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Reproductive Biology |
Department of Biological Sciences, Florida International University, Miami, Florida 33199 USA
Received for publication May 27, 2004. Accepted for publication December 13, 2004.
ABSTRACT
Sawgrass, Cladium jamaicense, is the dominant macrophyte in the Florida Everglades. We examined sawgrass flowering phenology and compatibility reactions in ex situ and in situ populations over 2 yr. Sawgrass flowers in May in southern Florida. Flower maturation was relatively synchronous within an inflorescence. Along the entire inflorescence, functionally male flowers emerged initially, followed by stigmas, then anthers of hermaphroditic flowers. Flowers of each sex expanded over 2 d with less than 1 d in between, totaling 6– 7 d for an inflorescence to complete flowering. Hand pollinations showed that sawgrass was self-compatible and not pollen-limited, because open pollinations produced fruit set similar to self- and cross-pollinations. Fruit set was low in autogamy and manipulation treatments. Manipulation treatments were used to study the effect of exposure to airborne pollen during hand pollinations. This treatment thus provides a useful technique for studies on the in situ compatibility of wind-pollinated graminoids. Sawgrass was able to self-fertilize, but the timing of flower maturation on an inflorescence promoted outcrossing. Actual outcrossing rates in sawgrass thus depend on clonal architecture and the timing of floral maturation on other inflorescences within a clone rather than on inflorescences of other genets in a population.
Key Words: anemophily • Cyperaceae • Everglades • protandry • protogyny • sawgrass • self-compatibility • wind pollination
Abiotic vectors of pollen transport, such as wind, have received far less attention than their biological counterparts (Ackerman, 2000
; Harder, 2000
; Culley et al., 2002
). Wind-pollinated or anemophilous species, which occur in 18% of all angiosperm families, typically have high pollen-to-ovule ratios and low percentages of effective pollen grains (Faegri and Van der Pijl, 1979
; Culley et al., 2002
). Anemophilous species are commonly viewed as having inefficient reproduction (Ackerman, 2000
). Contrary to this perceived inefficiency, wind-pollinated species usually reduce energy investment in perianth structures and floral rewards (Niklas, 1985
; Richards, 1997
), and the high allocation to pollen production can increase pollen dispersal in areas where turbulent or random wind flow dominates (Midgley and Bond, 1991
; Ackerman, 2000
).
Flowers of anemophilous species often separate sexes temporally (dichogamy) and/or spatially (herkogamy) (Ackerman, 2000
), which promotes outcrossing. The occurrence of physiological self-incompatibility in wind-pollinated species, however, has not been considered in recent reviews (Ackerman, 2000
; Culley et al., 2002
), although self-incompatibility is wide-spread in the anemophilous Poaceae (Baumann et al., 2000
). There have been few compatibility studies in the other major graminoid families (Juncaceae, Cyperaceae). Members of the Juncaceae are thought to self-fertilize abundantly (Proctor et al., 1996
), while both self-incompatibility and self-compatibility have been reported for the Cyperaceae (Davies, 1955
; Faulkner, 1973
; Pojar, 1974
; Handel, 1976
, 1978
; Vonk, 1979
; Schmid, 1982
; Standley, 1985
; Whitkus, 1988
; Dunlop, 1999
; Charpentier et al., 2000
).
In addition to being primarily wind-pollinated, graminoids are often ecologically dominant species that have high frequencies of clonal reproduction (Richards, 1997
). If crossing occurs between genets, sexual reproduction in clonal plants can help to avoid inbreeding depression and to maintain genetic diversity in populations through repeated recruitment events (Eriksson, 1989
, 1992
). Mechanisms that promote outcrossing, such as dichogamy, herkogamy, and self-incompatibility, would thus be evolutionarily advantageous in these populations. The genetic consequences of anemophily, however, have largely been ignored in natural populations of graminoids.
