Plants and Ecology 2011:3

Home , Atrichum undulatum, Buxbaumia viridis, Microbryum, Polytrichaceae

Wind dispersal of spores with focus on bryophytes

Niklas Lönnell

Plants & Ecology

Plant Ecology 2011/3 Department of Botany Stockholm University

Wind dispersal of spores with focus on bryophytes

by Niklas Lönnell

Supervisors: Kristoffer Hylander, Johan Ehrlén, Sebastian Sundberg, Bengt Gunnar Jonsson

Plants & Ecology

Plant Ecology 2011/3 Department of Botany Stockholm University

Plants & Ecology

Plant Ecology Department of Botany Stockholm University S-106 91 Stockholm Sweden

Summary Investigation of dispersal, especially long-distance dispersal (LDD), is of utmost importance for the understanding of many patterns and processes like species distributions, range expansions including responses to climate change and metapopulation dynamics. The exact distance beyond which dispersal can be defined as LDD is dependent on the species and can vary from 100 metres to intercontinental distances. The wind dispersal of small diaspores has been poorly studied (Diaspore sizes: e.g. in bryophytes (diameter 10–50(–100) μm), fungi (3–10–(300) μm), ferns (30–100 μm). According to Stoke's law they can travel farther than larger diaspores of the same shape and density given the same wind speed, even if larger seeds can increase the buoyancy with features like pappi or wings. Diaspore size, shape, weight, type of abscission (active or passive), abscission height, abscission time, horizontal wind speed and thermal updrafts/turbulence can influence the dispersal distances. The source i.e. the number of diaspores produced is very strong in many species (cfr the production of 100 million spores/m2 in Pleurozium schreberi). The most common direct method for studying dispersal includes putting out a point source and a number of spore traps at increasing distances. Indirect methods encompass approaches such as comparing 1. the genetic similarity between populations in different parts of a country or continent, 2. successful colonizations with connectivity (i.e. studying the patterns of realized dispersal), 3. the longevity of diaspores with the species distribution and 4. the species composition with prevailing winds. The question concerning the temporal and spatial scales on which species with small diaspores are dispersal limited still remains to be answered.

Sammanfattning Kunskapen om hur arter sprider sig särskilt över långa avstånd är viktiga för att förstå t.ex. arters utbredningsmönster, förändringar i artutbredningar som svar på t.ex. klimatförändringar. Det exakta avståndet över vilket spridning räknas som räknas som långdistansspridning kan variera från 100 m till avstånd mellan olika kontinenter. Vindspridning av små spridningsenheter har inte studerats i någon större utsträckning. (Storleksexempel: mossor (diameter 10–50(–100) μm), svampar (3–10–(300) μm), ormbunkar (30–100 μm)). De kan sprida sig längre än större frön som dock ibland har olika slags anpassningar som hårpenslar och vingar för att kunna spridas längre. Spridningsenhetens storlek, form, vikt samt hur (aktivt eller passivt) och på vilken höjd de kommer ut i luften, vindhastighet och om det förekommer turbulens eller varmluft som stiger kan påverka spridningsavstånden. Antalet spridningsenheter som produceras är stort hos många arter (t.ex. 100 miljoner sporer per kvadratmeter hos väggmossa Pleurozium schreberi). En vanlig metod att studera spridning är sätta ut en källa och ett antal fällor på olika avstånd. Även indirekta metoder använts så som att jämföra 1. genetisk skillnad mellan olika lokaler och populationer 2. framgångsrik etablering med hur långt det är till närmaste möjliga källor 3. hur långlivade spridningsenheterna är och vilken utbredning arten har samt 4. artsammansättning med förhärskande vindriktningar. I vilken utsträckning i fråga om tid och rum som arter med små spridningsenheter är begränsade av sin spridningsförmåga återstår att utreda.

Contents Summary ...... 3

Sammanfattning ...... 3

Contents ...... 4

What is dispersal? ...... 5

Transportation ...... 6

Abscission ...... 7

Abscission height ...... 9

Buoyancy ...... 10

Diaspore shape ...... 11

Diaspore size ...... 11

Diaspore longevity ...... 15

Number of diaspores ...... 16

Diaspore banks ...... 17

Dormancy ...... 19

Deposition ...... 19

How to study dispersal ...... 20

Direct methods ...... 20

Lagrangian methods – tracking individuals/single diaspores ...... 20

Eulerian methods – trapping ...... 21

Indirect methods ...... 23

Biogeographical studies ...... 26

Other studies ...... 27

Models ...... 28

Phenomenological models...... 28

Mechanistic models ...... 29

Conclusions ...... 29

References ...... 30

What is dispersal? The general meaning of the word "dispersal" can be stated as "the action or process of distributing or spreading things or people over a wide area" (Soanes & Stevenson 2005). In a biological context definitions like "intergenerational movement" (Bullock et al. 2002), "the actual scattering or distributing of organisms on earth's surface"; "transport of diaspores" (Holmes 1979) or "unidirectional movement of an individual away from its place of birth" (Clobert et al. 2001; Nathan 2008) may be more appropriate. As Pijl (1982) remarks, the term dispersal has been used synonymously with distribution which may lead to confusion when reading older publications. Since this work will be restricted to plants, a definition relevant for this context could be "transportation of diaspores away from the plant of origin". "Diaspore" is general term for a plant dispersal unit for example a seed, a spore, or a gemma.

The term "long-distance dispersal" (LDD) is more difficult to define. How far is long? The absolute distance varies between different organism groups as well as species. There are two ways of defining the approximate distance beyond which dispersal can be defined as LDD: to set an absolute value or to set a relative value beyond which a certain low percentage of diaspores are being dispersed. Cain et al. (2000) suggest 100 m as an absolute value and a relative value based on the distance beyond 1 % of the diaspores travel. In the examples given by Nathan (2008) the distance is a few hundred metres. Nathan (2005) suggests one should write the most relevant value for the study in question first, followed by the corresponding value for the other in parentheses after e.g. 1000 m (0.1 %). For Sphagnum Sundberg (2005) defines LDD as dispersal more than 1 km which is beyond the normal-sized mire in the study area. However, when Zanten & Pócs (1981) discuss "long-range dispersal" only distances over 2000 km were considered.

