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2 Department of Biological Sciences, University of Nevada, 4505 Maryland Parkway, Box 454004, Las Vegas, Nevada 89154-4004 USA; 3 University Herbarium, Jepson Herbarium, and Department of Integrative Biology, 1001 Valley Life Sciences Bld., #2465, University of California, Berkeley, California, 94720-2465 USA; and 4 T.H. Morgan School of Biological Sciences, 101 Morgan Bld., University of Kentucky, Lexington, Kentucky 40506-0225 USA
Received for publication September 21, 1999. Accepted for publication February 4, 2000.
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ABSTRACT |
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:1
). The "cost of sex hypothesis" derives from allocational theory and predicts that the sex which is most expensive should be the rarer sex. This hypothesis, which, as considered here represents the realized cost of sexual reproduction, is contingent upon two assumptions that are explored: (1) that male sex expression is more expensive than female sex expression, and (2) that sexual reproduction is resource limited. Using inflorescence biomass and discounting sperm, male sex expression was found to be in the neighborhood of one order of magnitude more expensive than female sex expression, and this difference is reflected in higher numbers of gametangia per male inflorescence, presence of paraphyses in male inflorescences, and a much longer developmental time for male inflorescences. The realized cost of female reproduction from two communities dominated by S. caninervis was found to be lower than the realized cost of male sexual reproduction. Resource-limited reproduction was assessed by determining the frequency of sporophyte abortion, the age distribution of sporophyte abortions, and patterns of sporophyte abortion that may be density dependent. Among ten sexually reproducing populations, abortive sporophytes occurred at a frequency of 0.64. Abortive sporophytes averaged 8% the mass of mature sporophytes, and cohort sporophytes from the same individual female were found to abort in a density-dependent pattern. We conclude that the two assumptions, upon which the cost of sex hypothesis depends, are supported.
Key Words: allocation • bryophyte • cost of sex • cryptogamic crust • desert • haploid dioecy • sex ratios • sporophyte abortion • Syntrichia caninervis.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Goldman and Willson, 1986
). This derives in part because the two sexes perform different reproductive functions, and it therefore follows that different resource demands will be placed on each sex. Males and females of dioecious species exhibit divergent resource allocation patterns (Lloyd and Webb, 1977
; Korpelainen, 1992
), as follows. Up to anthesis, male reproductive effort usually exceeds female reproductive effort. However, from fertilization through seed set, the heavy allocation to seeds and fruits results in female reproductive effort far exceeding male reproductive effort, with very few exceptions (e.g., Wolfe and Shmida, 1997
). Phenotypic patterns in dioecious species commonly observed and resulting from differential resource expenditures include (1) male-biased sex ratios, (2) greater ramet production from males (more shoots per genet), (3) greater longevity in males, (4) production of larger male shoots, (5) higher growth rates for males, and (6) increased flowering frequency of males (Grant and Mitton, 1979
; Meagher, 1981
; van Damme and van Delden, 1984
; Lokker et al., 1994
; Richards, 1997
). A consequence of this asymmetry in reproductive effort between the sexes may be gender specialization, where the sexes segregate along environmental gradients. In the cases studied, male individuals are usually more common in the more highly stressed habitats along gradients of salinity, moisture, nutrients, light, and temperature (Freeman, Klikoff, and Harper, 1976
; Cox, 1981
; Bierzychudek and Eckhart, 1988
; Lovett Doust and Lovett Doust, 1988
; Dawson and Ehleringer, 1993
; Ramadan et al., 1994
). Thus, in dioecious (and gynodioecious) species, owing in part to a sharp asymmetry in reproductive investment that may negatively affect the fecundity of the population, one gender may very often be at a competitive disadvantage with respect to the other (Richards, 1997
).
