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Sex expression and reproduction of four bryophytes following timber harvesting.

Introduction

It is essential that bryophytes have the ability to reproduce sexually for harvested forests to return to pre-harvest levels of bryophyte composition and richness with a high degree of genetic diversity amongst populations. Many bryophytes reproduce only by asexual means (Longton 1976), implying they may be unable to cope with changing environments (Stark et al. 1998); however, as long as periods of sexuality occur, there is no reason why bryophytes could not benefit from both long- and short-term advantages provided by both forms of reproduction (Longton 1976). Asexual reproduction is considered important for colony expansion and maintenance (Longton 1976, 2006), while sexual reproduction is considered important for genetic diversity, providing for the potential of survival in changed conditions and development of new populations in a new ecology (Longton 2006).

Many factors affect reproduction in bryophytes. For example, stress caused by changes in the physicochemical nature of the environment is known to promote a female-biased sex ratio (Stark 2002). Bryophytes depend on the appropriate signals for sex expression, and developmental pattern of gametangia and sporophytes. If the appropriate signals are lacking, the phenological events may not occur. Inhibition of archegonial maturation, when sperm are ready for release, would prevent fertilisation events (Longton 1972). If conditions have changed, growth can be affected. This, in turn, can affect reproduction. Benassi et al. (2011) concluded that limited water availability could stunt plants and thus inhibit sex expression, promote growth of female-only individuals and, therefore, limit sexual reproduction. Their data suggested that males of Syntrichia caninervis required more consistent water availability as they had a lower tolerance for repeated cycles of wetting and drying. Younger forests would have very different wetting and drying cycles from those in older forests, which, therefore, could affect reproduction. Needless to say, other factors that could be important to reproduction also vary between younger and older forests. Photoperiod would be shorter in a more closed forest than open forest because of shading effects. Similarly, temperatures are more extreme in open than closed forests. Nutrient levels also vary with forest age and may affect reproduction. The high nutrient demand necessary for reproduction means that limited nutrient levels can inhibit reproduction. In Syntrichia caninervis, Bowker et al. (2000) found greater sex expression was associated with shady microhabitats, higher soil moisture, greater nutrient availability and taller ramets. Male ramets were restricted to shaded microhabitats whilst female ramets were found in both shaded and exposed microhabitats. Forests at various stages of regeneration post-logging vary markedly in moisture levels, light and temperature regimes and nutrient availability, thus cues for sexual reproduction may vary with time or, in fact, be absent. It is important, thus, to understand logging effects on bryophyte reproduction.

Such studies are extremely few and, currently, effects of logging on bryophyte reproduction can be inferred only from studies where another disturbance has been investigated; however, Cronberg et al. (2003) investigated the sex ratio in the moss Plagiomnium affine in forests of contrasting age after timber harvest, screening for genetic variation at 23 allozyme loci. They found female bias occurred at the ramet level but balanced sex ratios occurred at the genet level. Forest age was positively correlated with sporophyte numbers and negatively correlated to the percentage of non-expressed shoots.

The number of studies on sex ratios outside the logging scenario is considerable. Such studies involve investigation into the number of stems bearing perichaetia or perigonia and whether sexual reproduction is taking place, usually evidenced by the presence and number of sporophytes. The number of non-expressed stems also is taken into account. Given that 60% of bryophytes worldwide are dioicous (Wyatt and Anderson 1984), most studies on sex ratios have been undertaken on dioicous species, whilst monoicous species have been neglected. Dioicous species are known for having a female biased sex ratio and high levels of non-expressed stems, with many studies on individual species showing this (Shaw and Gaughan 1993; Stark et al. 1998; Benassi et al. 2011; Cronberg et al. 2003; Stark et al. 2010; Rydgren et al. 2010). Bisang and Hedenas (2005) reviewed the sex ratios of 89 dioicous moss and liverwort species using literature reports and their own investigations, as well as herbarium specimens, of which ten were from Australia. They found 88% of herbarium specimens or 'patch in the field' and 68% of 'shoots in the field' showed a female skewed ratio. This 'trait' of dioicous species is strange, given that sex chromosome formation through meiosis 'should' result in the formation of male and female spores in equal numbers (Shaw and Gaughan 1993; Bisang and Hedenas 2005). A number of possible explanations have been put forward to explain this phenomenon. Stark (2002) suggested that female skewed sex ratios may be a product of a higher realised cost of sexual reproduction in males; however, Bisang et al. (2006) found Pseudo-calliergon trifarium showed no detectable costs to explain male rarity when they investigated the cost of allocation to sexual branches.