Production

Abscission

Transportation

Deposition Dispersal

Establishment

l Figure 1. The different stages of dispersal. Realized or effective dispersal can include establishment as well as production of new diaspores. 5

The dispersal can be divided into three different stages: abscission (release, liberation and discharge), transport (transportation, transfer) and deposition (capture) (Fig.1). But for dispersal to have an effect, post-dispersal events like germination and survival of the progeny must be successful. Hence "Effective dispersal" includes the establishment of a new plant that can reproduce itself (Nathan 2008). This can also be named "realized dispersal". At the regional scale species can be principally dispersal limited or habitat limited (Münzbergová & Herben 2005). The establishment phase is critical for many bryophytes and both germination and protonema growth could be limited by factors such as pH and water availability (Wiklund & Rydin 2004). As the production (formation) of diaspores is also a vital component in the success of dispersal, it may be included in an extended definition of what successful dispersal incorporates (Löbel et al. 2009).

I will deal with dispersal in space in this paper. Dispersal in time is, however, briefly discussed under the title "Diaspore banks".

Transportation The term used to describe the transportation is often a combination of a prefix describing the name of the agent in Greek and a suffix describing what kind of object that is being transported. Pijl (1982) describes the terminology extensively and I summarise it as follows. The suffix "- gamy" can be used for describing the transportation of and differentiation of gametes. The suffix "-phily" can be used of the transport of spores, especially microspores and their successors, pollen grains. The suffix implies that the transportation is to a friendly place e.g. the stigma/the megaspore (philein (Gr.) = to love). The suffix "-chory" is used for mere dispersal of seeds etc. (chorein (Gr.) = to wander). When referring to the transportation of isospores (same spore size in both sexes) of cryptogams both "-phily" and "-chory" can be used.

I will use "-chory" for transportation of spores in bryophytes and fungi.

Dispersal by an animal vector may expand the range as well as improve the percentage of diaspores that end up on a suitable substrate. This paper, however, will deal with abiotic vectors,

more precisely wind dispersal of spores (anemochory) with some references to wind dispersal of seeds (anemochory) and wind pollination (anemophily).

Bryophytes are generally considered to be hydrogamous even if Cronberg et al. (2006) demonstrated that springtails and mites may act as vectors of bryophyte gametes as well.

Abscission There are a multitude of ways and adaptions of how to release the diaspores into the air. Abscission can be active and explosive or passively triggered by wind, convection or raindrops. The role of abscission timing has been found to be an important factor for LDD (Greene 2005; Skarpaas et al. 2006; Soons & Bullock 2008).

Vascular plants

Pollen in wind-dispersed species is mostly released passively. In many species with dust seeds the abscission is passive and the seeds are discharged as the wind moves the drying capsule.

In Polypodiaceae the spores are actively discharged when the thickened sporangium wall is thrown back as the water content in the cells decreases. However in other species within Marattiales and Ophioglossales the discharge is passive. Club mosses Lycopodium-species have passive discharge while Selaginella-species have active. (Ingold 1974)

Liverworts

Most leafy liverworts have a capsule which opens entirely when the capsule wall breaks along four lines which expose the spore mass when it dries out. Inside the capsules there are elaters, up to 0.5 mm long tubes with spiral reinforcement in the walls. In some species (e.g. Cephalozia bicuspidata) the elaters spring loose from the capsule wall when they dry and hence can bring spores up in the air. In others, the elaters show more moderate hygroscopic movement (e.g. Marchantia polymorpha) and in still others they show very slight hygroscopic movement (e.g. Pellia epiphylla). In some species (e.g. Frullania dilatata) both ends of the elaters are fixed in the upper and lower part of the capsule wall and they act as spiral springs and cause a violent opening of the capsule which can throw spores 2 cm up in the air. (Ingold 1974)

Mosses

Unlike in liverworts, abscission is passive in most moss species. However in Sphagnum the spores are released explosively up to 20 centimetres in the air when the lid of the capsule dehisces (Ingold 1974). Turbulent vortex rings are created and facilitate dispersal of the spores (Whitaker & Edwards 2010). How high the spores reach varies according to capsule size (Sundberg 2010b). The violent abscission of the spores is due to air pressure at the basal part the capsule under the spore sack and has been compared to firing an air gun (Ingold 1974). That the air pressure causes the eruption has been questioned (Duckett et al. 2009) and the discussion continues about what causes the violent abscission (Duckett et al. 2010; Sundberg 2010a). The capsule of Andreaceae opens in four narrow openings along the side of the capsule. The top of the capsule is still intact unlike the case in liverworts. In the Polytrichaceae the capsule has a peristome which is like a membrane with small holes through which spores can escape, when wind moves the capsule, like from a saltcellar.

Within the true mosses (Bryopsida) most species have a capsule that dehisces with a lid and the mouth of the capsule has a peristome with one or two layers of teeth. The peristome teeth move when air humidity changes (hygroscopic). In the vast majority of moss species the peristome shuts when moist and opens when it dries out (xerocastique). However in a few species the peristome opens when it is moist (hygrocastique) (Hedenäs 1992). Hygrocastique peristomes occur foremost in epiphytic species in e.g. the families Meteoriaceae and Orthotrichaceae (Zygodon, Macromitrium, Orthotrichum, Orthomitrium) and the genera Pylaisia, Leucodon, Cryphaea and in the species Coscinodon cribosus (cfr. Hedenäs 1992; Porley & Hodgettts 2005).