The dioecious condition is much more widespread in bryophytes (>60% of species; Wyatt and Anderson, 1984
) than in seed plants (5%; Richards, 1997
). In bryophytes, sex is expressed in the haploid, gametophyte generation and is generally held to be under genetic control through segregation of X and Y chromosomes at meiosis (Ramsay and Berrie, 1982
). Despite an expected sex ratio at meiosis of 1:1, the predominant pattern among the 
30 species of dioecious bryophytes studied is that of female dominance among sex-expressing individuals (Longton, 1990
; Shaw and Gaughan, 1993
; Stark, Mishler, and McLetchie, 1998
). The frequent occurrence of female-biased sex ratios in bryophytes is inconsistent with the idea that there is a higher cost of reproduction in females compared to males. However, no study exists that quantifies the level of reproductive allocation (measured as biomass) in females and males in bryophytes. Nevertheless, it is usually assumed that, as in seed plants, females invest more in sexual reproduction (and have higher reproductive success) than males. This absence of data may result from the assumption that female individuals bear the majority of reproductive costs, since it is the female plant which largely supports the early growth and development of the sporophyte generation (Proctor, 1984
). This paper assesses the apparent paradox seen in bryophytes—a female-biased sex ratio while at the same time the female sex incurs the greater cost of reproduction—by proposing a hypothesis and investigating the two contingent assumptions of this hypothesis.
The cost of realized sexual reproduction hypothesis and its two contingent assumptions
Recent investigations into the sex ratio and distributional ecology of the dominant desert moss Syntrichia caninervis Mitt. revealed an extremely skewed sex ratio. Female ramets outnumbered male ramets in two communities, from 14:1 at an elevation of 1494 m, to 1:0 at an elevation of 750 m (Stark, Mishler, and McLetchie, 1998
; Bowker et al., 2000). Our unpublished investigations into the other Mojave Desert dioecious species in the genera Didymodon, Syntrichia, and Bryum indicate that this pattern of extreme male rarity is prevalent. Extreme evolutionary manifestations of this pattern include the xeric female-only species of Didymodon nevadensis Zand., Syntrichia chisosa (Magill, Delg. & Stark) Zand., and Syntrichia bartramii (Steere in Grout) Zand., with no known corresponding xeric male-only species.
We propose a hypothesis to account for the female-biased sex ratio in S. caninervis, called here the "cost of realized sexual reproduction hypothesis": male rarity in adults is a product of a higher prezygotic reproductive load incurred by male individuals (introduced in McLetchie, 1992
). A primitive sexual reproduction system that depends upon external water without sperm vectors, coupled with the juxtapositioning of male and female individuals, can result in a rarity of sexual reproduction. When sexual reproduction is rare (i.e., occurring in <3% of female populations; Bowker et al., 2000), the cost incurred by the female sex is restricted to gametangial production (females are sperm limited). That is, since females relatively rarely realize their full cost of sexual reproduction (from gamete production through sporophyte maturation), on average, males incur a greater cost if the cost of producing gametangia is higher for males. We propose that female-dominated sex ratios in dioecious mosses may be a product of a higher average realized cost of sexual reproduction in males. In order for this hypothesis to be viable, we must demonstrate that (1) sexual reproduction is resource limited and (2) that the cost of reproduction is indeed greater for males. Allocational studies in bryophytes are probably rarely attempted owing to the exceedingly small structures produced (gametangia) with resulting difficulty in partitioning these structures for allocation assessment. This paper explores the above two contingent assumptions of this hypothesis, as a first step toward evaluating the overall hypothesis. Predictions of these two contingencies include the following: (a) the biomass of the male inflorescence (perigonium) exceeds the biomass of the female inflorescence (perichaetium); (b) gametangial number is greater in male inflorescences; (c) a longer duration is required for maturation of the male inflorescence; (d) male inflorescence and sporophyte biomass constitute a significant portion of annual production; (e) sporophyte abortion is common; (f) most sporophytes abort early in development; and (g) a density-dependent sporophyte abortion pattern occurs.