Monoicous bryophytes develop both male and female gametangia on the one stem and have been found to be self-fertilising in the mosses Phascum cuspidatum, Pottia truncata and Weissia controversa (Roads and Longton 2003). Cross fertilisation takes place in other monoicous species such as Atrichum undulatum, Tortula muralis (Longton and Miles 1982) and Entodon cladorrhizans (Stark 1983). The ability to self-fertilise produces a higher number of sporophytes in monoicous as opposed to dioicous species.

This study investigated the sex expression of four bryophyte species inhabiting forests regenerating after clearfell-burn-sow logging over a chronosequence in Wet Sclerophyll Forest (WSF) in the state of Victoria, Australia. The specific aims were to determine: (1) if sexual reproduction occurred; (2) the timing of phenophases and whether these were affected by years-since-harvest; (3) whether a bias in sex expression occurred; and (4) if sex expression altered with years-since-harvest.

Methods

Study Area

Toolangi State Forest is located in the Central Highlands of Victoria approximately 80 km north-east of Melbourne (Fig. 1). The climate is described as temperate with a mean annual temperature of 15.8[degrees]C and monthly means ranging from 8.6[degrees]C to 23.2[degrees]C. The mean annual rainfall is 1370 mm. Mean monthly rainfall varies from 77 mm to 138.5 mm (Bureau of Meteorology 2008).

The area has wet sclerophyll forest dominated by Eucalyptus regnans, which is able to reach heights of 100 m (Attiwill and May 2001; Costermans 1996) although records prior to 1935 included specimens higher than 100 m (Ashton 1975; 2000; Beadle 1981; Hardy 1968; DNRE 1996). Eucalyptus regnans is the tallest (Beadle 1981) and fastest growing eucalypt (Ashton and Attiwill 1994), thus such ecosystems are used widely for forest harvesting. Selective logging was undertaken in Toolangi State Forest prior to severe bushfires in 1926 and 1939, and salvage operations were conducted following these fires (Ough and Ross 1992; DNRE 1996). Since the 1960s, clearfell logging has been the major silvicultural technique used in the area.

Sampling

Forests of five age classes along a chrono-sequence were selected for investigation, all previously having undergone clearfell logging. Applicable sites were derived from logging history maps supplied by the then Department of Natural Resources and Environment. Sites consisted of areas logged 10, 15, 20, 25 and 30 years prior to the study. All had been burnt previously in the 1939 wildfire. These ages were chosen because the target species occurred frequently, allowing for the sampling regime. When these species were present within younger sites, they occurred less frequently, more sporadically, and in much smaller populations. Also investigated was a 63-year-old forest regenerating from the 1939 wildfire that had not been logged or burnt since.

A 900 [m.sup.2] quadrat was examined within each of five sites from each age class. Sites were determined using a computer-generated random number table. Quadrat size and number was determined by the use of a 'species area curve' (Andrew and Mapstone 1987) undertaken in the 63-year-old forest, which was visually most species-rich.

To limit any possible edge effects, quadrat placement was at least 50 m from any road edge or forest of a different age or type. Sampling occurred from October 2002 to November 2003.