Sawgrass, Cladium jamaicense Crantz, (Cyperaceae), is wind-pollinated. Sawgrass is the dominant macrophyte in the Florida Everglades, historically comprising 70% of the vegetative cover (Loveless, 1959
). The Everglades ecosystem, which originally was an oligotrophic wetland with alternating wet and dry seasons, has undergone nutrient and hydrologic alterations as a result of anthropogenic influence. In altered landscapes, sawgrass abundance has declined, and it is often outcompeted by other species, particularly the cattail Typha domingensis (Alexander et al., 1973
; Wood and Tanner, 1990
; Urban et al., 1993
; Davis and Ogden, 1994
; Rutchey and Vilcheck, 1994
; Jensen et al., 1995
; Anderson et al., 1997
). Sawgrass has been the focus of numerous ecological studies (Brewer, 1996
; Newman et al., 1996
; Miao et al., 1997
; Busch et al., 1998
; Ponzio, 1998
; Daoust and Childers, 1999
; Richardson et al., 1999
; Vaithiyanathan and Richardson, 1999
; Chabbi et al., 2000
; Lorenzen et al., 2001
), but research has only recently begun to address its population structure and reproduction. Several sawgrass propagation studies have focused on clonal rhizome and/or plantlet production (Bernard et al., 1985
; Brewer, 1996
; Miao et al., 1998
), but recent investigations have found sawgrass to exhibit genotypic diversity at the m2 scale in Everglades populations (Ivey and Richards, 2001
). To generate this fine-scale genotypic diversity, sexual reproduction must occur, but the details of reproductive phenology and type of breeding system are unknown. This study describes some of the basic parameters of sexual reproduction in sawgrass. The main objectives of our study were to describe the phenology of sawgrass flowers, spikelets, and inflorescences and to determine whether sawgrass is self-incompatible.
MATERIALS AND METHODS
Sawgrass reproductive morphology
In southern Florida Cladium jamaicense flowers from late April to early June, near the end of the Everglades dry season. Flowering culms produce an inflorescence stalk that elevates the cymose inflorescence over its own foliage and that of adjacent vegetation. Each inflorescence bears axillary branches that have clusters of spikelets, hereafter referred to as lateral clusters. Each lateral cluster is branched; the lower clusters of vigorous plants have five to six orders of branching. All branches terminate in spikelets (Richards, 2002
). Internode length decreases acropetally along the inflorescence, as does the number of branches, orders of lateral cluster branching, and number of spikelets on the lateral clusters (Richards, 2002
). Sawgrass spikelets have five to nine bracts and two developmentally bisexual flowers, the terminal (or F1 flower) and an axillary (or F2 flower) (Richards, 2002
). Each flower has two stamens and a single ovary and ovule, although the gynoecium of the F1 flower frequently aborts (Richards, 2002
). A detailed description of spikelet and floral morphology can be found in Richards (2002)
.
Floral phenology
Flowering phenology was investigated in an ex situ population at Henington Pond on the University Park campus of Florida International University (FIU), Miami, Florida (25°45.632' N, 80°22.620' W). Sawgrass plants in this population were transplanted in 1998 from two natural populations and currently grow in discrete patches or clones fringing the north side of the manmade pond. Phenology of flowering was followed in May 2002 and 2003; 51 inflorescences in eight clones (2002) and 53 inflorescences in 11 clones (2003) were observed (Ni = 104, Nc = 11, where i refers to individual inflorescences, and c refers to clones observed). Although some clones were observed in both years, individual inflorescences in these clones were only followed during their respective flowering year. Inflorescences were examined daily from when they first expanded until they ceased flowering. Within the population, these observations occurred from initial to peak flowering of the population. During each observation period, gender was recorded for all lateral clusters along an inflorescence with >50% of the flowers expanded. Each lateral cluster of an inflorescence was scored as either F1 female, F1 male, F2 female, F2 male, mixed gender, or immature.
