See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/7440086 Factors influencing reproductive success in the clonal moss, Hylocomium splendens ARTICLE in OECOLOGIA · APRIL 2006 Impact Factor: 3.09 · DOI: 10.1007/s00442-005-0290-2 · Source: PubMed CITATIONS 22 READS 22 3 AUTHORS: Knut Rydgren Sogn og Fjordane University College 59 PUBLICATIONS 1,134 CITATIONS SEE PROFILE Nils Cronberg Lund University 47 PUBLICATIONS 1,025 CITATIONS SEE PROFILE Rune Halvorsen University of Oslo 124 PUBLICATIONS 3,517 CITATIONS SEE PROFILE All in-text references underlined in blue are linked to publications on ResearchGate, letting you access and read them immediately. Available from: Knut Rydgren Retrieved on: 04 February 2016
Factors influencing reproductive success in the clonal moss,Hylocomium splendens
Received: 6 July 2005 / Accepted: 12 October 2005 / Published online: 3 December 2005� Springer-Verlag 2005
Abstract Female reproductive success in the unisexualperennial clonal moss Hylocomium splendens wasexamined by recording, if the segment was reproductive[produced sporophyte(s)] or not, together with severaldistance-to-male and male density variables, and seg-ment size. This was done for every female segment in apopulation over a 5 year study period. A high fractionof the population could be sexed because we monitoredthe population in situ for 5 years, and thereafter har-vested the population for electrophoretic analysis fromwhich the clonal identity and expressed sex could bededuced. Fertilization distances in H. splendens wereshort, indicated by the fact that as many as 85% of thefemale segments with sporophytes were situated within adistance of 5.0 cm from the nearest male. The longestdistance measured between a sporophytic female and theclosest male was 11.6 cm. However, analysed within ageneralized linear modelling (GLM) framework, theyear was the best single predictor for the presence of H.splendens sporophyte although female-segment size anddistance to the closest situated male were also stronglysignificant. The two latter factors explained larger frac-tions of variation in sporophyte presence in a GLMmodel with three predictors than in single-predictormodels. This is because (i) the large variation in sporo-phyte production among years partly obscures thestrong general increase in sporophyte production with
increasing female-segment size and vitality, and (ii) thebetween-year variation and the size obscure the effect ofthe distance to the most proximate male. To ourknowledge, this study is the first to incorporate into onemodel the relative importance of several factors forbryophyte reproductive success. Our results demonstratethe value of multiple-predictor approaches in studies ofreproductive success.
Bryophytes are representatives of three separate lineages(mosses, liverworts, and hornworts), related to the firstland plants, which emerged some 475 million years ago(Wellman et al. 2003). Despite long separate evolution-ary histories, they still share similarities with respect towater-dependent fertilization and life-cycle features.Their life cycle is dominated by a haploid gametophyte,whereas the short-lived diploid sporophyte is initiatedafter fertilization and remains connected to the femaleshoot. Bryophytes constitute an ecologically importantplant group, which is living in the shadow of the evo-lutionary much younger seed plants (Proctor and Tuba2002; Raven 2002), even with respect to quantities ofbiological studies (Rydgren and Økland 2002a). Bryo-phytes are cryptogams, implying that the ‘‘wedding’’, thefusion of gametes, is hidden from the human eye.Accordingly, our knowledge concerning the relativeimportance of different factors at different stages in thereproductive process (from the development of gam-etangia via fertilization to sporophyte formation andliberation) is fragmentary, relying mainly on the indirectevidence from studies of one or just a few factors at thesame time.
The reproductive success of many seed plants is lim-ited by the quantity or quality of male gametes (pollen),i.e., they are pollen-limited (Burd 1994; Ashman et al.