Four bryophyte species common to wet sclerophyll forests were chosen for investigation: Wijkia extenuata (Fig. 2a), Rhaphidorrhynchium amoenum (Fig. 2b), Rosulabryum billarderii (Fig. 2c) and Rhynchostegium tenuifolium (Fig. 2d). Rhaphidorrhynchium amoenum is a monoicous species widespread throughout Australia and New Zealand (Scott and Stone 1976). It is found in all but the driest of habitats (Meagher and Fuhrer 2003) on trunks of trees, rocks, soil and logs. It grows in densely woven mats and is pinnately branched. Rhynchostegium tenuifolium is a soft, slender, pleurocarpous moss quite variable in its appearance, either matted into flattened tufts or loose and straggly. It is an autoicous species, which means the perichaetia and perigonia occur on the same plant, but never on the same stem or branch. It is found widely throughout southern Australia (Meagher and Fuhrer 2003), and commonly inhabits soil, logs and bark in wet habitats. Rosulabryum billarderii is an acrocarpous, dioicous species widely spread throughout all of Australia. It occurs also in Asia, South and Central America, Africa, New Zealand, Oceania and Europe (Scott and Stone 1976). It is found in many habitats but is known to occur mostly in wet environments. Wijkia extenuata is also a dioicous species common to wet habitats throughout Victoria, Tasmania, ACT and NSW (Scott and Stone 1976). It also occurs in New Zealand. It is a pleurocarpous, prostrate, matted moss, commonly found on logs, soil, trunks, rocks and ferns.

Within each forest of differing age, 50 stems of each species were collected seasonally over a 12 month period. Each stem was examined for the presence of perichaetia, perigonia and sporophytes, the number of each was recorded and sex expression of stems determined. They were further examined for the number of antheridia and archegonia. These, along with the sporophytes, were assigned a maturation stage (Longton and Green 1969) (Table 1).

Data Analysis

Analysis of similarity (ANOSIM) was conducted to determine if a difference in the number of perichaetia, perigonia, sporophytes and gametangia existed for each species across the chronosequence. ANOSIM provides a test statistic, R, between -1 and 1. If R=0, there is no difference in the reproductive traits along the chronosequence. If R=1 or -1, perfect separation exists.

Results

Sex expression

Sex expression of stems within each forest age-class was higher than non-expression for the three pleurocarpous species (Table 2). The two dioicous species, Rosulabryum billarderii (acrocarpous) and W extenuata, produced more female than male stems (Table 2b, d). The female bias was very strong in Rosulabryum billarderii, as few male stems occurred; however, the total number of sexually non-expressing stems was high for this species. At times the number of perigonia or antheridia occurring within an age class reduced the female bias, especially in W. extenuata. In W. extenuata, there was a trend for variation in sex expression of stems to be greater in forests at either end of the temporal chronosequence. In no instance did statistically significant variation of reproductive attributes occur across the temporal chronosequence for either species (Rosulabryum billarderii: Fertile and non-fertile stems: Global R=0.03; p=0.63. Perichaetia and perigonia: Global R=0.08; p=0.81. Archegonia and antheridia: Global R=0.53; p=0.06. W. extenuata: Fertile and nonfertile stems: Global R=0.06; p=0.70. Perichaetia and perigonia: Global R=0.01; p=0.56. Archegonia and antheridia: Global R=0.13; p=0.94).

Rhapidorrhynchium amoenum is recognised as a monoicous species (Scott and Stone 1976) and although the majority of stems expressed monoicy, a number of stems were found to bear solely female or solely male organs (Table 2a). The female bias was clearly shown in terms of higher numbers of perichaetia although greater numbers of antheridia than archegonia occurred within four age classes. Forest age did not show an affect on any of these reproductive attributes (Fertile and non-fertile stems: Global R=0.17; p=0.03. Perichaetia and perigonia: Global R=0.11; p=0.92. Archegonia and antheridia: Global R=0.43; p=0.99). Pairwise tests showed a significant difference occurred between forests of 15 and 25 years-since-harvest (R=0.698; p=0.03) but this one-off occurrence was not considered indicative of an effect of forest age and is attributed to chance.

Rhynchostegium tenuifolium did not bear any female only or male only stems; all stems bore both sexes as expected for a monoicous species (Table 2c). Perigonia outnumbered perichaetia in forests of 15-30 years-since-harvest, as did antheridia compared to archegonia, thus a male bias occurred. Antheridia also outnumbered archegonia in forests of 10 years-since-harvest. Again, forest age did not show any effect on reproductive attributes (Fertile and non-fertile stems: Global R=0.10; p=0.86. Perichaetia and perigonia: Global R=0.13; p=0.04. Archegonia and antheridia: Global R=0.15; p=0.90).