Floral compatibility
Compatibility experiments were conducted at Henington Pond and an in situ population at the FIU Singeltary property (25°24.070' N, 80°27.83' W). The Singeltary site was once part of the continuous Everglades ecosystem but is now separated from more western Everglades marshes by a highway, U.S. 1. The study site was in a sawgrass marsh on the eastern side of U.S. 1. Controlled pollinations were carried out during the 2002 and 2003 flowering seasons; a total of 17 sawgrass plants were pollinated in 2002 and 26 in 2003 (Ni = 43). Sawgrass reproduces clonally and can spread distances of 10 to 100 m (Ivey and Richards, 2001
). Clones become interdigitated, and a study of genotypic diversity showed that most m2 quadrats have two genotypes (Ivey and Richards, 2001
). Individual clones at the planted Henington Pond population were still identifiable, although we do not know the genotypic relations of the original plantings. The genetic relationship of culms in the FIU-Singeltary population was less clear. In an effort to maximize the number of genetic individuals used at the Singeltary site, recipient plants in controlled pollinations were more than 3–4 m from each other; Ivey and Richards (2001)
found mean distance between sawgrass clones in 11 x 2 m transects to be 3.92 m. As an additional measure to avoid duplicating genetic individuals in the Singeltary population, only one plant was used from any patch of culms that appeared to a clone.
A split-plot design was used in the compatibility experiment, in which all five pollination treatments were performed on separate branches of the fourth lateral cluster of each recipient plant's inflorescence. To assess within-plant positional differences in response to treatments, these five treatments were also completed on the second lateral cluster in 2002. On each lateral cluster, a different second-order branch within the cluster was chosen for each treatment. The number of spikelets (Ns) on each branch was counted prior to experimentation. Approximately 1 mo after flowering, fruit set in each treatment was counted to estimate the proportion of seed set per treatment. Sawgrass produces single-seeded fruit, thus fruit set is equivalent to seed set.
Our five pollination treatments were cross-pollination (CROSS), self-pollination (SELF), manipulation (MANI), autogamy (AUTO), and an open-pollinated (OPEN) treatment. Because sawgrass is wind-pollinated and controlled pollinations were carried out in the field, we used the MANI treatment (described later) as a control that accounted for exposure to ambient pollen during our pollinations. Prior to stigmas expanding on a branch, cross-pollination (CROSS), self-pollination (SELF), manipulation (MANI), and autogamy (AUTO) treatment branches were enclosed in aluminum foil packets that were tightened around the base of the branch but had open space around the spikelets on the branch. After stigma expansion, CROSS treatment foil packets were opened, and flowers were hand-pollinated by rubbing dehisced sawgrass anthers collected from another population over the exposed receptive stigmas. The foil packets were then re-closed to avoid self-pollen. A similar procedure was used for SELF treatments, except self-pollen was used during hand pollinations. Because the recipient inflorescence usually bore no dehisced anthers, pollen from the nearest flowering ramet of that clone was used for self-pollinations. MANI treatments were used to examine the effect of opening and closing bags during hand pollinations. Foil was removed from MANI branches for length of time required to uncover and hand pollinate CROSS and SELF treatments, then replaced, to insure that MANI spikelets were exposed to ambient pollen for a period equivalent to the exposure of the hand-pollinated spikelets. AUTO treatments were used to test the rate of automatic self-pollination, or autogamy, within each bag. AUTO treatments were bagged until the conclusion of the plant's flowering cycle. Open pollination treatments (OPEN) established rates of natural seed set. OPEN branches were tagged prior to stigma expansion but were not otherwise manipulated. To avoid potentially altered seed set in response to our physical disturbance of flowers during the pollinations, OPEN branches were enclosed in foil during all hand pollinations, and then unbagged for the remainder of the flowering season. An additional OPEN treatment on the fifth lateral cluster was used to estimate natural seed set on an unmanipulated branch located above other treatment branches.
Anemophilous pollen can be short-lived, with life spans ranging from minutes to days (Proctor et al., 1996
). To insure that pollen was living at the time of pollinations, viability was tested hourly after dehiscence using fluorescein diacetate (Heslop-Harrison and Heslop-Harrison, 1970
). More than 65% of sawgrass pollen was viable for at least 3 h post dehiscence, thus all pollinations were performed within this time frame. Timing of anther dehiscence varied between the Henington Pond and Singeltary sites, so controlled pollinations were carried out between 0630 and 0930 hours at Henington Pond and 0800 and 1100 hours at the Singeltary population.