Communicated by Jacqui Shykoff
K. Rydgren (&)Faculty of Science, Sogn og Fjordane University College,133, 6851 Sogndal, NorwayE-mail: [email protected].: +47-5767-6216Fax: +47-5767-6201
N. CronbergPlant Ecology and Systematics, Lund University,Ecology Building, 223 62 Lund, Sweden
R. H. ØklandSection of Botany, Natural History Museum, University of Oslo,1172, 0562 Blindern, Oslo, Norway
2004). The distance between the sexes affects the repro-ductive success in dioecious or self-incompatible speciesin relation to the abundance and efficiency of theirpollen vectors (Widen and Widen 1990). Similarly, fer-tilization distances in bryophytes are restricted by theability of male gametes (spermatozoids) to swim in anambient water surface in order to reach a female gam-etangium. Studies of maximum distances between themales and the fertilized females suggest that the fertil-ization distance is less than 10 cm unless special devicesfor gamete dispersal such as splash-cups are present(Longton and Schuster 1983; Longton 1997; van derVelde et al. 2001). Spermatozoid-dispersal ranges of upto 34 cm have, however, been recently demonstrated(Bisang et al. 2004). In spite of the fact that limitedsperm-dispersal distance is crucial for bryophytes, morethan 60% of the species are dioecious, or unisexual(Wyatt and Anderson 1984; Shaw 2000), while only 5%of the seed plants are dioecious (Richards 1997). In seedplants, the maintenance of dioecy in the presence ofhermaphroditic competitors seems to require a sub-stantial increase in relative fitness and/or a large dis-persal advantage of dioecious seeds (Heilbuth et al.2001). Notwithstanding, the close proximity of femalesand males is certainly an important factor for bryophytereproductive success (Wyatt 1977; McLetchie 1996; Bi-sang et al. 2004), but many other factors may also beimportant, e.g., developmental failure or rarity of gam-etangia (Longton 1976), the size and vertical distributionof individuals in the bryophyte carpet (Rydgren et al.1998; Rydgren and Økland 2002c), and weather condi-tions during the fertilization period (e.g., Benson-Evans1964; Callaghan et al. 1978; Rydgren and Økland 2001),as well as resource limitation (Stark and Stephenson1983; Ehrlen et al. 2000; Stark et al. 2000; Stark 2001;Bisang and Ehrlen 2002; Rydgren and Økland 2002b,2003). Since these factors have not been examinedsimultaneously, their relative importance for bryophytereproductive success remains poorly understood.
In order to unravel the relative importance of factorsthat may influence the reproductive success of bryo-phytes, the sex of all ramets in the studied populationsshould ideally be known. This is, however, complicatedby a frequent lack of gametangial branches, notably ofsmall ramets, and difficulties with non-destructive in situdetermination of sex in general. The proportion of sex-determined ramets in the populations of unisexual spe-cies can be increased by a careful long-term monitoringin situ, by which the sex of all ramets on a branchedshoot chain will be known once one part of the chain hasexpressed its sex (Rydgren and Økland 2002c). It can befurther increased by harvesting the population after aperiod of field monitoring, directly by screening for thesex chromosomes (Newton 1971) and/or indirectly byusing molecular markers to infer the clonal identity ofshoots of which some may express the sex (Cronberg2002; Cronberg et al. 2003).
Hylocomium splendens (Hedw.) B. S. G. is one of themost widely distributed and common bryophytes in the
northern hemisphere (Persson and Viereck 1983). Theunisexual H. splendens shows large variation in sporo-phyte production between years and habitats, and withvariation in incoming radiation, position in the bryo-phyte carpet, shoot density, and female size (e.g.,Callaghan et al. 1978; Økland 1995; Rydgren et al. 1998;Rydgren and Økland 2001, 2002c; Cronberg 2002). Al-though H. splendens is one of the best studied bryo-phytes, we do not know the relative importance of thedifferent factors that may influence the variation insporophyte production. Therefore, the aim of our studyis to explore the relative importance of presumablyimportant factors for sporophyte production in H.splendens by simultaneous analysis within a generalizedlinear modelling (GLM) framework.
Materials and methods
The species
Hylocomium splendens is a large, perennial, clonal,pleurocarpous moss with modular growth due to annualperiodicity in the emergence of new modules that remainconnected as segment chains until they become sepa-rated by decomposition from below (after 2–20 years) orare damaged (Tamm 1953; Økland 1995). Growingpoints become mature segments in their second autumn.H. splendens is unisexual and gametangia develop inspring on growing points that develop into mature seg-ments the following autumn (Bakken 1994). Perichaetiaare positioned along the main stem and perigonia onfirst- or second-order branches. Both structures arehardly visible without magnification. Fertilization nor-mally occurs in July and is followed by seta elongationin autumn and the sporophytes reach maturity the nextspring or summer (Arnell 1875; Bakken 1994).