Only Rhaphidorrhynchium amoenum showed a comparatively respectable number of sporophytes (795) from a total of 1200 stems (Table 2a). The other three species had 151 or fewer sporophytes out of 1000 stems (Table 2b-d). ANOSIM showed no significant differences across the temporal chronosequence for any of the four moss species (Rhaphidorrhynchium amoenum: Global R=0.13; p=0.95. Rhyncostegium tenuifolium: Global R=0.23; p=0.93. W. extenuata: Global R=0.18; p=0.99 Rosulabryum billarderii: Global R=0.25; p=0.19).

Phenology

Generally, the sequence and timing of sporophyte development for each species was similar for each forest age class so data was pooled for each species and peaks of each phenostage were used to better show the phenological development (Fig. 3). Rhaphidorrhynchium amoenum began sporophyte development in spring with the production of swollen venters, while W. extenuata began in summer. Both showed a similar sequence of development, and completed their cycles within 12 to 14 months with empty and fresh sporangia peaking in summer (Fig. 3). The data for Rhynchostegium tenuifolium have gaps but are suggestive of a similar developmental sequence to those of Rhaphidorrhynchium amoenum and W. extenuata (Fig. 3). Data for Rosulabryum billarderii were insufficient to make any meaningful deductions as to the developmental sequence of sporophytes.

Age of forest did not seem to have affected the timing and sequence of development for archegonia and antheridia so, as was done for sporophytes, data were pooled for each species to better demonstrate any pattern in phenological development. All stages of development in Rhaphidorrhynchium amoenum occurred in spring although dehisced archegonia were also noted in summer and winter. The observation of mature archegonia receptive for fertilisation during spring supports the findings that the number of sporophytes at the swollen venter stage occurred during this season (Fig. 3). Juvenile and immature antheridia peaked in winter while mature and dehisced antheridia peaked in spring, suggesting antherozooids were available for fertilisation. The maturation of the archegonia and antheridia and the occurrence of swollen venters during spring provide strong evidence that fertilisation occurs during this season.

The number of juvenile archegonia of W extenuata peaked in autumn, which was followed by a peak in number of immature archegonia in winter, then a peak in number of mature archegonia in winter and spring and, lastly, a peak in number of dehisced archegonia in summer. The data for antheridia did not allow interpretation of a phenological sequence.

The juvenile, immature and mature phenostages of both archegonia and antheridia of Rhynchostegium tenuifolium peaked in summer but dehisced stages peaked in autumn. The accompanying peak in swollen venters in summer (Fig. 3) strongly suggests fertilisation occurred during this season.

With respect to Rosulabryum billarderii, all phenostages of archegonia peaked in spring although juvenile and mature stages occurred in good numbers in winter, but only in forests of 15 years-since-harvest. Antheridia were noted only in spring but all were at the immature stage.

Discussion

Each of the four species produced sporophytes at the swollen venter stage when gametangia were mature and gametes were available for fertilisation events. Thus the evidence is very strong that sexual reproduction occurs in each of the four species examined and does so regularly, although the data for both W extenuata and Rosulabryum billarderii were insufficient to determine the phenological development of antheridia.

Although the data sets were incomplete, as not all stages were found in all forest age groups, forest age did not appear to inhibit sexual reproduction or its timing. As logging was shown to reduce species richness significantly (Sinclair 2012), these findings are reassuring in that they suggest logging does not affect the sexual abilities and capacities of those species able to recolonise, and they should be able to survive in the regenerating forests. These four species, however, are common, and the story for less common species may be very different and require further investigation. Other studies, such as those of Cronberg et al. (2003), found logging did affect sexual reproduction. They examined the effects of forest age post-logging in Plagiomnium affine and found that female bias occurred at the ramet level although balanced sex ratios occurred at the genet level. They also found forest age positively correlated with sporophyte numbers and negatively correlated to the percentage of non-expressed shoots. Obviously, the results for one species cannot necessarily be used to predict what happens to another species, although in management this frequently occurs.