Statistical analysis
In the floral compatibility experiment, differences between treatments in the proportion of seeds set were analyzed as generalized linear mixed model (GLiMM) ANOVAs. Individual culms were random subjects; sites (Singeltary and Henington Pond) and years (2002 and 2003) were treated as fixed between-subject factors. Position of the lateral cluster on the inflorescence (second or fourth lateral cluster) was treated as a random effect within culms, and treatments (AUTO, SELF, CROSS, MANI, OPEN) were fixed effects applied within lateral clusters. The response variable (fruit set = seed set/spikelet) used a logit link and binomial error. Because overall variation among the five treatments is not biologically meaningful, the GLiMM was run repeatedly for pairs of treatments that had biological interpretations of interest (e.g., SELF vs. CROSS). A separate ANOVA was run to test for positional differences in seed set between the second and fourth lateral clusters in 2002; positional differences between the fourth and fifth lateral cluster in 2003 were tested for only the OPEN treatment. All analyses were performed using the PROC MIXED procedure in SAS 8.2 for Windows (SAS Institute, 2001
).
RESULTS
Floral phenology
Flower and spikelet development
Both the gynoecium and androecium within a flower were functional for less than a day. Stigmas expanded between 0630 and 0800 hours and were dried out by 
1100. Anthers expanded and dehisced at approximately the same time as stigmas and pollen were shed throughout the morning. Bisexual flowers of sawgrass were dichogamous, with genders segregated over time. When both gynoecium and androecium were functional within a flower, stigmas and styles expanded and senesced prior to stamen maturation, which occurred either 1 or 2 d later (mean = 0.3d, SD 0.5). Thus, bisexual flowers were protogynous. In the two-flowered spikelets, flower expansion and maturation was also temporally segregated. Terminal F1 flowers emerged and senesced prior to the F2 flowers. Although located within the same spikelet, F1 and F2 floral development also differed. The F1 flowers were morphologically bisexual, but F1 carpels aborted in >96% of all inflorescences observed, so F1 flowers generally functioned as males. The gynoecium in F2 flowers developed normally, and F2 flowers functioned as bisexual flowers. Thus, sawgrass spikelets were andromonoecious and protandrous, having a functionally male F1 flower that matured first and a bisexual F2 flower that matured subsequently. Over time, the spikelet progressed through three gender phases: the initial F1 male stage, followed by the F2 female stage, and lastly by the F2 male stage. Plants that did not follow this pattern (4% of observed inflorescences) had some spikelets in which the F1 flowers were functionally bisexual and protogynous, similar to the F2 flowers. These hermaphroditic spikelets then had four gender phases: F1 female, F1 male, F2 female, and F2 male.
Inflorescence development
Floral expansion, which involved several thousand flowers per inflorescence, occurred acropetally along the inflorescence (Fig. 1). Flowering was relatively synchronous within an inflorescence. Each gender stage took 2 d to fully expand along the inflorescence, with less than 1 d between each stage, so inflorescences took 6–7 d to complete flowering (SD 1) (Fig. 1). Thus inflorescences switched sexes twice over the week (Fig. 1). Asynchronous flowering, in which both sexes were present contemporaneously on an inflorescence, occurred in <17% of observed inflorescences (Ni = 17, Nc = 8). These mixed sex inflorescences were more prevalent in 2003 than in 2002, occurring on 13 inflorescences in six of 11 clones.
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Population phenology
At Henington Pond, sawgrass flowered from the second week of May to the second week in June in both years sampled (Fig. 2). A total of 144 inflorescences expanded in 2002, compared to 118 in 2003. A week after the first inflorescences expanded, flowering peaked within the population, with 49 and 27 blooming inflorescences in 2002 and 2003, respectively (Fig. 2). The four inflorescences with F1 females flowered early in 2003, initiating the flowering cycle in the first 3 d of the season (Fig. 2). Asynchronous or mixed inflorescences were observed only in the first 8 d of the flowering season of both years (Fig. 2).