Biology of Syntrichia caninervis
In the Mojave Desert, S. caninervis occupies the xeric portion of an elevation gradient that extends to two closely related species: S. ruralis (Hedw.) Web. & Mohr at intermediate elevations and S. norvegica Web. at the highest elevations (Oliver, Mishler, and Quisenberry, 1993
). Syntrichia caninervis is differentiated from its close relatives in the S. ruralis complex by its bistratose leaves and substereid costal cells (Flowers, 1973
, as Tortula bistratosa Flow.; Kramer, 1980
; Mishler, 1985
). At low to middle elevations in the Mojave Desert, S. caninervis is the dominant species of bryophyte, exhibiting the third highest percent cover of all plants in the Coleogyne community (6%), a vegetation belt that constitutes one of the most widespread vegetation zones in the southwestern United States (Smith, Monson, and Anderson, 1997
; Bowker et al., 2000). Large populations of S. caninervis populations are often situated along the north-facing bases of Coleogyne shrubs, while smaller and more diffuse populations occur in exposed habitats. This is a perennial species capable of clonal growth, and where mature individuals may not have expressed sex, i.e., neither sex expression nor sexual reproduction is required for long-term survival. Through the assessment of internal stem markers, annual growth rates were found to be very low, 0.36 mm/yr, with the probability of expressing sex (producing an inflorescence) also low, 0.09 per ramet (Stark, Mishler, and McLetchie, 1998
). Sex expression was dependent upon the size of the ramets and the degree of exposure of the inhabited microsite: larger ramets expressed sex significantly more frequently than smaller ramets, and shaded ramets expressed sex significantly more frequently than exposed ramets. Increased soil moisture in shaded microsites in the days immediately following rainstorms may be responsible for extending the period of hydration in shaded microsites (Bowker et al., 2000).
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MATERIALS AND METHODS |
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Field sampling
Ten sporophytic populations were located, each of which contained at least one current-cycle sporophyte, i.e., a sporophyte from the most recently matured cohort. The rarity of sporophytic populations precluded random selection; the study site was systematically searched in the summer of 1998 until the ten sporophytic populations were found. From each population, a 2 x 2 cm core was removed that included at least one current-cycle sporophyte, along with the associated 2-cm layer of soil beneath the plants.
Isolation of individual plants
A current-cycle sporophyte was randomly selected from each 2 x 2 cm population core. The individuals immediately surrounding this sporophyte were further subsampled using 15–30 x 15–30 mm cores. Each of these cores of individuals was gently agitated in a watch glass containing a shallow layer of water to remove large soil particles. In a 20-mL scintillation vial, the core or fractions thereof was vigorously shaken in water to remove finer soil particles. This step was repeated as necessary in order to tease apart and to further cleanse individuals without manual dissection. An "individual" was defined as an organically connected set of ramets, and no assumption was made regarding the potential genetic identity of these individuals. The product of this step was either separated individuals or groups of adhering individuals. In a 20-mL scintillation vial, groups of adhering individuals were placed in water and shaken vigorously until individual plants were separated (30–90 sec). Individuals were then manually separated, with care to avoid severing connected ramets. Thirty individuals were then randomly selected from this group of individuals for further study. As a final cleansing step, each individual was again washed in a 20-mL scintillation vial to remove most remaining fine soil particles. If a ramet detached from an individual during the final cleaning wash, it was still considered as part of the individual, provided a clean break point could be established. Individuals were allowed to air-dry in labeled micropackets, and then oven dried to constant mass at 60°C for at least 3 d.
Individual dissections
Each individual was hydrated on a microscope slide, and leaves were removed along the stem, exposing inflorescences and sporophytes from previous years and the current season. Annual growth intervals were recognized using internal markers described in Stark, Mishler, and McLetchie (1998
: stem coloration, leaf base appearance, lateral bud position, and inflorescence position). These internal markers were used to identify cohorts of sporophytes, i.e., sporophytes sharing the same year of fertilization. The denuded individual was checked for diploid tissue (abortive, previous-cycle, old sporophyte fragments, or recent-cycle sporophytes). If present, the diploid tissue was carefully separated from haploid tissue, excepting haploid tissue whose growth is stimulated by fertilization (vaginular tissue and embryonic calyptral tissue). Sporophytes, including abortive, previous-cycle fragments of sporophytes, and operculate sporophytes, were excised at their bases and placed in labeled micropackets, oven dried for 3 d at 60°C (to constant mass), and weighed on a Cahn microbalance to the nearest 0.1 µg. Recognition of sporophyte abortions included (1) tissue brown (dead), (2) diploid tissue withered, (3) fungal colonization present, and (4) the sporophyte represented a pre-1998 fertilization. Some polysetous abortions probably went unaccounted if paired with a mature sporophyte, especially a fragmentary sporophyte.