The hygroscopic movement of the outer peristome teeth can throw spores into the air. During 171 such movements the number of discharged spores was calculated to be 15,000 out of a total of approximately 500,000 spores in one capsule of Eurhynchium confertum (Ingold 1974). The peristome can regulate when the spores are to be released and the peristome structure can also affect wind conditions and cause turbulence which can facilitate spores to become airborne. During dry conditions the probability of convection and longer transportation are higher. In wet conditions deposition near the capsule of origin is higher through wet deposition. So why do

some species have a hygrocastique peristome that prevents dispersal during dry conditions? Many of those species are epiphytes and the establishment phase is suspected to be the bottleneck for many epiphytic species (Löbel 2009). A higher establishment rate may be more important than long dispersal in these species. But some epiphytes as well as species on other substrates lack a peristome or have a heavily reduced one. Why is that? Vitt (1981) implies that this is a character of xerophytic species, but he offers no explanation for the benefit of this in a dry environment. Shaw & Robinson (1984) note that many species with erect capsules lack a peristome, but they also remark that as many of the species with erect capsules, e.g. epiphytes, grow on perpendicular surfaces and the orientation of the capsules becomes in fact horizontal and within the genus Schizymenium the species with the most advanced peristome have erect capsules whereas the ones with reduced peristome are pendant.

Raindrops can also trigger spores to leave the capsule, and the splash cups with gemmae in the thallous liverwort Marchantia polymorpha extend gemma transportation distances.

Fungi and Lichens

In fungi and lichens the spores are released both by active and passive discharge. Some ascomycetes generate a wind by synchronizing the abscission of spores (Roper et al. 2010). In many polypores the discharge away from the fruiting body is passive where the spores fall from console-shaped fruitbodies even if the release from the asci is active.

Abscission height The height from which the diaspores are released influences how far the diaspores travel. Firstly, it influences the time for the diaspore to reach the ground, which increases the chance that updrafts or winds will move the diaspore vertically and horizontally. Secondly, the amount of time that the abscission point is above the laminar layer is influenced and hence the opportunities for diaspores to be released in wind conditions more suitable for dispersal.

If thermal updrafts are disregarded the distance (xd) that a diaspore travel can be described as a function of the abscission height (h) and horizontal wind velocity (u) and the terminal velocity of the diaspore (vt) (Kuparinen 2006): 9

xd = hu/vt

In mosses it ranges from less than one millimetre to tens of centimetres for those species with the longest setae. In liverworts it ranges from Riccia whose spores are released only when the thallus is disintegrated to e.g. Marchantia with up to 1 decimetre tall gametophores. In the average leafy liverwort the thin, hyaline seta is elongated to a few centimetres after the spore capsule is fully developed. In club mosses as well as horsetails Equisetum spp. the spores are released at the highest point of the plant which range from a few centimetres to over a metre in the tallest species. Ferns release spores from specialized fronds or from the sporangia on the lower side of unspecialized fronds and the height varies along with the height of the species from a few centimetres to several metres in tree ferns. Many basidiomycetes release spores from the underside of the hat of the fruit body toadstool/mushrooms. The abscission height in ground dwelling lichen is rather small as well, from millimetres to a few centimetres.

Many epiphytic or epilithic species reaches much higher and the abscission heights for these species are noticeably increased. If there is a dense canopy the wind speed may be negatively affected.

Buoyancy Buoyancy is sometimes used to describe the ability of a diaspore to float in water. However, in the context of this report it is used to describe the ability for a diaspore to "float" or remain in the air. This ability is often estimated by the terminal velocity (=falling velocity or settling speed). The terminal velocity can be estimated from Stoke's law. It applies to spherical objects with a smooth surface. For very small and very large diaspores one can apply some corrections to adjust the equation to better reflect the true terminal velocity (Gregory 1973). This approximation must be complemented with measurements to determine the true terminal velocity that can deviate from the ideal terminal velocity due to deviating (non-spherical) shape, surface structures and air-filled spaces within the diaspore. The terminal velocities for pollen are from 2 to 6 cm/s (Whitehead 1983).

2 Stoke's law: vs = (2/9) (σ-ρ/μ) *gr vs = terminal velocity σ = density of sphere in g/cm3 (water = 1.00) ρ= density of medium (air = 1.27x10-3 g/ cm3) g = acceleration of gravity (981 cm/s2) μ = viscosity of medium (air at 18° C = 1.8 x 10-4 g/ cm/s) r =radius of sphere in cm

There are also simplifications to similar estimates for non-spherical objects (Sundberg 2010b).

Diaspore shape The shape varies much among different spores and pollen types. Many are rounded but others are cylindrical, oval, kubic etc. Most bryophyte spores are more or less isodiametric while fungal spores vary more in shape by often being longer than wide.

Among the 303 european polypores investigated by Kauserud et al. (2008) most species have a spore shape ratio between 1 and 3. The largest ratio (6.5) belonged to Skeletokutis stellae. White rot species and parasites have more spherical spores than brown rot species and saprotrophs, and larger spores tend to be more spherical.

How the shape affects the terminal velocity and hence the dispersal capacity is not fully illuminated. It has been suggested, however, that an elongated shape should decrease the terminal velocity (McCubbin 1944; Gregory 1973).

Diaspore size In different taxonomical groups and different publication the size of a diaspore can be estimated in length and width, diameter, area (length x width), volume and weight. To be able to compare the different estimates I have made the following conversion table (Table 1). However this is a great simplification since it assumes that the diaspore is smooth, spherical and has the density of 1 g/cm3.

As the size increases the terminal velocity increases. What exact implication this has for dispersal is harder to predict. In aerosols (when particles are suspended in air like smoke) most particles have a diameter less than 5 μm. Wilkinson (2001) investigated testate amoeba assemblages in the Artic and Anarctic and found that the largest species confined to one of those areas was 230 μm while those with a cosmopolitan distribution had a maximum size of 135 μm.

Table 1. Overview over different measures used to define the size of diaspores. The conversion anticipates that the diaspore is smooth, sphaerical and has a specific density of 1 g/cm3.

Diameter Area Volume Weight Terminal velocity μm μm2 μm3 mg mm/s 1 1 0.5 0.0005 0.03 5 25 65 0.07 0.76 10 100 523 0.52 3 20 400 4187 4 12 50 2500 65417 65 76 100 10000 523333 523 302 200 40000 4186667 4187 1210 500 250000 65416667 65417 7560

Pollen grains and spores vary much in size; From 1–5 μm (spores of Penicillum and Aspergillus and pollen of Myosotis) to 200 μm (e.g. pollen in Curbitaceae and Nyctaginaceae) or even 800 μm (megaspores in Selaginella). (Nilsson 1980). However, most wind-dispersed spores and pollen are usually smaller.