It was not surprising that logging did not affect sexual reproduction, as many mosses show strong seasonality in terms of reproductive development and fertilisation events. This suggests temperature, moisture levels and daylength beyond the range of variation caused by logging would be triggers for the onset of phenological events. This, in turn, suggests the seasonal cycle is genetically controlled (Mishler and Oliver 1991; Sinclair 1999). Seasonality of the phenological cycle has been demonstrated for Atrichum androgynum (Biggs and Gibson 2006), Atrichum undulatum, Bryum argenteum (Miles et al. 1989), Atrichum angustatum (Zehr 1979), Mnium hornum (Greene 1967), Pleu rozium schreberi (Longton and Greene 1969), Dicranoloma billarderii, D. platycaulon and D. menziesii (Milne 2001). In other species, the sporophytic cycle is seasonal although the gametangial cycle is not, e.g. Grimmia pulvinata and Tortula muralis (Miles et al. 1989). Other species, e.g. Funaria hygrometrica, show no seasonality in development of their phenostages but can produce gametangia and sporophytes throughout the year (Longton 1976).

Development of sporophytes in Rhaphidorrhynchium amoenum, W. extenuata and Rhynchostegium tenuifolium extended over a 12 to 14 month period. This was not unusual. Some species complete development in a few months while others take years. Dicranoloma platycaulon and D. billarderii take 18 to 24 months (Milne 2001), Atrichum rhystophyllum, Pogonatum inflexum (Imura 1994) and Entodon cladorrhizans (Stark 1985) take nine months, and F. hygrometrica can take as little as two months (pers. obs. M Gibson).

Archegonia often undergo rapid development while antheridial development often requires more time (Imura 1994; Miles et al. 1989; Milne 2001). In these situations, maturation of both the male and female gametangia often occur at the same time and facilitates more successful fertilisation, particularly in dioicous spe cies (Longton and Greene 1967, 1969; Imura and Iwatsuki 1989). This study examined two dioicous, Rosulabryum billarderii and W. extenuata, and two monoicous species, Rhaphidorrhynchium amoenum and Rhynchostegium tenuifolium. The length of time required for development of the gametangia of the four species examined in this study requires clarification.

Sixty per cent of bryophytes are considered dioicous (Wyatt and Anderson 1984). Thus it is understandable that most published studies concerning sex ratios were on dioicous species. Dioicous species are known for their female biased sex ratios and high levels of non-expressed stems; however, while Rosulabryum billarderii continued the trend with a higher level of non-expressed stems than fertile stems, W. extenuata had a greater number of stems showing sex expression. If stress had an effect on the number of female and male stems produced, it would be expected to be seen in species of the younger, more open forest, where the moss is more exposed and subjected to less humidity and shade than in the older forests of 30 and 63 years -since-harvest. This, however, was not the case; neither species showed a significant difference in sex ratio with forest age in terms of either stem number or the number of inflorescences.

The monoicous mosses, Rhaphidorrhynchium amoenum and Rhynchostegium tenuifolium, were expected to have high numbers of sporophytes due to the ability of many monoicous species to self-fertilise. This was found to occur in Japan where investigation into 81 mosses, 61 dioicous and 20 monoicous, found the monoicous mosses had much higher rates of fertilisation than the dioicous species (Une et al. 1983 as cited in Stark 2002). In this study, whilst Rhaphidorrhynchium amoenum followed suit with sporophytes on 98% of fertile stems, Rhynchostegium tenuifolium had sporophytes on only 21% of fertile stems. Kimmerer (1991) found that in the monoicous species Tetraphis pellucida sex expression increased as shoot density increased. This phenomenon was not examined in this study. Kimmerer also found that as shoot density increased, the number of males increased and grew to outnumber the females. Both species showed a tendency towards a male bias although this was not statistically significant. Rhynchostegium tenuifolium dem onstrated a male bias in terms of both perigonia and antheridia. Rhaphidorrhynchium amoenum had a greater number of antheridia than archegonia, which offset the greater number of perichaetia than perigonia.

Rhynchostegium tenuifolium has both male and female inflorescences on the same stem but on separate branches. This may contribute to the lower sporophyte production in Rhynchostegium tenuifolium compared to Rhaphidorrhynchium amoenum, which has both male and female inflorescences on the same stem or branch. Distance for sperm to travel would, therefore, be smaller in Rhaphidorrhynchium amoenum, thus fertilisation is likely to occur more often.