Study site and data collection
The present study utilizes a part of the population dataof Rydgren and Økland (2002b, c, 2003); see Rydgrenand Økland (2002c) for a more thorough description.Data were collected over a 5-year period (1995–1999) ona boulder (area: ca. 0.8 m2; average slope; 38�) almostcompletely covered by H. splendens, situated in a smallPicea abies-dominated forest valley north of Stampe-tjern, Skedsmo municipality, Akershus County, SENorway (11�09¢E, 59�59¢N), 170 m a.s.l. A rectangularsampling site of 0.4·0.9 m was placed on the top surfaceof the boulder and divided into 36 grid plots, 10·10 cmeach. For the entire 5-year study period. all H. splendensshoots were censused annually in the nine plots thatcontained two or more sporophyte-carrying segments atthe start of the study in 1995. A 4:1 female-biased sexratio has been reported for this population, but malesmay have been slightly underestimated as they were onlysought at one census while sporophyte-carrying females
were recorded at every census (Rydgren and Økland2002c).
In the present study, we use data from five of thesenine plots in which all H. splendens segments were har-vested for genetical analysis in May 2001 (see below).The frequency of female segments producing thesporophytes (ns/n$) in the five study years, during 1995–1999, was: 0.39, 0.24, 0.30, 0.49, and 0.14, respectively).At each annual census, we searched for all growingpoints present at the previous census and all newgrowing points were mapped and non-destructivelytagged, using plastic rings (c.f., Økland 1995). The seg-ments were inspected for the presence of sexual struc-tures, archegonia, and antheridia, in July 2000, whilesporophytes were recorded at every annual census(Rydgren and Økland 2002c). The size (dry mass, DM,expressed as base-2 logarithms whereby one unit corre-sponds to doubling of the size and sizes become nearlynormally distributed) of all mature segments was esti-mated from in situ morphological measurements (seg-ment length, number of branches, and length of thelongest branch) by a nonlinear regression model(R2=0.913, n=328; Økland 1995).
The five 10·10 cm plots formed two continuoussampling areas (Fig. 1). Each sampling area was dividedinto a core and a 2-cm broad border. For all femalesegments (with or without sporophytes) within the cores,we recorded and calculated distances to all males presentthe given year within a circle centred on the female, witha radius of 12 cm. Furthermore, all recorded males wereallocated to circle sectors: A90 (the 90� sector above thefemale; 45� on either side of the direction of the steepestascent through the female); A140 (the 140� sector abovethe female); A180 (all males situated above the female);B90, B140, and B180 (like the corresponding A sectorsbut below the female). For every sector (with 12 cmradius), we counted the number of males (NA90,NA140, etc.) and recorded the distance to the male
closest to the female (DA90, DA140, etc.), obtaining 12variables. Distance from the female to the closest situ-ated male (D) was recorded as the 13th variable. Forsectors not fully contained within the sample area, amissing value was recorded, although ‘‘white sectors’’were allowed for females in the lower right plot wherethe three plots were connected to distances to malesabove (Fig. 1), since this part of the sampling areacontained few males all years. A few ‘‘sterile’’ H. splen-dens segments that could not be sexed were left out fromthe analyses. Most likely these were females (Rydgrenand Økland 2002c).
The annual mean precipitation is 830 mm (stationSkedsmo-Hellerud ca. 10 km SW of the study area;Førland 1993), and the annual mean temperature is3.8�C (station Gardermoen ca. 25 km N of the area;Aune 1993). In the study period, July precipitation washigh in 1995 (106 mm) and very low in 1997 (31 mm),while 1996, 1998, and 1999 had 45, 67 and 63 mm ofprecipitation, respectively. The year 1998 differed fromall other years in having considerably higher number ofdays in July with precipitation above 0.1 mm (19 days);figures for the other years were 12 (1995), 8 (1996), 6(1997), and 10 (1999). All the years except 1996 werewarmer than normal, most notably because autumnswere warmer.