Pollen grains of most anemophilous plants have a diameter of 20–30(–60) μm. Some species have pollen grains with air sacs to facilitate the dispersal. One example of this is pines Pinus spp. that have large (50–150 μm) and heavy pollen grains (Faegri & Pijl 1979).

Pijl (1982) mentions examples of weights from some families with dust diaspores: 0.003 mg (Orchidaceae), 0.004 mg (Pyrolaceae) and 0.001 mg (Orobanchaceae). The seeds from the 12

Finnish species of Pyrolaceae are 200 μm to 1 mm long and 80 μm to 200 μm broad (Pyykkö 1968). The seeds of Orchidaceae are also elongated and some examples of seed lengths in Orchidaceae range from 0.19 to 3.8 mm (Clifford & Smith 1969). The larger orchid seeds may thus not qualify as dust seeds. Seeds that are lighter than 0.02 mg–0.05 mg and seeds with plumes and wings can be classified as having wind as the primary dispersal vector (Greene & Calogeropoulos 2002).

Ferns tend to have larger spores than mosses and have higher points of initial spore release (Ingold 1974). Spores of ferns are 30–100 μm (Tryon & Lugardon 1990 in Wolf et al. 2001). Spores of Lycopodium and Selaginella in Taiwan range from 20–40 μm (Huang 1981).

Histogram of spore size in liverworts Histogram of spore size in mosses

120

100

Number of species of Number

0 0

20 40 60 80 100 120 50 100 150 200

Mean spore diameter (µm) Mean spore diameter (µm)

Figure 2. The mean spore size of 1035 British bryophyte species according to Hill et al. (2007).

Most bryophyte spores have a diameter that is less than 50 μm. A higher proportion of the liverworts than of the mosses have spore diameters in the range from 40 to 100 μm (Hill et al. 2007). (Fig. 2)

The largest moss spores are found in Archidium. Most of the species in this genus have an average spore diameter between 100 μm and 200 μm. The species with the largest average spore diameter is A. brevinerve 235 (200–260) μm whereas the one with the largest measured spore is A. ohioense 162 (110–310) μm (Snider 1975). The species that is widespread in Europe is A. alternifolium 180 (139–223) μm (Boros et al. 1993). The cleistocarpous capsule has a very short seta and is hidden among the leaves. The spores are spread when the capsule wall is ruptured by decomposition. This suggests that wind dispersal is not likely in Archidium and other vectors should may be important, e.g. water. The same could be said about the species in the thallous liverwort genus Riccia which also have large spores.

As Mogensen (1981) suggests the spore diameter distribution in a single species may not be unimodal. The bimodality can be due to that some spores are aborted or that the sexes have spores of different size. It may be a matter of resolution and accuracy of measurement as he showed for Ceratodon purpureus.

The main focus in this report has been on spores as they usually are smaller and hence more likely to be contributing to the LDD of most species. However, it is important not to forget that bryophytes and lichens can disperse by means of fragmentation as well as by specialized asexual diaspores. Fragments and asexual diaspores have an advantage in the establishment phase and are generally thought to contribute to short-distance dispersal. The fragments of bryophytes retrieved from a late snowbed in early spring in the alpine zone consisted primarily of species occurring in the vicinity, but a few species from the subalpine belt were found as well (McDaniel & Miller 2000). This implies that in open habitats fragments can even be dispersed by wind over the snow but it does not contradict that this includes mostly short-distance dispersal. However, in Anastrophyllum hellerianum the spores and gemmae are of equal small and are thought to be able to contribute to LDD as well (Pohjamo et al. 2006). Tubers seem unlikely to disperse by wind since they mostly develop on rhizoids in the soil. Lichens have a diversity of specialized modes for asexual propagation. Lichhen soredia were the most common diaspores in a survey with Rotorod samplers on Signy Island in Antarctica (Marshall 1996).

Most fungal spores have a diameter of around 10 μm but they range from 3 μm in diameter in Beauveria spp. to up to 200 μm in Tuber (ascospores), Mucorales (zygospores) and Endogone 14

(chlamydospores) (Weber & Hess 1976). Among the 303 European polypores investigated by Kauserud et al. (2008) 85 % of the species have spores with a volume less than 100 μm3. Chaetoporellus latitans has the smallest spores (0.94 μm3), while Perenniporia ochroleuca has the largest spores (548 μm3). These volumes (100, 0.94 and 548 μm3) correspond to diameters of approximately 6 μm, 1 μm and 10 μm of spherical spores. Species with larger basidiocarps tend to produce larger spores; Parasitic species have larger spores than saprotrophic species; Species on deciduous wood have larger spores than species on coniferous wood; White rot species have larger spores than brown rot species on the same kind of wood (deciduous and coniferous)(Kauserud et al. 2008). Basidiospores in the species of hymenomycetes (including e.g. the orders Agaricales, Russales and Boletales) are rather small (mean length = 8.4, width = 4.9 μm and volume = 156 μm3) and elongated (mean L/W quota = 1.8) (Parmasto & Parmasto 1992).

Diaspore longevity To disperse in space as well as in time it is necessary that spores can survive the conditions in the air and in the ground. The spore may encounter drought, UV-light and freezing in the atmosphere. Zanten (1977; 1978) tested the viability of spores from several species from the southern hemisphere and New Zealand as well as from the northern hemisphere after drought, dry freezing and wet freezing up to three years. He concluded that the species with restricted distributions stayed viable for a shorter time than those that occurred on different continents. He also concluded that the species from the northern hemisphere on average stayed viable for a longer time. Malta (1922) tried to germinate moss spores from herbarium specimen of different age. Most collections that were older than 10 years did not germinate, and most of the spores that germinated were younger than 5 years. The oldest collection which contained viable spores was 16 years (Ceratodon purpureus). This result contradicts the fact that weedy plants like Ceratodon purpureus and Funaria hygrometrica are seldom found in the diaspore bank. During (1987) tried to investigate this by sowing spores of Funaria hygrometrica in a chalk grassland. The spores germinated in the greenhouse still after two years but not in the field. Löbel (2009) noted a 30–40 percentage decline in viability of spores during 50 days of dry storage.