Concluding remarks

No statistically significant differences occurred in the number of unisexual or bisexual stems, or the number of inflorescences, gametangia or sporophytes across the chronosequence for any of the four species. Nor was there any obvious difference in timing of the reproductive phenostages for either sporophytes or gametophytes. This suggests that time post-harvest did not have a deleterious effect on the sex expression of mosses investigated. Other studies, however, have found effects of harvesting on bryophyte phenology and reproduction, or environmental effects that could be due to the changed conditions of forests regenerating subsequent to harvest. It is not possible, therefore, to use one species as a surrogate to predict what might occur in other species, as is often done in management. More studies on reproduction for Australian bryophyte species are recommended to provide for more informed management of bryophytes both within forests that are harvested and within our protected forests. Data used in this study were seasonal, and monthly sampling is recommended as it might better indicate any post-harvesting effects; however, this is very time-consuming.

Glossary

(after Meagher and Fuhrer 2003) acrocarpous Having sporophytes terminal on stems or branches. Old sporophytes can seem to be lateral as the branches resume growth in the subsequent growing season. The majority of acrocarpous mosses are erect. antheridium (pl. antheridia) The male sex organ containing motile male gametes. antherozooid Motile male gamete produced in the antheridium.

archegonium (pl. archegonia) The female sex organ containing the female gamete (ovum). calyptra In mosses, a thin membrane protecting the developing sporophyte and forming a hood over the sporangium (structure containing spores). It is shed at maturity. dioicous Having the antheridia and archegonia on different plants.

inflorescence Cluster of sex organs and the specialised leaves that surround them.

monoicous Having male and female sex organs on the same plant.

operculum The cap or lid covering the mouth of the capsule, which detaches at maturity to allow dispersal of the spores. perichaetium (pl. perichaetia) Female inflorescence, comprised of specialised leaves surrounding the archegonia. perigonium (pl. perigonia) Male inflorescence, comprised of specialised leaves surrounding the antheridia.

pleurocarpous Having the sporophytes arising from specialised side branches, so that the habit or form of the plant tends to be creeping or pendent.

phenostage Developmental stage that can be defined by a start and end point. venter Swollen part of the archegonium, containing the egg.

Acknowledgements

The authors would like to thank Tim Wardle and Linda Moon for their kind assistance in the field. The study was conducted under the terms of research permit 10002309 issued by the Department of Sustainability and Environment.

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Zehr DR (1979) Phenology of selected bryophytes in southern Illinois. The Bryologist 82, 29-36.

Received 30 July 2015; accepted 29 October 2015

Bernadette Sinclair (1) and Maria Gibson (1,2)

(1) School of Life and Environmental Sciences, Centre for Integrative Ecology, Deakin University,

(2) 21 Burwood Highway, Burwood, Victoria 3125. 2Contact author

Table 1. Maturation stages of mosses
(derived from Longton and Greene 1969)

Stage                           Description

Sporophytes

Swollen venter (SV)             Venter of archegonium begins to
                                  swell
Early calyptra in               Calyptra assumes pale yellow
  perichaetium (ECP)              colour
Late calyptra in                Calyptra becomes half exserted
  perichaetium (LCP)              from perichaetial bracts
Early calyptra intact (ECI)     Calyptra becomes fully exserted
                                  from perichaetial bracts
Late calyptra intact (LCI)      Swelling of capsule begins
Early operculum intact (EOI)    Operculum becomes brown in colour
Late operculum intact (LOI)     Capsule becomes brown in colour
Operculum fallen (OF)           Operculum falls
Empty and fresh (EF)            75% of spores are shed
Aborted (A) Gametangia          Apex of sporophyte wither prior
                                  to spore formation, usually in
                                  ECP, LCP or ECI stages
Juvenile (J)                    Gametangia become visible.
                                  Pale green colour
Immature (I)                    Gametangia reach half length of
                                  dehisced gametangia
Mature (M)                      Apices of gametangia rupture.
                                  Archegonia become receptive for
                                  fertilisation and liberation of
                                  antherozoids begins.
Dehisced(D)                     Development of brown colouration
                                  begins in gametangia at
                                  ruptured apices
Aborted (A)                     Development of brown or hyaline
                                  colouration begins in
                                  gametangia with unruptured
                                  apices in J or I stages