For estimating the mass of inflorescences, the three most recent cycles of vegetative growth were used. After removing the specialized leaves surrounding each inflorescence, the inflorescence was carefully excised at the "bed" (the tissue supporting the bases of gametangia), a wet mount was made, gametangia and paraphyses were counted using a compound microscope, and the dissected inflorescence was then placed in a micropacket and air dried. The specialized perichaetial and perigonial leaves could not be included in allocational analyses because these leaves had to be torn away in order to determine sex. However, no male/female dimorphism with respect to size or shape of these leaves was noted. When the micropacket contained >5 inflorescences of the same sex, the contents were oven dried for 3 d at 60°C to constant mass, and weighed using a Cahn microbalance to the nearest 0.1 µg. No attempt was made to omit abortive gametangia that were frequently encountered in perichaetia. Since male and female individuals exhibit no size differences (unpublished observations), allocation data are presented as absolute values. The developmental time for inflorescences was estimated using inflorescence location along the stem in conjunction with known stem architectural patterns discussed in Stark, Mishler, and McLetchie (1998)
. For estimating the mass of a growth interval, the interval (leaves and stem) was carefully excised and placed in a micropacket, dried, and weighed as above. Sex of the stem was not assigned.
Average realized cost of sexual reproduction
For these estimations, we used community-wide sex expression data from previous studies at two study sites: the present site (Bowker et al., 2000) and a low-elevation site (Stark, Mishler, and McLetchie, 1998
). Such data on sex expression were coupled with the information on inflorescence allocation from the individual dissections of the present study. Therefore, we calculated the mean cost of sexual reproduction for those ramets (not individuals) expressing sex, using sex expression frequency data from previous studies and allocational averages from the current study. For the high-elevation site, two methods were employed to assess the sex expression across the community: (1) a community-wide sampling of 890 ramets from 89 populations, and (2) an analysis of 30 randomly located shaded and exposed populations paired to a blackbrush shrub (described in Bowker et al., 2000). These data are pooled in our analyses and represent a random sampling of ramets from a total of 119 populations of S. caninervis. For the low-elevation site, a total of 481 ramets were randomly sampled from 16 populations (described in Stark, Mishler, and McLetchie, 1998
). Please note that at these two study sites sex expression was presented on a ramet, rather than individual, basis, which thus diverges from earlier sets of observations on individual dissections. However, since allocation data are presented in absolute annual values, the unit used, ramet or individual, does not affect the results. Of the ramets expressing sex at each site, the cost of sexual reproduction incurred by a female ramet was taken as the biomass of a single perichaetium plus the biomass of the sporophyte, provided that fertilization had occurred at any time during the life span of that ramet. The cost of sex incurred by a male ramet was simply the biomass of a single perigonium. Thus the results represent the cost of production of structures of sexual reproduction during a year in which sex is expressed, as opposed to an annual average cost of sex for the ramet. Furthermore, this estimate represents a maximum cost for females, since sporophytes are seldom produced each year on the same female ramet.
Statistical analyses
We used 2 x 2 contingency tables to test for an association between sporophyte condition (matured or abortive) and cohort type (same or different cohort) and 2 x 4 contingency tables to test for an association between sporophyte condition (matured or abortive) and number of sporophytes per individual (1, 2, 3, or 4). These tests were performed using the Statistical Analysis System (SAS, 1994
). Two-tailed t tests assuming unequal variances were used to compare mean gametangial number per inflorescence between female and male individuals.