Whitehouse (1984) found that tubers of Dicranella staphylina were still viable after 50 years of storage. Sundberg & Rydin (2000) showed that 15-35 % of Sphagnum spores survive 13 years of storage under humid conditions.

Spores and fragments were stored in water for up to six months of the following five mosses: Schistidium rivulare, Racomitrium aciculare, Dicranoweisia crispula, Oligotrichum hercynicum and Ceratodon purpureus by Dalen & Söderström (1999). The spores survived longer when stored under dry conditions compared with storage in water except for in Schistidium rivulare, whereas the fragments did not have a higher survival stored under dry conditions (Dalen & Söderström 1999).

The spores of the fungus Beauveria bassiana showed 90% germinability after 635 days in darkness at 0% relative humidity and 8 °C. However within 28 days in light at 75 % relative humidity at 18°C none were germinable. (Clerk & Madelin 1965)

Number of diaspores The number of spores per capsule is substantial. Ingold (1974) states that the capsule of Eurhynchium confertum contains between 250,000 and 750,000 spores. Kreulen (1972) estimated the number of spores in one capsule to be 450,000 in Atrichum undulatum and 1.4 million in Polytrichum juniperum. Buxbaumia viridis has 6 (1.4–9) million spores per capsule (Wiklund 2002). Sundberg & Rydin (1998) counted the number of spores in eight peatmosses and estimated from 18,500 spores per capsule in Sphagnum tenellum to 240,000 in Sphagnum squarrosum. For additional estimations of the number of spores per capsule see Fig. 3. More interesting for dispersal is the spore output per area unit. Sundberg (2002) studied several Sphagnum species and reported an annual production of 16 million spores per square metre of mire. Longton (1976) estimated the spore production of Pleurozium schreberi at one site to be 100 million spores per square metre. The spore production of the liverwort Ptilidium pulcherrimum varied from approximately 20 to 300 million spores per square metre colony during a four year period and the production per square metre of forest land was estimated to 75,000-150,000 (Jonsson & Söderström 1988). Spore production estimations have been done for

three moss species in millions per square metre of substrate: 37 for Atrichum undulatum, 7,400 for Grimmia pulvinata and 38,300 for Tortula muralis (Longton & Schuster 1983). So even if the vast majority of the spores are deposited very near the mother colony there are many that can contribute to the LDD.

Figure 3. The number of spores per capsule (y-axis on a logarithmic scale) versus the mean spore diameter (x-axis in μm). The data have been compiled from several sources (Ingold 1959; Schuster 1966; Kreulen 1972; Ingold 1974; Longton 1976; Mogensen 1978; Söderström & Jonsson 1989; Miles & Longton 1992; Boros et al. 1993; Sundberg & Rydin 1998; Wiklund 2002; He & Zhu 2010; Cuming 2011) and are based on estimates from 92 species with many species from some genera e.g. Riccia and Sphagnum.

Diaspore banks Bryophytes may survive in the soil as fragments of e.g. the stem, spores and specialized asexual propagules such as tubers or gemmae. It may facilitate species' survival under unfavourable conditions. This makes it more difficult to interpret and investigate dispersal in space under certain circumstances.

Dominant, common pleurocarpous mosses seem to be rare in the diaspore bank, while short- lived species that only are present above ground some time after disturbance seem to be more common in the diaspore bank. A higher proportion of larger than of smaller diaspores is represented in the diaspore bank of bryophytes. The opposite is true for vascular plants. As mentioned above not only spores can constitute the diaspore bank. For example Barbiolphozia lycopodioides was present in the diaspore bank in forests in northern Sweden even if it does not produce gemmae and sporulates very rarely (Jonsson 1993). Most studies of diaspore banks have consisted of cultivating soil samples (During 1997; During 2001). To assess if the diaspore bank consists of spores or vegetative parts of the bryophyte is therefore difficult. It has been proven that Sphagnum can regenerate from the diaspore bank Clymo & Duckett 1986; Sundberg & Rydin 2000). The latter buried spores at different depth and that the survival was best under wet but aerobic conditions and that the spores died within 2-3 years under anaerobic conditions.

Diaspore banks can be classified as transient, short-term persistent or long-term persistent (During 2001) (Table 2). Since a direct measurement of the diaspore age is difficult to acquire, the age must be assessed by means of indirect estimates such as the time since the species was observed last or some approximation of humus accumulation rates.

Table 2. Different types of diaspore banks with some examples among the bryophytes.

Diaspore banks Time frame Example species Spore size transient months short-term persistent 1–5 years Anthoceros Anthoceros punctatus 36–60 μm Phaeoceros (30–)38–56(– 75) (Zanten & Pócs 1981) long-term persistent >5 years Physcomitrium –30 μm

sphaericum

Frahm (2006) suggested that the occurrence of several rare thermophilic openland species (Microbryum curvicolle, Acaulon triquetrum, Weissia longifolia) on the edge of a forest road could be interpreted as coming from a diaspore bank from the time when a wineyard had been situated at the site almost 100 year old ago. The species are very rare in the area and the nearest known recent site is 40–100 km away.

Dormancy Most bryophyte diaspores seem to have enforced dormancy, i.e. they start to germinate when suitable conditions concerning e.g. light and water are available. There seems to be some exceptions. The disc-like gemmae in Blasia pusilla do not seem not able to germinate right away after dispersal (During 2001). Laaka-Lindberg & Heino (2001) studied the gemmae of Lophozia silvicola and suggested that part of them enter dormancy. Sundberg & Rydin (2000) noted a better germination of 3 years old spores than 2 years old ones and concluded that it could be due to the wet and cool conditions during the third year and the spores' need to be hydrated for a long period and possibly chilled to germinate.

Deposition Deposition of small diaspores is highly affected by the weather conditions. Turbulent diffusion and precipitation are two important factors (Schmidt 1967). A small object collects diaspores better than a large object due to the thickness of the boundary layers around objects. With increasing wind velocity the boundary layer becomes thinner. A beech pollen with a diameter of 42 μm settles more easily than a birch pollen with a diameter of 21 μm but the difference decreases with increasing wind velocity (Whitehead 1983).