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Within plant differences
AUTO and OPEN treatments performed on fourth lateral clusters produced higher seed set than the same treatments on the second lateral cluster flowers (Table 2). Seed set resulting from either hand pollinated (SELF and CROSS) or MANI treatments did not differ between lateral clusters (Table 2). Although OPEN treatments differed in second and fourth lateral cluster seed set (Table 2), position did not influence fourth and fifth lateral cluster seed set over both years (P = 0.1004). Open pollinations over these years produced 55% (Ns = 1061, SD 31) and 52% (Ns = 836, SD 34) seed set on the fourth and fifth lateral clusters, respectively.
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Breeding system
Our results show that sawgrass is self-compatible. Although empirical studies within the family are limited, this self-compatibility in sawgrass agrees with data from other Cyperaceae, including some species of Carex (Davies, 1955
; Faulkner, 1973
; Pojar, 1974
; Handel, 1976
, 1978
; Vonk, 1979
; Schmid, 1982
; Standley, 1985
; Whitkus, 1988
; Dunlop, 1999
), but contrasts with a report of self-incompatibility in Scirpus maritimus (Charpentier et al., 2000
).
Sawgrass plants are dichogamous with respect to flowers, spikelets, and inflorescences. Although sawgrass can self-fertilize, the temporal separation of sexes encourages outcrossing (Stout, 1928
). Most inflorescences are protandrous, but variation in sex expression in the F1 flower means that occasionally plants are protogynous. Dichogamy is complete in flowers and spikelets, meaning there is no overlap of pollen and stigma presentation (Lloyd and Webb, 1986
), and it is usually complete in inflorescences. This separation of timing both promotes outcrossing and avoids interference between pollen and stigma function (Lloyd and Webb, 1986
). The F1 anthers abscise after they function, before the F2 stigmas expand, so stigmas on spikelets in the female phase are relatively unobstructed in the open lateral clusters. The tri-phase complete dichogamy seen in sawgrass is called duodichogamy, in which there are 1
"male/female" cycles in a flowering season (Lloyd and Webb, 1986
). Duodichogamy typically has male phases before and after a single female phase (Lloyd and Webb, 1986
), as we found in sawgrass.
Genets of sawgrass are hemisynchronous (Lloyd and Webb, 1986
); inflorescences on different clonally produced ramets do not flower synchronously. Sawgrass is sympodial, producing rhizomes that initially grow horizontally and bear bracts, then turn up and begin producing foliage leaves in a rosette. This orthotropic stem produces adventitious roots and additional horizontal rhizomes, as well as the terminal inflorescence. Rhizome connections between the orthotropic shoots are lost over time. Inflorescences on the ramets produced by this clonal spread can flower at different times; this genet asynchrony means that geitonogamous pollinations can occur (Handel, 1985
; Bhardwaj and Eckert, 2001
). Thus sawgrass has the potential to have a mixed-mating system, where both crossing and selfing occur in the population (Richards, 1997
). We do not know the relative proportions of these two modes of reproduction in sawgrass, but the data on compatibility response and reproductive phenology presented here suggest that rates of outcrossing vs. selfing will depend on factors such as size of the clone, number of flowering ramets, and timing of flowering among ramets (Chung and Epperson, 1999
), as well as the competitive ability of cross- vs. self-pollen (Lloyd and Schoen, 1992
). The degree of outcrossing vs. selfing thus should be independent of the abiotic factors known to affect wind pollination.
Spikelet dichogamy has been described in the Cyperaceae (Standley, 1985
; Whitkus, 1988
, 1992
; Charpentier et al., 2000
), although asynchrony of flowering in spikelets was found to promote geitonogamy in clones of Carex (Vonk, 1979
; Whitkus, 1992
). The marked inflorescence dichogamy observed in sawgrass, however, has not been reported for the family. Simple observations of flowering phenology in other sedges could provide a basis for initial hypotheses about the degree of outcrossing vs. selfing.
Whether sawgrass flowers and spikelets are protandrous or protogynous depends on whether or not the F1 gynoecium aborts. F1 ovule abortion varied within an individual, a population, and over time, as well as among populations (Richards, 2002
). We found F1 ovule abortion to vary in Henington Pond plants from 100% in 2001 (Richards, 2002
) and 2002 to 92% in 2003 (Fig. 2). Thus, spikelet sex expression, with the accompanying phenological changes, may vary at the individual lateral cluster, ramet, and genet levels. Because ovule abortion in sawgrass is plastic, it may be a strategy to optimize fitness through resource allocation. Shifts by Sagittaria trifolia (Alistmataceae) from protogyny to functional protandry during early blooming events were hypothesized to serve as a strategy to conserve resources via ovule abortion (Huang et al., 2002
).