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RESULTS |
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Sporophytic allocation patterns
Sporophyte mass was assessed at four possible phases in its life history: abortive, operculate, previous-cycle, and fragmented (Fig. 4). Abortive sporophytes were predominantly arrested in the embryonic phase of development (Figs. 2, 3). Operculate sporophytes had the full complement of spores, whereas previous-cycle sporophytes differed in having dehisced their spores at least 1 yr prior to sampling. Fragmented sporophytes ranged from only the foot and associated vaginula persisting on the stem, to naked setae or partially intact capsules. These fragments represented relatively old sporophytes that had begun to deteriorate, normally greater than 3 yr of age.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Finding males to incur a greater cost to sexual expression than females was not unanticipated. In >80% of species studied (N = 96), antheridia are initiated prior to archegonia and take longer to mature (Lackner, 1939
), suggestive of a greater metabolic cost associated with the production of the more complex and numerous male gametes. This process is probably compounded in deserts where water required to mature gametangia is limiting: in low desert populations of the moss Tortula inermis (Brid.) Mont., the most xeric habitat to be studied in this regard, the antheridial maturation period is the longest on record, requiring at least 12 mo; this compares to archegonia of the same species initiating and maturing in the same winter (Stark, 1997
). In addition, analyses of numbers of gametangia per inflorescence and numbers of inflorescences per stem indicate that in all five dioecious species studied, prezygotic reproductive effort is higher in males (Longton and Greene, 1969
; Deguchi and Yananose, 1988
; Miles, Odu, and Longton, 1989
; McLetchie, 1992
). Perigonia in S. caninervis have a much greater biomass than perichaetia, even subtracting sperm. This greater size (illustrated in Fig. 1) is due to a larger mean gametangial number and the numerous paraphyses that proliferate upon antheridial maturation. The relatively high cost of expressing sex on the part of a male individual of S. caninervis is perhaps mitigated by initiating the perigonium in the first winter and maturing it during the second winter (i.e., spreading out the investment). Clearly, the need exists to measure alternative currencies to biomass (e.g., caloric value, nutrient content; Goldman and Willson, 1986
) to assess the cost of male and female sex expression. Given the lipid-rich nature of sperm cells (Paolillo, 1979
), it is reasonable to assume that expressing males require nutrients that expressing females do not require. This limitation alone may serve to preferentially hinder the survival of male individuals in a population, if, for example, the sperm requirement entails a trade-off with desiccation tolerance.
Male reproductive load is expected to be lower in selfers compared to outcrossers (Charlesworth and Charlesworth, 1981
; McKone, 1987
). In mosses, if we assume monoecious (bisexual) species to be selfers, we would expect male reproductive load to be lower than in related dioecious species. In the desert, we can comment on two monoecious species in the same family, and compare these to S. caninervis. In both Trichostomum sweetii (Bartr.) Stark and Tortula inermis, perigonia are produced just below the perichaetium and consist of seven antheridia per growth interval in T. sweetii, and ten antheridia per perigonium in T. inermis (Stark and Castetter, 1995
; Stark, 1997
) This compares to a mean of 19 antheridia per perigonium in the dioecious S. caninervis.