Besides the source strength, the amount of suitable target habitat in an area is determining the probability of realized dispersal because the number of diaspores that reaches a suitable habitat varies with the area of that habitat if we assume a random dispersal. n/N~a/A

where N=the total number of diaspores, n=the number of effective diaspores, a=the area of target surfaces/suitable area, A=the total area of the surroundings (vegetation and habitat). a (the total area of stigmata) is lower for pollination than for most other kinds of spore dispersal where the total area of the target substrate often is larger. (Faegri & Pijl 1979)

How to study dispersal Dispersal can be studied by direct or indirect methods. The direct methods can be divided into Lagrangian methods and Eulerian methods. The first method include tracking a single diaspore and the second trapping diaspores

Direct methods

Lagrangian methods – tracking individuals/single diaspores These methods include measuring how far, how fast and in what direction individuals move and have the advantage that it is easier to track LDD events. This kind of approach is used in studies first and foremost on large animals with radio or satellite tracking, but experiments with insects has also been performed (Nathan et al. 2003). It is also easier to detect clumped patterns in the dispersal of diaspores with these kinds of methods. It may also be applied to plants dispersed by animals and humans. (Bullock et al. 2006)

The movements by stolons of clonal plants such as Trifolium repens can be backtracked by looking at the annual growth of the individual (Cain et al. 1995), but this will be restricted to short distances and cannot be defined as LDD by any means.

As Langrangian methods are rather labourious the number of diaspores that can be followed is limited (Nathan et al. 2003). Larger diaspores, like those with pappi in e.g. Cirsium arvense and Senecio nemorensis, can be followed individually (Tackenberg 2003). However as the size of the diaspores decreases it becomes more difficult to follow them. Hence no studies using these kinds of methods have been done on small wind-dispersed diaspores.

Release of marked diaspores is an approach that is somewhere in between the Langrangian and the Eulerian approach. But as diaspores rarely are marked individually and the trajectory from

release to catch is not observed these methods should be categorised as Eulerian methods. Studies of insect dispersal of pollen have used coloured powder. Other studies have used artificial propagules to mimic dispersal of e.g. seeds in rivers (Andersson et al. 2000).

Eulerian methods – trapping Here, the information of the diaspores' whereabouts between release and capture is lacking. Since only a small proportion of the surface is sampled, the diaspore source needs to be very strong to detect LDD (Nathan et al. 2003).

Many authors have studied the deposition of spores around a central colony using microscope slides with some sticky substance such as melted petroleum jelly. Stoneburner et al. (1992) studied the deposited spores of two colonies of the acrocarpous moss Atrichum angustatum up to 15 m. The traps at 1.5 m right above the colony did not catch any spores but those at the other distances (0.5, 1.5, 2.5 and 15 metres) caught spores at both 0.5, 1 and 1.5 metres height. Söderström & Jonsson (1989) studied the spore deposition around one colony of the leafy liverwort Ptilidium pulcherrimum in 7 distance intervals at 49 collection points up to 10 m from one colony. They concluded that 43 % of the spores were deposited within 2.5 m from the colony. Sundberg (2005) studied the dispersal of six Sphagnum species, which have an active release, up to 3.2 m from a central colony and found that 8 to 32 % of the spores which were dispersed outside the colony did not travel farther than 3.2 m. Miles & Longton (1990) trapped spores from the acrocarpous mosses Atrichum undulatum and Bryum argenteum up to 2 m from a colony and estimated that 7.2 % to 12.7 % and 2.2 to 4.5 % of the dispersed spores were deposited within 2 m from the colony. In contrast 70 % of the spores were estimated to be deposited within 2 m of a colony of 46 sporophytes of the moss Tortula truncata (Roads & Longton 2003). Pohjamo et al. (2006) compared the dispersal of spores of equal size and gemmae (diameter = 9–12 μm) of the liverwort Anastrophyllum hellerianum. They concluded that between 17.5 and 43.1 % of the spores released each day and between 0.64 and 4.8 % of the gemmae available were deposited within 10 m from the central colonies. The percentages for spores were calculated of the released spores, whereas the percentages for gemmae were calculated of the total of available gemmae and included also gemmae that remained attached to the shoots after the study period. Since the ratios were calculated in different ways they cannot

be compared directly. Rain did not affect the dispersal pattern significantly. More gemmae were however released during rainy days.

The problem with many small wind-dispersed diaspores is that they are difficult to recognize and determine to species level. One way is to remove all possible spore sources within a certain radius or study realized dispersal where the spores have germinated and become easier to identify. Kallio (1970) used petridishes with agar and wood discs up to 200 m from a spore source to study the spore dispersal of the root-rot fungus Heterobasidion annosum. He exposed agar plates up to 2 minutes and the wood discs up to 2 hours. Under the colony and at 1 m the petridishes were exposed for 5-10 seconds. The deposition were here estimated to at least 200,000 spores/dm2/hour and 30,000 spores/dm2/hour. The deposition at 50, 100 and 200 m were similar and varied from 0 to 49 spores/dm2/hour calculated from an exposure time of 1-2 minutes. Mycologists can also study a sort of realized dispersal using traps with monokaryotic mycelia and check if they have been dikaryonized by looking for clamp connections or other morphological changes in the mycelia after an incubation time in a laboratory. There strains are selfincompatible, so the arriving spore must be of a different mating type in order for a dikaryotic mycelium to develop (Edman & Gustafsson 2003). The monokaryotic mycelia have been cultivated on nutrient agar (Adams et al. 1984; Williams et al. 1984) but Edman & Gustafsson (2003) cultivated monokaryotic mycelia of some polypores on wood-discs instead.

Norden & Larsson (2000) studied dispersal of the wood-inhabiting polypore Phlebia centrifuga using single spore mycelia on agar and obtained dicaryonized mycelia up to 100 m using ten fruit bodies as a source in a circle where all the fruitbodies within 200 m from the center had been removed. In a second experiment they trapped spores at 0–350 m and at 500–800 m from the limit of a nature reserve with old-growth forest with a more diffuse spore source. In this experiment they detected spore deposition on 15 of 60 in the first distance and on 4 of 59 in the second distance.