Sawgrass was not pollen limited at the fourth lateral cluster in either the ex situ or in situ populations, because hand pollinations and open pollinations produced similar seed set (Figs. 3, 4; Table 1). Hand pollinations also had similar seed set between the second and fourth lateral clusters (Table 2). In open pollinations, we observed that basal clusters had a lower proportion of seed set (Table 2), contrary to the frequently observed pattern of acropetal decline (Diggle, 1995
). Reduced seed set in these clusters likely resulted from reduced pollen availability. Spikelet density is greatest in basal clusters (Richards, 2002
), and these clusters are closest to the rosette of linear leaves. Airborne pollen thus may lodge in either the foliage or the denser clusters themselves.
Our results indicate that intrafloral fertilization is not typical for sawgrass, as autogamy treatments produced negligible seed set. These results are also supported by the phenology data, which showed at least 1 d separating male and female function in both flowers and spikelets, as well as by our observations on stigma longevity in the field and on pollen viability. Although some seed was set in the autogamy treatment, the amount decreased from 2002 to 2003, paralleling a decrease in seed set in the manipulation treatment. We think this seed set was an artifact and attribute the change over time to improvement in our technique. Although we did not test for agamospermy, the low levels of seed set in the AUTO and MANI treatments suggest that it is unlikely in sawgrass.
Seed set was lower in plants from the natural population across all treatments in both years. Differences in resource availability between populations are suspected to cause the disparity between seed set rates. In contrast to natural populations, the transplanted population at Henington Pond had water throughout the year and elevated nutrient levels as a result of fertilizer application to the bordering lawn. Reduced seed set may be a metabolic trade-off under stressed and/or low nutrient conditions, where nutrient allocation patterns are phenotypically plastic (Charnov, 1982
; Reznick, 1985
; Biere, 1995
; Elle, 1999
). Resource limitation in the natural population may also have influenced maternal and/or paternal performance from reduced pollen quality, quantity, and/or successful seed development (Byers, 1995
; Elle, 1999
).
Anemophily
Wind pollination is arguably the most common plant pollination system in terms of numbers of individuals because it is the predominant mode of pollination in grasses, sedges, conifers, and many temperate deciduous trees; these species dominate grassland, savannah, temperate and boreal forest, and taiga biomes. Despite this, anemophily has been poorly studied (Harder, 2000
). Anemophily is considered to be common in dry environments and open habitats and rare in the tropics (Regal, 1982
; Culley et al., 2002
). These generalizations ignore the predominance of wind-pollinated species in savannah habitats and in tropical wetlands, both of which are dominated by anemophilous graminoid species.
We have limited understanding of the reproductive strategies of anemophilous plants in these tropical environments. Southern Florida, although located in the subtropics, has a seasonal wet–dry climate typical of many tropical and subtropical regions (Duever et al., 1994
). In our study, sawgrass flowered during May. In the Florida Everglades, May is a transitional month between the winter dry season and the summer wet season (Duever et al., 1994
). Temperatures in May are warm, and rainfall is variable but primarily comes in the summer rainfall pattern, with thunderstorms building up through the morning and releasing in the afternoon (Duever et al., 1994
). Precipitation events drastically decrease the amount of airborne pollen (McDonald, 1962
), so sawgrass plants maximize pollination by releasing pollen synchronously in the drier, warm morning hours, avoiding the afternoon thunderstorms. Sawgrass's relatively short flowering season and the fact that male and female parts of the flowers function for a single morning may have been selected to optimize sexual reproduction in this subtropical climate.