Electrophoretic procedures
In order to increase the proportion of sex-determinedsegments in our H. splendens population, we harvestedthe population in May 2001. All shoots were keptgrowing in a growth chamber until extraction. Someshoots were in poor shape at the time of sampling dueto a prolonged period of drought. Most of theseregenerated after a growth period of up to 6 months,allowing inclusion in the analyses. Electrophoretic
Fig. 1 The spatial distributionof H. splendens haplotypes inthe sample plots in 1998inferred from the geneticalanalysis. The shortest distancebetween the two sampling areaswas 32 cm
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procedures for the analysis of nine enzymes systemsfollowed Cronberg et al. (1997) and Cronberg (2002).Homogenate from a single clone of Pleurozium schre-beri was placed at five positions on every gel to providea control against which relative bands in the otherindividuals could be scored.
Data analysis
All statistical analyses were made using S-PLUS version6.0 for Windows (Anonymous 2001). A randomization(Monte Carlo) approach (Legendre and Legendre 1998)was used to test the hypothesis (H0) that the 99 recordedfemale segments with sporophytes (sporophytic females)did not differ from the 219 female segments withoutsporophytes (non-sporophytic females) with respect tomeans for segment size (dry mass) and the 13 variablesdescribing male distribution relative to the female. Foreach variable, we first calculated the observed mean M0
for the sporophytic subsample. Next, 9,999 randomsubsamples, each with 99 observations, were drawn fromthe entire sample (n=318) and the mean M1 calculatedfor each. The significance P of the test against one-tailedalternative hypotheses was obtained by counting thenumber s of subsamples for which M1>M0 (variablesNx; number of males) or M1<M0 (variables Dx; dis-tance to the closest male):
P ¼ 0:0001 � ð1þ sÞ
We used GLMs (Venables and Ripley 2002) to modelthe effects of a set of predictor variables (here: femaledry mass, year and D, distance to the closest situatedmale) on variation in a response variable (here: sporo-phyte presence/absence). GLM was chosen because itallows flexible handling of data over a wide range ofstatistical properties (Venables and Ripley 2002).
The D variable was lognormally distributed; trans-formation to (1+log D) before analysis reduced skew-ness and made the variances homogeneous. The yearwas recorded as a factor variable with five levels, de-noted as factor (year) 95 ... factor (year) 99. Because theresponse variable was binary (0–1), logistic regressionmodelling [GLM with logit link function and binomialdistribution of errors (Venables and Ripley 2002)] wasused.
In all nested GLM models (i.e., M is a submodel ofM0), the parameters bi were tested (null hypothesis:bi=0, against the two-tailed alternative) by the F-sta-tistic,
Fp�q;n�p ¼(DM0
� DM)
hðp � q);
where DM0and DM are the deviances of models M0 and
M with numbers of parameters q and p, respectively, n isthe number of observations, and h is the scale param-eter, which is one in models with binomially distributederrors.
Initially, separate models were constructed for eachpredictor. Next, the sporophyte presence was modelledas the response to all three predictors, using a forwardselection procedure by which (1) the best single predictor(see below) was included in the model and (2) theadditional effect of the other variables was evaluated,one in turn, by sequentially including them in themodels. Interaction terms were only allowed to enter amodel after both the main effects had been included.Models were validated by consideration of F and theassociated P values. The submodel M of the model M0
was considered superior to M0 if the extra predictor(s) inM was significant at the P<0.05 level in the F-test.
Regression coefficients for significant fixed terms arereported as treatment contrasts, to be interpreted asfollows: the intercept gives the predicted value for theresponse variable (probability that a female segmentcarries sporophytes) with logit link function, ln p
1�p ; forvalues of zero for the transformed continuous predictors(size and distance to the closest situated male) and forfactor (year) 1 (=1995). The coefficients for factor levelsshow the difference in the intercept from that ofyear=1995. Main-effect coefficients for continuousvariables are to be interpreted as the predicted slope forthe dependence of the response variable on the predictorfor year=1995 while the coefficients for interactions ofthis predictor with factor (year) give the predicteddeviations from the slope for factor (year) 1 (=1995).Because all the coefficients, bi (relative to the ithparameter) pertain to the GLM with logit link, thepredicted back-transformed values for the sporophyte-occurrence probability may be obtained from theequation:
Polymorphisms at seven allozyme loci identified fourhaplotypes within plots, one female and three males.Each of these haplotypes differed at several polymorphicloci, suggesting a high reliability of haplotype identifi-cations. Visual sex determinations in combination withidentification of haplotypes thus allowed us to determinethe sex of almost all shoots (Fig. 1).