Hallenberg & Kuffer (2001) also used petri dishes with single spore mycelium to trap spores from eight wood-inhabiting basidiomycetes. They were exposed on a roof in Gothenburg for 24 h six times during October and November. They detected spores from those species that were

common in the vicinity as well as the species that had the nearest known site 1000 km to the south as well as to the east.

One possibility to be sure that the trapped diaspores originate from the mother colony is to apply 15N isotopes to the mother plants during the flowering stage so the seed will also have higher content of this isotope than other plants. Carlo et al. (2009) applied three urea doses to plants of Solanum americanum and Capsicum annuum and concluded that it was possible to detect this enrichment even in seedlings. Since many spores are very small compared to the stages after germination and that at least many bryophytes live in nutrient poor environment it still remains to be tested if this method is applicable for studies on spore dispersal.

Another method for tracing the origin of diaspores is to use genetic markers. By analysing the pericarp, which is inherited maternally, it is possible to determine from which of the sampled mother plants the diaspore originates or if it has dispersed from some unsampled plant outside the study area. This is feasible for large seeds like acorns that Grivet et al. (2005) studied with microsatellites and found that the dispersal distance was not more than 100 m. However, for very small seeds and spores this method is not applicable. Instead one could sample all possible parents, both males and females, as well as seeds and/or seedlings in an area or population. As this will lead to extensive sampling only small areas/populations can be investigated with this approach. The "Two-Gener" method includes collecting seeds from the mother plant and by analysing pollen genetic structure estimate the average pollen dispersal distance by sampling possible father plants in the vicinity (Broquet & Petit 2009). Parentage analysis has also been used to study pollen dispersal in a similar way. Oddou-Muratorio et al. (2010) used microsatellites to investigate dispersal of seeds and pollen in Fagus sylvatica and F. crenata by estimating the historical and recent gene flow.

Indirect methods Genetic similarity between populations can be used as a measure of the connectivity between populations and assess historic dispersal. The easiest way is if the different genotypes could be distinguished with the naked eye. An elegant way to study realized pollen dispersal was used by

Bannert & Stamp (2007) who used differently coloured maize to detect pollen dispersal between fields. In a valley in Switzerland they planted one field with yellow maize and at several distances (50–4500 m) from this field they planted white maize. Cross-pollination, which could be detected easily by yellow kernels, was detected at 50–371 m in the main wind direction.

However, one is rarely fortunate enough to have such traits available. Neutral genetic markers are an increasingly used tool in the study of dispersal in recent decades. The price, the amount of information generated, the ability to detect heterozygotes (codominance) and the specificity (and hence the risk of contamination) are some factors to take into account when choosing the method.

Enzymes with the same function can be separated on gels with an electric current due to their different size and charges. Isozymes are enzymes with the same function coded by different loci whereas allozymes are variant coded by different alleles in the same loci. Isozymes/allozymes is a rather cheap method where you separate different variations of an enzyme (allozymes) on a gel.

The intercontinental genetic structure of the basidiomycete Schizophyllum commune was investigated by James et al. (1999) using sample strains from North America, Central America as well as from South America, Asia, Africa, Europe and Australasia. Since there was a higher genetic variation within than between intercontinental populations they concluded that LDD could be efficient enough in this species to secure a gene flow even over large distances.

Grundmann et al. (2007) studied the moss Pleurochate squarrosa in the Mediterranean area using both allozymes markers and DNA sequence data. The data from allozymes showed no isolation by distance but the sequence data did.

Thirty-two populations from Asia, America and Europe of the copper-moss Scopelia cataractae were investigated for 15 allozymes loci. It was concluded that the species was native to America and Asia and that LDD has been important for the species. (Shaw 1995)

Different types of PCR-based fingerprinting methods have become more used recently. They can generate more information than alloenzymes. Some are not codominant like RAPD (Random Amplified Polymorphic DNA), AFLP (Amplified Fragment Length Polymorphism). RFLP

(Restriction Fragment Length Polymorphism) is often codominant. Restriction enzymes cut the DNA at certain sequences. The fragments of different lengths are separated on a gel.

Microsatellites (ISSR – Inter Simple Sequence Repeat) are codominant. In opposition to the methods mentioned above microsatellites can reveal the relationship to other alleles (Silvertown & Charlesworth 2001). SNP (Single Nucleotide Polymorphism) is a novel method that has not been used in so many studies on bryophytes yet.

James & Vilgalys (2001) trapped spores of the common basidiomycete Schizophyllum commune using haploid mycelia on agar in petri dishes exposed for 12 hours in five out of seven sites from northern South America through the Caribbean to southeastern USA and calculated from this a deposition of 18 spores/m2/hour. The samples were taken in areas where no fruit bodies were expected to occur in the closest vicinity (non-forested areas) so the result should describe the background deposition. They analysed five loci of the dikaryotic mycelia with RFLP. Dispersal over the Caribbean Sea could not be showed unambiguously. However, they showed in one locus a possible pattern that could be interpreted such that gene flow had occurred from the south to the north (which was the prevailing wind direction) but not the other way around.

Snäll et al. (2004) studied the genetic structure of Orthotrichum speciosum and O. obtusifolium in a forest landscape in Finland using AFLP. They concluded that both species were limited by dispersal beyond 300-350 m.

Szövényi et al. (2008) investigated the genetic structure for six peatmosses with amphi-Atlantic distribution using microsatellites and concluded that both migration and the polymorphism of the founders can explain the genetic structure of the intercontinental populations. The moss Polytrichastrum formosum showed a low genetic differention ( showed both with allozymes and microsatellites) between three populations in Denmark and three in the Netherlands approximately 450 km apart and Van der Velde et al. (2001) concluded that this was due to spore dispersal.