Owing to the presumed high cost of sporophyte maturation, fertilized females are expected to incur a far greater total reproductive cost than males. This high cost is borne out by findings reported here, with operculate sporophytes reaching a biomass slightly greater than net annual vegetative production. For this to result in a higher realized cost of sexual reproduction for females, however, the majority of females expressing sex would need to be fertilized and thus incur the cost of maturing a sporophyte. Unlike females, male individuals expressing sex always realize their total cost of sexual reproduction, and this cost is equivalent to the cost of sex expression. Our evidence suggests that fertilization is sufficiently rare in desert populations of S. caninervis to conclude that females are highly sperm limited, and thus their realized cost of sexual reproduction is roughly equivalent to their cost of expressing sex. To our knowledge, there are no examples of dioecious seed plants where female individuals frequently remain unfertilized. However, this life history pattern is probably widespread among dioecious species of bryophytes, particularly arid species, given the low frequencies of sporophytic populations in these taxa (Rohrer, 1982
; Stark and Castetter, 1987
). In dioecious flowering plants, biomass allocated to male function usually exceeds that allocated to female function through anthesis. However, female investments accelerate after pollination, and nearly always exceed that of males due to fruit maturation (Goldman and Willson, 1986
). Cross-pollinated plants with inefficient pollination mechanisms (e.g., wind-pollinated species) will have lower male fitness than will efficiently pollinated species and thus should devote correspondingly more resource to male function (Richards, 1997
). Therefore, a parallel may be drawn between angiosperms and S. caninervis, in that the inefficient gamete dispersal mechanism in dioecious mosses has selected for a greater male reproductive effort at the level of the individual. We also note that female reproductive success is first limited by sperm (and then subsequently limited by resources), a pattern true in perhaps a third of all angiosperms (Burd, 1994
).
Differentials between the sexes in regard to the cost of sexual reproduction are meaningless unless sexual reproduction depends upon the availability of resources. Surplus flowering, where a species commonly produces more flowers than mature fruits, is present in most flowering plant species. One hypothesis to explain surplus flowering (among several, see Sutherland and Delph, 1984
) is that it serves to match an uncertainty in the availability of resources or pollen. One means of approaching potential resource limitations during reproductive events in plants is to study patterns of fruit abortion (e.g., Stephenson, 1981
; Elmqvist, Agren, and Tunlid, 1988
). The structure in bryophytes that is analogous to the fruit of flowering plants is the sporophyte; both structures are in part nutritionally dependent upon the maternal plant. Reports of sporophyte abortion are infrequent. In the pleurocarpous, dioecious Pleurozium schreberi (Brid.) Mitt., a frequency of abortive sporophytes of 38% was found in a survey of six stems and 114 sporophytes; the abortions occurred early in development (Longton and Greene, 1969
). In polar populations of the same species, the frequency of abortion increased to >50% (Longton, 1988
). In Pennsylvania populations of the pleurocarpous, monoecious Entodon cladorrhizans (Hedw.) C. Muell., the overall frequency of sporophyte abortion across five populations was 20% (172 of 846 sporophytes; Stark and Stephenson, 1983
). The most active period of translocation of resources from gametophyte to sporophyte occurs during capsule expansion (Chevallier, Nurit, and Pesey, 1977
; Proctor, 1977
); thus maternal investment should be made as early as possible. Our data suggest that spore + operculum biomass accounts for up to 47% of total sporophyte biomass (mass of operculate sporophytes subtracting the mass of previous-cycle sporophytes). In the monoecious Tetraphis pellucida Hedw., as experimental shoot density increased, the proportion of sporophyte abortions increased along with the proportion of male shoots, suggesting to the author that resource limitations associated with high shoot densities may cause the plants to switch to male shoot production, which costs less than sporophytic females. Furthermore, the biomass of the sporophyte of Tetraphis pellucida constituted 41% of the shoot (gametophore) mass (Kimmerer, 1991
). Since each female of S. caninervis was assessed over her entire multiyear life span, the high incidence of sporophyte abortion indicates that this high frequency does not result from a single aberrational season. Given the poikilohydric nature of bryophyte growth and reproduction, the high frequency of sporophyte abortion coupled to the desert habitat is likely not coincidental. Furthermore, this abortive frequency of 0.64 is likely to be an underestimate for the species as a whole in the Mojave Desert; the value derives from upper elevational mixed-sex populations bearing mature sporophytes and ignores mixed-sex populations that have not produced mature sporophytes, especially those at lower elevations. Several mixed-sex populations have been identified at the study site that are productive only of abortive sporophytes (Stark, unpublished observations).
