ), but also show that N. sativa expresses this cost as a trade-off with seed maturation rather than subsequent flower production. The latter observation may partly be an effect of the determinate flowering pattern in this species. The number of floral meristems is fixed at an early stage and decreases after flower development starts; consequently, plants with determinate flowering may have difficulty optimizing the use of "delayed" pulses of resources, such as those resulting from perianth removal. Furthermore, given the close proximity of perianths and ovaries in the same flower, developing seeds should be able to monopolize resources not used by the perianths, thus reducing the amount of resources that can be allocated to other flowers (see also Andersson, 1999 ).

In this regard, it is necessary to emphasize that the observed costs include not only the resources allocated to maturing perianths, but also the resources invested in the production of nectar, maintenance respiration, and transpiration by fully developed perianths (Ashman and Schoen, 1996 ). To separate production and maintenance costs, it would be necessary to manipulate flower or perianth longevity (Ashman and Schoen, 1997 ; see also Andersson, 2000 ). Another unresolved issue is whether perianth costs are mitigated by floral photosynthesis and/or resource resorption from senescing sepals and nectaries (Ashman, 1994a ). Finally, whether the observed resource costs are manifested as negative genetic correlations between perianth size and total seed biomass remains to be seen. It is the latter type of association that could facilitate or constrain the evolution of reproductive characters (Reznick, 1985 ).

The detection of costs in the present investigation contrasts sharply with the results of previous emasculation experiments: stamen-less plants of N. sativa produced heavier seeds than plants whose stamens remained intact, but this response was balanced by a compensatory reduction in total seed number, resulting in a nonsignificant treatment effect for total seed biomass (Andersson, 2003 ). Apparently, the removal of all stamens affected the balance between seed size and seed number, rather than the total amount of resources devoted to seed production. Regarding the lack of detectable effect on total seed biomass, the stamens may have been removed too late to reduce investment in these structures (Andersson, 2003 ), or part or most of the resources invested in stamens may have been resorbed prior to abscission (cf. Ashman, 1994a ). In contrast to the results of the perianth removal experiment, stamen removal also caused a slight increase in the number of flowers that died before fruiting, perhaps by disturbing the flow of assimilates into the ovaries (Andersson, 2003 ). Whatever the mechanisms underlying the deviating responses to stamen removal, resource-based trade-offs can reasonably account for the results of the perianth removal experiment.

My results provide no evidence to suggest that increased allocation to perianths leads to reduced allocation to direct components of fitness. First, plants both with and without perianths did not differ in fecundity or total flower number. Second, even though the perianth-less plants produced heavier seeds with earlier germination dates than the control plants, I found no detectable effect of perianth removal on seed viability or the fecundity of plants in the progeny generation. However, high seed mass and germination speed had positive and independent effects on progeny fecundity. Based on this observation, I hypothesize that trade-offs play a role in exerting selection pressure on the size of the perianths, at least when seed mass and time of emergence represent major determinants of fecundity. However, to assess the direction and magnitude of selection on perianth size, it will also be necessary to determine whether the presence of large, conspicuous perianths enhances the amount of cross-pollination. If so, one would expect perianth size to be under stabilizing selection, the optimum phenotype being a compromise between pollinator-mediated selection for larger floral displays and trade-offs with seed size and/or germination speed. Only field experiments can determine how resource costs and ecological forces operate simultaneously in exerting selection on perianth size.

Nigella species differ greatly in the size of the floral structures. This variation is strongly associated with differences in mating system, with autogamous species having smaller perianths than species that fail to set seed in the absence of pollinators (Strid, 1969 , 1970 ; S. Andersson, unpublished observations). Numerous hypotheses, involving both selective and genetic factors, have been proposed to explain this pattern (Andersson, 1997 ). One obvious hypothesis is that small flower size reduces the energetic cost per flower, a factor that would reduce the optimum perianth size under conditions of stress (Galen, 1999 ) or low pollinator abundance (Charlesworth and Charlesworth, 1987 ; Lloyd, 1987 ). Results of this study and a previous perianth removal experiment with a related species (N. degenii; Andersson, 2000 ) indicate a great potential for selection—mediated through resource trade-offs—to cause, or at least facilitate, evolutionary reductions in flower size if plants become less dependent on outcrossing.

Plants of N. sativa are capable of setting seed without being cross-pollinated, an advantageous feature in seed crops, which should be under strong selection for increased seed production. However, the domesticated variety (var. sativa) has undergone little, if any, reduction in flower morphology compared with conspecific populations in more natural habitats (var. hispidula; Zohary, 1983 ). It is possible that the large, conspicuous perianths increase outcrossing rate or male fertility (pollen donation) to a greater extent than female fertility; for example, high pollinator visitation rates during the male phase would allow plants to increase their success as pollen donors. The retention of large perianths could also be an incidental effect of selection for maximum seed production, if seed number increases with capsule size and some genes control the growth of both capsules and perianths (Primack, 1987 ). Lack of heritable variation in relevant characters could be a similar constraint on floral evolution.

Previous work has shown conflicting results in the costs of producing and maintaining floral organs associated with display and reward. Pyke (1991) and Ashman and Schoen (1997) documented floral maintenance costs in Blandfordia grandiflora R. Br. and Clarkia tembloriensis Vasek, respectively. Andersson (1999 , 2001) removed rays to assess the overall cost of floral display in two members of the sunflower family: Achillea ptarmica L. showed a significant increase in percent fruit set after ray removal, contrasting with the lack of treatment effect in Senecio jacobaea L. Experimental data from N. degenii not only verified the existence of construction and maintenance costs, but also provided evidence for population-specific allocation patterns: perianth removal increased flower production in one population and had a positive influence on fruit set and seed viability in another population (Andersson, 2000 ). These findings and those of the present study demonstrate considerable heterogeneity in the extent to which floral investment causes reduced allocation to other plant functions, a conclusion that also applies to the variety of patterns seen in correlational analyses (Connor and Via, 1993 ; Eckhart, 1993 ; Mossop et al., 1994 ; Robertson et al., 1994 ; Andersson, 1996 ; Campbell, 1997 ; Worley and Barrett, 2000 ).

	FOOTNOTES

 
¹ The author thanks Tommy Olsson and Maj-Britt Larsson for carrying out the chemical analyses, and Bengt Jacobsson for taking care of the plants in the greenhouse. Financial support by the Swedish Natural Science Council is also acknowledged.

² For correspondence: E-mail: stefan.andersson{at}ekol.lu.se

	LITERATURE CITED

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