Another tropical anemophilous species, Trophis involucrate (Moraceae), also sheds pollen during the early morning hours of the dry season in lowland rainforests of Costa Rica (Bawa and Crisp, 1980
). Bullock (1994)
found the flowering season for several anemophilous neotropical tree species in Mexico to peak during this same transition from dry to wet seasons. In addition to optimizing pollen dispersal by flowering during drier periods, plants that bloom at the end of the dry season shed seeds in the following wet season. For sawgrass, its floating seeds can disperse while the Everglades have standing water and germinate in the subsequent dry period (Alexander, 1971
).
We do not know how sawgrass reproductive phenology in southern Florida compares to sawgrass phenology in habitats with different climatic patterns, such as cold wet winters or dry summers. Cladium jamaicense is distributed north to Virginia, west to Texas, and south into northern South America (Tucker, 2002
), so the species grows in a range of climatic conditions. Accounts of reproductive phenology in C. jamaicense vary from "spring–summer" fruiting (Tucker, 2002
) to "summer–fall" reproductive season (Wunderlin and Hansen, 2003
). This disparity may reflect phenotypic variation in sawgrass flowering from north to south, with southern Florida having the earliest U.S. flowering season. Alternatively, the infructescences that develop from the inflorescences are prominent summer to fall throughout Florida. Information on reproductive phenology in sawgrass, as well as other large graminoids, may often reflect observations of these more long-lasting stages of the reproductive cycle rather than actual flowering.
Because sawgrass is the dominant macrophyte in the Everglades, it probably saturates the air with pollen during its burst of flowering. How the seasonal and diurnal flowering phenology of other anemophilous graminoid species in the Everglades compares to that of sawgrass is unknown. Although abiotic factors are usually considered to be the selective forces that drive evolution of reproductive characters in wind-pollinated species, biotic factors can also be important (Culley et al., 2002
). We do not know whether pollen of one wind-pollinated species can interfere on stigmas of another, although several studies suggest that this does not happen (Honig et al., 1992
; Linder and Midgley, 1996
). Additionally, studies that have examined whether anemophilous communities seasonally partition the timing of sexual reproduction among species have not found evidence for such dispersion (Rabinowitz et al., 1981
; Bolmgren et al., 2003
).
Techniques to study compatibility in wind-pollinated species
Many wind-pollinated species are either trees or large herbaceous perennials. Greenhouse studies of the incompatibility relations of such species are often limited by the time and space needed to grow sexually reproductive individuals. Field studies are thus most feasible for research on the reproductive biology of these species. We found two techniques especially useful for studying compatibility relations of sawgrass in the field. Our pollination manipulation (MANI) treatment allowed us to interpret results of the other hand-pollination treatments. Some amount of non-treatment pollination likely occurs when doing hand pollinations outdoors in wind-pollinated species. Such pollination could especially affect interpretations of self-pollination treatments in a self-incompatable species. Exposing unpollinated stigmas for the same amount of time required to do hand pollinations allows quantification of the effect of this non-treatment pollination.
A second informative control was the use of an open pollination treatment on an unmanipulated branch in the same region of the inflorescence. In our experiment, this was the comparison of open pollinations on the fifth lateral cluster, which we did not use for other treatments, and open pollinations on the fourth lateral cluster, where we did our treatments. We found no seed set differences between open pollinations on the fifth lateral cluster and the fourth lateral clusters, which indicated that hand pollination treatments did not artificially increase or decrease open pollination rates. Application of these techniques should improve our ability to study compatibility relations of large, wind-pollinated species in situ.
FOOTNOTES
The authors thank Tom Philippi, Suzanne Koptur, David Lee, and Ralph Saporito for their constructive comments on earlier versions of the manuscript, and Wendy Wilsdon for her assistance in the laboratory and field. This research was supported by a grant from the Florida International University Office of the Provost. Wendy Wilsdon received assistance from a Research Experiences for Undergraduates award to the Florida Coastal Everglades Long Term Ecological Research (FCE LTER) grant (National Science Foundation grant no. 9910514). This is Florida International University's Southeast Environmental Research Center (SERC) Contributed Paper No. 245. 
2 Author for correspondence (e-mail: jmsnyder{at}ucdavis.edu
) current address: Department of Environmental Science and Policy, University of California, One Shields Avenue, Davis, California 95616-8573 USA
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