Two questions surface with regard to the abortion patterns of sporophytes observed in S. caninervis. First, one might question why the sporophyte, rather than gametophytic branches, is preferentially aborted. Such a pattern of abortion would suggest a greater fitness value for asexual reproduction. Alternatively, since branches (ramets) represent potentially photosynthetic sources, whereas sporophytes represent current photosynthetic sinks, the individual is seen to be "cutting its losses." Second, given that sporophytes undergo a summer dormancy phase as embryos as part of their normal development, the question can also be raised as to why the sporophyte development cannot be extended to two summers of dormancy, if resource-limiting conditions prevail during the winter months. One possible explanation may include a minimum embryonic size, beyond which summer dormancy is unable to be attained, noting that it is the summer wet/dry cycles that probably impose a significant metabolic cost on survival (Oliver, 1991
).
Most flowering plants abort fruits at or near 10% of mean mature fruit biomass; this early abortion presumably allows maternal plants to conserve on limited resources, in addition to allowing maternal regulation of offspring quality in some species (Stephenson, 1981
; Stephenson and Winsor, 1986
). Similarly, if resources are in short supply (e.g., water) in desert populations of S. caninervis, fertilized female plants are expected to abort most sporophytes early in development. Mean biomass of abortive sporophytes reported here was 8% of operculate sporophyte biomass, consistent with fruit abortion patterns. The greatest expense incurred by the partially parasitic sporophyte appears to coincide with capsule expansion and meiosis, i.e., spore formation. Given the high cost of male sex expression, one might expect male individuals to regulate resource allocation via antheridial abortion. While gametangial abortion was not assessed in the present study, males could regulate resource allocation detrimental to their survival by varying the number of antheridia matured or the regulation of sex expression itself.
Density-dependent abortion patterns have been reported previously for two monoecious species of mosses, Entodon cladorrhizans and Phascum cuspidatum Hedw. (Hughes, 1979
; Stark and Stephenson, 1983
). Each of these species initiated more sporophytes in a given year than it matured, either within the same inflorescence (Phascum) or among multiple inflorescences (Entodon). In pleurocarpous mosses, multiple perichaetia are initiated and matured each growing season, resulting in sporophyte cohorts along the same ramet. However, in the dioecious and upright S. caninervis, at most a single perichaetium is initiated and matured each season at the apex of each ramet. Each individual may have multiple ramets, so it is possible for an individual to initiate more than one sporophyte per season. Such sporophytes would be considered "cohorts," since they are initiated in the same year, albeit on different ramets. Thus a distinction is made between the cohorts of E. cladorrhizans (same ramet) and the cohorts of S. caninervis (different ramets). Conclusions suggested from these findings are that (1) a shortage of resources available for sporophyte maturation exists and (2) ramets of an individual are not necessarily nutritionally independent units, despite potential separations of multiple annual growth intervals (a finding previously reported between adjacent growth intervals for the pleurocarpous Hylocomium splendens (Hedw. BSG; Økland, Steinnes, and Økland, 1997
). Similarly, in Polytrichum alpinum (Hedw.) G.L. Smith, shoots are not allocationally independent units: photosynthate is transported from one shoot, through a rhizome, and into a developing shoot at remarkably rapid rates (3.1 mm/h; Collins and Oechel, 1974
). Note, however, that in Polytrichum, transport of photosynthate is assisted by internal conducting tissues that are absent in Syntrichia. Whereas in flowering plants, a strong tendency exists for resources to flow into fruits from the nearest leaves, and "each inflorescence and its adjacent leaves behave more or less as an independent unit" (Stephenson, 1981
), our data suggest that ramets are not necessarily independent. However, the photosynthate contribution from subtending inflorescence leaves remains to be determined. The relatively high cost of sporophyte maturation to female individuals is mitigated phenologically in a pattern similar to sex expression in male individuals. Both embryos and antheridia are initiated in the first winter, go through the following summer in a dormant phase, and complete their maturation in the second winter (unpublished observations). This prolonged developmental period allows these expensive structures to mature slowly, thus lessening the presumed negative impacts on the vegetative growth and survival of the individual.