Table 2. Sex expression of a. Rhaphidorrhynchium amoenum
b. Rosulabryum billarderii c. Rhynchostegium
tenuifolium d. Wijkia extenuata in different
aged forest post harvest (NE = Non expressed stems).

a. Rhaphidorrhynchium amoenum (pleurocarpous)

                                              Forest age

Number of:                            10       15       20       25

Stems examined                       200      200      200      200
% fertile stems                     65.5     82.5     75.5     55.5
% NE stems                          34.5     17.5     24.5     44.5
Female stems                           0        6       12        5
Male stems                             0        9        6        5
Male & female stems                  131      150      133      101
NE stems                              69       35       49       89
Perichaetia                          304      223      236      205
Perigonia                            166      197      229      187
Ratio perichaetia:perigonia        1.8:1   1.13:1   1.03:1   1.09:1
Archegonia                            93      138       75      224
Antheridia                           285       91      338       72
Ratio archegonia:antheridia        1:3.1    1.5:1    1:4.5    3.1:1
Sporophytes                          163      153      112      123
Fertile stems with sporophytes       131      165      151      111

b. Rosulabryum billarderii (acrocarpous)

                                             Forest age

Number of:                           10       15       20       30

Stems examined                      200      200      200      200
% fertile stems                    23.5       15     35.5       28
% NE stems                         76.5       85     64.5       72
Female stems                         46       29       58       49
Male stems                            1        1       13        7
NE stems                            153      170      129      144
Perichaetia                          46       29       58       49
Perigonia                             1        1       13       14
Ratio perichaetia:perigonia        46:1     29:1    4.5:1    3.5:1
Archegonia                           25      168        0       54
Antheridia                           14        0       87       24
Ratio archegonia:antheridia       1.8:1    168:0      0:9    2.3:1
Sporophytes                          11        7       12       10
Fertile stems with sporophytes       47       30       71       56

c. Rhynchostegium tenuifolium (pleurocarpous)

                                             Forest age

Number of:                           10       15       20       25

Stems examined                      200      200      200      200
% fertile stems                    48.5     37.5     46.5       35
% NE stems                         51.5     62.5     53.5       65
Male & female stems                  97       75       93       70
NE stems                            103      125      107      130
Perichaetia                         120       84       94      134
Perigonia                           103      127      104      188
Ratio perichaetia:perigonia       1.2:1    1:1.5    1:1.1    1:1.4
Archegonia                          186       84      102       78
Antheridia                          311      323      300      442
Ratio archegonia:antheridia       1:1.7    1:3.9    1:2.9    1:5.7
Sporophytes                          12        5       17       23
Fertile stems with sporophytes       97       75       93       70

d. Wijkia extenuata (pleurocarpous)

                                              Forest age

Number of:                            10       15      20       25

Stems examined                       200      200     200      200
% fertile stems                     59.5     44.5    58.5       69
% NE stems                          40.5     55.5    41.5       31
Female stems                          71       38      62       70
Male stems                            30       51      55       68
Ratio female:male stems            2.4:1    1:1.3   1.1:1    1.0:1
NE stems                              99      111      83       62
Perichaetia                          129       77     146      118
Perigonia                             94      229     204      186
Ratio perichaetia:perigonia       1.37:1   1:2.97   1:1.4   1:1.58
Archegonia                           141      142     142      124
Antheridia                           131      439     355      147
Ratio archegonia:antheridia       1.08:1   1:3.09   1:2.5   1:1.19
Sporophytes                           30       26      24       17
Fertile stems with sporophytes       119       89     117      138

a. Rhaphidorrhynchium amoenum (pleurocarpous)