Dependence of sporophyte production on proximityof males
Sporophyte-carrying female H. splendens segments weresituated significantly closer to a male than female seg-ments devoid of sporophytes (randomization tests ofvariable D; Table 1, Fig. 2). Distance to the closest sit-
uated male was much more strongly significantly dif-ferent among sporophytic and non-sporophytic femalesthan any other recorded variable (P=0.0001 as com-pared to P>0.003). However, significant differenceswere also found for sector distances, most strongly fordistance to the closest male situated above the female(DA180; P=0.0038), followed by DA140 (P=0.0182).Distance to the closest male in the narrowest sectorabove the female (DA90) was not significantly different,but distance to the closest situated male below the fe-male was significant but not strongly so (P=0.0365;Table 1). Distances to the closest situated male abovewere invariably more strongly significantly different be-tween sporophytic and non-sporophytic females thandistances to the males below, in sectors of equal widths.The number (density) of males below the female (threevariables) was non-significantly different between thetwo groups of H. splendens female segments, while maledensity above the female was indicatively significantlydifferent (0.05<P<0.10; Table 1).
GLM modelling of sporophyte production probability
The probability that a female segment produces sporo-phytes was strongly significantly affected by all threepredictor variables, as tested in single-variable GLMmodels (Table 2). Sporophyte frequency thus differedsignificantly among years. The effect of size was positivewhile the effect of distance to male was negative(meaning that sporophyte presence increased withdecreasing distance to male).
The most strongly significant single predictor, factor(year), was selected first in the multiple logistic model.Size was added next, with twice as much deviance
accounted for than in the single model, indicating thatthe effect of female size on sporophyte presence becamestronger after the confounding effect of good and badyears for sporophyte production was accounted for. Thesame applied to the effect of distance to the closest sit-uated male. The interaction between factor (year) anddistance to the male was also included in the final model,indicating that the effect of distance to the male variedsignificantly among years (Table 2). The coefficients forterms in the final model (Table 3) and model predictionsas visualized in Fig. 3 show that the year 1998 wasexceptional, both in the high sporophyte-occurrenceprobability and in the strong dependence of sporophyteproduction on distance to the nearest male. Years 1995and 1997 were average years and 1999 was the poorestyear for sporophyte production. In none of these years,was the sporophyte production dependent on the dis-tance to the male. However, in 1996, the rather pooryear for sporophyte production, sporophytes were much(but only indicatively significantly; see Table 1) morestrongly favoured by the female being situated close to amale segment (Fig. 3).
Discussion
The distances from a female segment to the neighbour-ing males influenced reproductive success in H. splen-dens. This accords with results obtained for otherdioecious bryophytes, without (McLetchie 1996; Bisanget al. 2004) and with splash cups (van der Velde et al.2001), and the results from the out-crossing seed plantsin which seed set may decrease with increasing popula-tion fragmentation (Lennartsson 2002). Our resultsshowed that fertilization distances in H. splendens are
Table 1 Summary statistics for the 99 recorded female segments with sporophytes (Sp), the 219 non-sporophytic female segments (NSp)and male proximity variables
Variable (unit) Sp mean (n=99) NSp mean (n=219) Grand mean (n=318) Randomized sample P
P is the significance of randomization tests, testing the hypothesis that the 99 recorded Sp female segments do not differ from the 219 NSpfemale segments with respect to means for segment size (dry mass) and the 13 variables describing male distribution relative to a givenfemale in a 12 cm radius centred on the female: D is the distance from a female to the closest situated male, DA, DB, NA, and NBrepresent the distance to (D) respectively number of (N) all males within a sector of the given number of degrees (90, 140, or 180) of thecircle of radius 12 cm either above (A) or below (B) each female
449
Fig. 2 Distribution of femaleH. splendens segments with(n=99) and withoutsporophytes (n=218),respectively, on distancegroups, reflecting theirminimum distance to the closestmale within the sample plotsover all the years (1995–1999)and for each year
Table 2 The influence of single predictor variables [factor (year), log (1+D) where D is the distance from a female segment to the closestsituated male and female size (dry mass)] on sporophyte presence and the best multiple-predictor model
Modelling by logistic regression within a generalized linear framework (logit link function and binomial error distribution). Predictor +1refers to the null model. df model degrees of freedom. F and P refer to a marginal F-test of the model
450
generally short; 85% of the female segments withsporophytes are situated within a distance of 5.0 cmfrom the nearest male and the longest distance is 11.6 cm(cf., Fig. 2). However, longer fertilization distancesprobably occurred since the measurements of distancesfrom sporophytic females to the nearest male providedminimum gamete-dispersal distances, and such mea-surements are likely to underestimate the real fertiliza-tion distances though more strongly in species withsplash cups (Reynolds 1980; van der Velde et al. 2001).