The production of an exserted sporophyte in Syntrichia must place a great deal of pressure on the transfer cells at the sporophyte–gametophyte junction, which have specialized wall ingrowths to facilitate a one-way flow of water and nutrients from gametophyte to sporophyte (Ligrone and Gambardella, 1988
; Yip and Rushing, 1999
). The presence of abundant small vacuoles in the placental region of embryonic sporophytes of Acaulon muticum (Hedw.) C.M. was presented as evidence for protection against water stress in this diminutive plant (Rushing and Anderson, 1996
). The greatest need for water transfer would begin during seta elongation and extend through capsule expansion. However, the nearly uniform occurrence of abortive sporophytes prior to seta elongation in S. caninervis indicates that a shortage of gametophytic nutrients may be detected early in sporophyte development. Preliminary observations on the interval during which ramets in a population of S. caninervis are hydrated suggest that this period is very restricted and that its duration may affect net productivity and sex expression. The general pattern of selective fruit abortion (excess flower production) in hermaphroditic species has been attributed to five hypotheses: (1) contributing to male function through pollen donation; (2) attracting more pollinators through larger floral displays; (3) allowing increased fruit set during occasional but unpredictable years of resource or pollinator abundance (mast years); (4) providing "reproductive assurance" that sufficient seeds will be formed in the face of potential losses to herbivores, weather, and mechanical accidents; and (5) providing a larger pool from which superior fruits can be selectively matured (the "wide choice" hypothesis; Burd, 1998
). For S. caninervis, the latter three hypotheses are viable and could be potentially tested with carefully designed experiments enhancing maternal resources.
Density-dependent sporophyte abortion patterns are consistent with other aspects of the life history of desert mosses, which indicate severe resource constraints operate on both the reproductive biology and vegetative growth of these species. Desert mosses exhibit extremely short annual growth intervals of <0.5 mm/yr (Stark and Castetter, 1995
; Stark, 1997
; Stark, Mishler, and McLetchie, 1998
). The annual production in S. caninervis of 0.2 mg constitutes only 4–13% of the annual biomass increase in four species of forest mosses in central Norway (Hanslin, 1999
), and the annual growth increment is an order of magnitude shorter than Racomitrium microcarpon (Hedw.) Brid. growing on xeric granite faces in northern Ontario (Vitt, 1989
). Similarly, the low levels of sex expression and positive correlation between ramet length and sex expression are predicted from limited resource budgets. In deciduous perennial herbaceous seed plants, the percentage of whole plant biomass devoted to sexual reproduction each season ranges from 1 to 51% (N = 44 species), with a mean (of means) of 10% (Bierzychudek, 1982
). This value (10%) is an order of magnitude greater than expressing males allocate to reproduction in S. caninervis. Assuming an average individual biomass of 2.5 mg (unpublished data), the mean male sexual allocation is only 1% (0.0171 mg/2.5 mg). However, females realizing their full cost of sexual reproduction (maturing a sporophyte) allocate a comparable amount of biomass to reproduction as do forest herbs, 9% (0.232 mg/2.5 mg), although unfertilized expressing females contribute far less to sexual reproduction (1% of annual biomass and only 0.1% of individual plant biomass, 0.0027 mg/2.5 mg). Given that the vast majority of female individuals are unfertilized and many individuals are not expressing sex at all, this line of evidence provides support for the hypothesis that S. caninervis is devoting a disproportionate amount of resources to growth, survival, and to clonal (asexual) growth through branching, when compared to seed plants. Many bryophytes rely heavily on asexual reproduction, especially in xeric habitats (Mishler, 1988
; Newton and Mishler, 1994
); future research should incorporate measures of asexual components of fitness.
The next step in exploring this "cost of realized sexual reproduction hypothesis" will be to investigate a series of trade-off predictions, including: females live longer; females are larger (biomass, total stem length); females grow faster (greater growth intervals); females express sex more frequently and at a lower threshold size; females produce more ramets (branching frequency); females are more desiccation tolerant; and females are better competitors.
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FOOTNOTES |
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5 Author for reprint requests (702-895-3119, FAX 702-895-3956, e-mail: LRS{at}nevada.edu
).
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LITERATURE CITED |
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