                                     Forest age     Total   Mean

Number of:                           30       63

Stems examined                      200      200    1200
% fertile stems                    70.5     53.5            67.2
% NE stems                         29.5     46.5              33
Female stems                          0        0      23
Male stems                            0        0      20
Male & female stems                 141      107     763
NE stems                             59       93     394
Perichaetia                         243      274    1485
Perigonia                           264      150    1193
Ratio perichaetia:perigonia      1:1.09    1.8:1            1.2:1
Archegonia                            0      123     653
Antheridia                          190      215    1191
Ratio archegonia:antheridia         0:1    1:1.8            1:1.8
Sporophytes                         113      130     794
Fertile stems with sporophytes      141      107     806

b. Rosulabryum billarderii (acrocarpous)

                                 Forest
                                    age

Number of:                           63    Total    Mean

Stems examined                      200     1000
% fertile stems                      31             26.6
% NE stems                           69             73.4
Female stems                         53      235
Male stems                            9       31
NE stems                            138      734
Perichaetia                          53      235
Perigonia                             9       38
Ratio perichaetia:perigonia       5.9:1             6.2:1
Archegonia                           45      292
Antheridia                            0      125
Ratio archegonia:antheridia        45:0             2.3:1
Sporophytes                          20       60
Fertile stems with sporophytes       62      266

c. Rhynchostegium tenuifolium (pleurocarpous)

                                 Forest
                                    age

Number of:                           30    Total    Mean

Stems examined                      200     1000
% fertile stems                    41.5             41.8
% NE stems                         58.5             58.3
Male & female stems                  82      417
NE stems                            118      583
Perichaetia                         128      560
Perigonia                            95      617
Ratio perichaetia:perigonia       1.4:1             1:1.0
Archegonia                           88      538
Antheridia                           78     1454
Ratio archegonia:antheridia       1:1.1             1:2.7
Sporophytes                          33       90
Fertile stems with sporophytes       82      417

d. Wijkia extenuata (pleurocarpous)

                                     Forest age

Number of:                           30       63    Total   Mean

Stems examined                      200      200    1200
% fertile stems                      60     69.5            60.2
% NE stems                           40     30.5            41.3
Female stems                         61       83     385
Male stems                           59       56     319
Ratio female:male stems           1.0:1    1.5:1           1.2:1
NE stems                             80       61     496
Perichaetia                         106      169     745
Perigonia                           225      357    1295
Ratio perichaetia:perigonia      1:2.12   1:2.11           1:1.7
Archegonia                           99      170     818
Antheridia                          115      451    1638
Ratio archegonia:antheridia      1:1.16   1:2.65           1:2.0
Sporophytes                          21       33     151
Fertile stems with sporophytes      120      139     722

Fig. 3. Sporophyte developmental sequences for
(a) Rhaphidorrhynchium amoenum (blue), (b) Wijkia extenuata
(black) and (c) Rhynchostegium tenuifolium (red)
showing peaks of occurrence for phenological stages.
Data was pooled from forest regenerating following
logging (i.e. at 10, 15, 20, 25 and 30 years-since
-harvest) and from a 63 year old forest. Arrow
indicates increasing level of maturity. SV=Swollen
venter, ECP=Early calyptra in perichaetium, LCP=Late
calyptra in perichaetium, ECI=Early calyptra intact,
LCI=Late calyptra intact, EOI=Early operculum intact,
LOI=Late operculum intact, OF=Operculum fallen,
EF=Empty and fresh.

Phenological   Spring   Summer   Autumn   Winter   Spring   Summer
stage

EF                                                          (abc)
OF                                         (a)      (bc)
LOI                                        (a)      (a)
EOI                                        (b)
LCI                               (a)      (ab)     (a)
ECI                               (a)      (b)
LCP                      (ac)     (b)
ECP                      (ac)     (b)
SV              (a)      (bc)
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Title Annotation:Research Report; Rhaphidorrhynchium amoenum, Rhynchostegium tenuifolium, Wijkia extenuata, and Rosulabryum billarderii
Author:Sinclair, Bernadette; Gibson, Maria
Publication:The Victorian Naturalist
Article Type:Report
Geographic Code:8AUST
Date:Dec 1, 2015
Words:6239
Previous Article:From the editors.
Next Article:The earliest known camera trapping in Australia: a record from Victoria.
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