Distance to the nearest male was more importantthan the direction from the female to the male, asdemonstrated by the increasing strength of the rela-tionship between sporophyte-occurrence probability anddistance to the nearest male above a female segment withincreasing sector width, and by distance to the nearestmale being the best predictor of sporophyte-occurrenceprobability. Downslope dispersal of spermatozoids wasmore likely than upslope dispersal but upslope dispersalalso occurred, as observed for Abietinella abietina andRhytidiadelphus triquetrus (Bisang et al. 2004). Upslopedispersal of spermatozoids may be due to the ability ofspermatozoids to swim by means of their flagella,
although their movement is usually considered erraticand aimless (Paolillo 1981; Longton 1997). Observationssuggest that chemotactic stimuli are present in somemosses (Longton and Schuster 1983). Sugar excreted byreceptive archegonia is effective in this respect, at least inFunaria (Watson 1971). If such attractants occur in H.splendens, they could partially explain the relative effi-ciency of the upslope movement of spermatozoids, sinceattractants are likely to move downwards from the ar-chegonia. Upslope movement may also be due to otherprocesses such as raindrop splashes, the movement ofsmall animals, etc. (Longton 1990). In general, sperma-tozoid dispersal distances upslope and downslope weredependent on terrain inclination (ca. 38� at the studysite) probably due to gravity (Bisang et al. 2004). Thisexplains why the distances from sporophytic and non-sporophytic H. splendens females to the closest situatedmale were more strongly significantly different for malessituated above than for males below. We found someindications that the male density influenced the femalereproductive success; the three measures of male densityabove the female were indicatively significant(0.05<P<0.1). This weak relationship might be due todensity being a coarse measure of the overall sperma-tozoid availability, as the quantity and quality of sper-matozoids, the things that really matter, were notmeasured. Second, we recorded male density within 12-cm sectors, which may be unrealistic when 85% of thesporophytic females occur within a distance of 5 cmfrom the closest male.
The GLM model of H. splendens sporophyte proba-bility showed that the year was the best single predictor,followed by female size, and distance to the nearestmale. All the three predictor variables were, however,strongly significant (P<0.002) in single-predictor andmultiple-predictor models. In fact, both female size anddistance to closest situated male explained a largerfraction of variation in sporophyte occurrence proba-bility in the multiple-predictor than in the single-pre-dictor models. This is due to the considerable differencein sporophyte presence among years (Rydgren and Øk-land 2002c), which partly masks the strong general in-crease in sporophyte production with female segmentsize and vitality (Rydgren and Økland 2002c, 2003). Inour data, this was exemplified by the year 1999, in which
Table 3 Fixed effects of thefinal model: coefficients for allincluded predictor variableswith estimated standard errorsand a marginal t-test of theindividual coefficients
Coefficients significantlydifferent from zero at thea=0.01 significance level aregiven in bold. df=305
Predictor variables Coefficient Standard error t value P value
Fig. 3 Probability (P) that a female H. splendens segment of size6.00 (=6.4 mg) produces sporophytes in a given year, modelled asa function of distance to the closest situated male (in cm)
sporophyte production was low although segments wereparticularly large. Similarly, the effect of distance to thenearest male became clearer once the effects of the yearand female size were accounted for. A particularlyinteresting result of the GLM modelling was the differ-ence between years with respect to the strength of thedependence of female sporophyte production on thedistance to the closest situated male (see Fig. 3). It is welldocumented that sporophyte production may vary a lotbetween years, in bryophytes in general (Callaghan et al.1978; Rydgren and Økland 2001; Stark 2002; Wiklund2002) and in our H. splendens population in particular(Rydgren and Økland 2002c). This variation is probablymainly due to variation in weather conditions whichinfluences the formation and development of sexualstructures, the probability of fertilization, sporophytedevelopment, and spore maturation (Hancock andBrassard 1974; Longton 1990; Sundberg 2002). Simi-larly, weather is important for reproductive success inseed plants (e.g., Bengtsson 1993; Westley 1993; Stens-trom 1999). The year with exceptionally high sporophyteproduction, 1998, was an average year regarding Julyprecipitation, the period of fertilization in H. splendens(Arnell 1875). However, 1998 differed from all otheryears in having considerably higher number of days withprecipitation above 0.1 mm in July. This, indicates thatfrequent, episodic precipitation is more favourable forfertilization success in bryophytes than infrequent, hea-vy rain (Andersson 2002). The year 1998 was also theonly year in which sporophyte production was signifi-cantly dependent on distance to the nearest male (in1996, this relationship was indicatively significant),indicating that the proximity to a male was more deci-sive for fertilization success when conditions were gen-erally favourable. One likely explanation for this is thatthe sex expression of males varies from year to year,perhaps due to climatic conditions, so that in years whenfew male ramets are fertile, the distance between asporophytic female and the closest male is a poor indi-cator of fertilization distance.
The GLM model showed that female size wasimportant for sporophyte production. Although femalesize has rarely been considered an important factor forsporophyte production in bryophytes, sporophyte-pro-duction frequency increases almost linearly withincreasing log2-transformed size in H. splendens femalesuntil levelling off for large segments (6–7 log2 DM) andthen decreasing (Rydgren and Økland 2002c). Obvi-ously, a female H. splendens segment needs a certain sizebefore it is capable of producing sporophytes (Rydgrenet al. 1998; Rydgren and Økland 2002c), because theproduction of sporophytes incurs a substantial cost,both in the short and long terms (Rydgren and Økland2002b, 2003). Thus, the lack of a relationship betweensporophyte production and the distance to the nearestmale in some years could be due to many females havingexhausted their energy reserves. A likely case was 1999,which was the year with the lowest frequency of sporo-phytes in contrast to 1998, which was the year with the
highest frequency of sporophytes. Existence of athreshold size for reproductive success, a trait found inmany seed plants (Lacey 1986; Wesselingh et al. 1997), islikely to be more common among bryophytes thandocumented so far and should be taken into accountwhen the relative importance of different factors for thereproductive success of bryophytes is examined.
Reproductive success in a dense H. splendens popu-lation, with an approximately female-to-male ratio of4:1 (Rydgren and Økland 2002c) and occurring on asteep slope with realistic swimming distances for sper-matozoids to the nearest female was explained, in theorder of decreasing importance, by inter-year variation,by female segment size, and distance to the closest sit-uated male. Clearly, all variables that influence femalesporophyte production were unlikely to have beenidentified and taken into account. Potentially importantfactors, not included in this study are the vertical posi-tion of segments in the bryophyte carpet (Økland 2000;Rydgren and Økland 2002c), male size (cf., McLetchie1996), and properties of the gametangia themselves.Nevertheless, to our knowledge this study is the first toincorporate into one model the relative importance ofseveral factors for reproductive success in bryophytes.
Bryophyte reproductive ecology shows fast progress,and a variety of important questions have recently beenaddressed (e.g., Bowker et al. 2000; Ehrlen et al. 2000;Stark et al. 2000; Bisang and Ehrlen 2002; McLetchieet al. 2002; Bisang et al. 2004; Pohjamo and Laaka-Lindberg 2004). Use of new techniques, both demo-graphic (Økland 1995; Rydgren and Økland 2002a) andgenetic (van der Velde et al. 2001; Cronberg 2002, 2004),opens new insights into the life histories of these‘‘cryptogamic’’ plant groups with long lineages back tothe first land plants.
Acknowledgements Christian Korner, Jacqui Shykoff and twoanonymous referees gave valuable comments on an earlier draft ofthe manuscript.
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