Other genetic methods can be used to study dispersal over longer time spans. For phylogenetic studies and immigration history of a species in different areas, sequencing of certain parts of the genome has been used, e.g. ITS (Internal Transcribed Spacer) a non-coding RNA part of the

Ribosome DNA. Huttunen et al. (2008) studied Homalothecium and used a substitution rate of 0.8–2.0 %/106 year and a mean of 0.014 substitutions/site/106 year based on (Bakker et al. 1995) for green algae and higher plants. Moncalvo & Buchanan (2008) studied the basidomycete Ganoderma applanatum-australe species complex and refers to a substitution rate of fungi of 1.26 % /108 year and concludes that there is a occasional gene flow due to LDD in the southern hemisphere after the separation of Godwanaland in this species.

Biogeographical studies Dispersal and vicariance are two factors that have been used to explain species distributions. The number of endemic taxa is lower in ferns (34%) compared with angiosperms (80 %), which can be explained by: 1. that many fern taxa are older. 2. speciation rate is lower for ferns 3. ferns are better dispersers (Smith 1972 in Wolf et al. 2001). This can be said of many other organism groups with small diaspores. Factors that could be contributing to the opinion that all micro- organisms are omnipresent, are that distribution data is incomplete for many species and that many rare species are still to be described. Some flagship species have restricted distribution, and even if many species have drought resistant diaspores, such as cysts, others have more sensitive diaspores. The fraction of endemic micro-organisms has been assumed to be 30 %. (Foissner 2006)

A comparison of the composition of floras among continents or islands can be used as an indirect way of detecting dispersal and connectivity between land areas. For example, Munoz et al. (2004) showed a close correlation between the predominant wind direction in the summer and the composition of bryophyte flora in the southern hemisphere. Zanten & Pócs (1981) compared the composition of bryophytes of the southern hemisphere. The sensitivity of the spores to drought and freezing was investigated in several species. They concluded that the endemic or geographically restricted species had spores with lower longevity than those with a wider distribution. Species that are endemic but have long-lived spores may have been overlooked and may in fact occur in other continents than hitherto known.

Other studies Smaller scale patterns can be used for interpreting shorter time scale processes. Miller & McDaniel (2004) studied the moss flora on calcareous mortar along a highway in a landscape with only acidic substrata. During the 65 years since the construction of the highway a number of calcicolous bryophytes that did not occur in the vicinity earlier had colonised the calcareous substrate and many species had dispersed 5 km or more during this time span.

Hutsemekers et al. (2008) compared the bryophyte species on slag heaps of different ages (aged by dendrochronology of rooted trees) with the nearest 4x4 km grid cell with occurrence of the species according to a bryophyte atlas of Belgium. They concluded that the area of the patch and time available for colonization were important for the number of species and that 56 % of the species emanated from a source located 6-86 km during the last 50 years.

The two mosses Campylopus introflexus and Orthodontium lineare were accidently introduced to Europe from the southern hemisphere. By documenting the first finding of the species in provinces across Europe it is possible to get a approximate estimation of how fast the species disperse across the continent (Hassel & Söderström 2005).

Lichen species were inventoried on 94 gravestones in five counties in England, and classified according to which 20 year period they were raised (1650 to 1980). Abundance (=average ratio of gravestones with the species for all periods that it occurred), area of occupancy (=number of squares in Great Britain), spore size and colonization ability (=e.g. the most recent period with an occupied stone) were noted for 92 saxicolous species. Area of occupancy was positively correlated with both abundance and colonization ability, while spore size was not correlated to any of the parameters. (Leger & Forister 2009)

By studying the distribution of trees and the occurrences of the two epiphytic mosses Orthotrichum speciosum and Orthotrichum obtusifolium in a forest area, Snäll et al. (2003) found that the occurrences of the spore dispersed O. speciosum was influenced by connectivity, while the gemmiferous O. obtusifolium was not. They also predicted that 17 % of the colonizations of O. speciosum occurred farther away than 15 m (Snäll et al. 2003). Hedenås et al. (2003) noted that the sexually dispersed epiphytes Collema curtisporum and Orthotrichum

speciosum were more aggregated than their host trees Populus tremula while three asexually dispersed species C. furfuraceum, Leptogium saturninum and O.obtusifolium were not.

Models Phenomenological models try to fit the best model disregarding other measurements than distance, while mechanistic models try to find the best model from measured parameters like wind speed and abscission height. There are also intermediate models which e.g. Snäll et al. (2007) have proposed.

When comparing functions from different studies it is important to be aware of that several different functions are used. In response to the confused use of dispersal curves and dispersal kernels, Cousens et al. (2008) used probability density function (pdf) as a general term and recognized three functions (distance pdf: f(r), density vs distance relationship: ωθ(r) and density pdf: g(r). A function of one type of distribution should not be compared to any of the others unless they have been transformed. The function that describes the probability of single diaspore to arrive at a certain distance is called the "distance pdf". Taking samples in form of e.g. traps will generate a density vs distance relationship. The probability density function for a diaspore landing in an infinitely small area at distance r from the origin is called the "density pdf". Power, negative exponential, Weibull, half normal, half student t and Cauchy have been used to describe density vs distance relationship. A possibility, especially to describe fat-tailed curves, is to use a mixed model, i.e. combining two functions. (Cousens et al. 2008)

Phenomenological models Fitt et al. (1987) compared 325 data sets with deposition of pollen, micro-organisms and spores. Power law and exponential models were fitted to these. The fit was similar for both models in most cases. However, fungal spores (<10 μm) fitted better with the power law function and droplets with exponential. A curve should not be extrapolated beyond the available field data.

Bullock & Clarke (2000) fitted negative exponential and inverse power models to a data set of seed dispersal of Calluna vulgaris and Erica cinerea up to 80 m from the source. Even if the inverse power fitted the data better none of the models estimated the tail very well. A mixed model was used to get a better fit in the entire span of the function.

Mechanistic models Different functions and parameters have been used. Dispersal models often include properties of the diaspore such as terminal velocity, as well as meteorological and landscape properties such as wind speed. Tackenberg (2003) found that the thermal updrafts and other turbulence had a large influence on the rate of LDD. The question is what is most important in LDD: extreme windy conditions during hurricanes and tempests or warm conditions with convection. Horn et al. (2001) also emphasised the effect of updrafts on winged seeds and even if some diaspores of a certain species fall faster than others every diaspore can be caught in an updraft and contribute to LDD.

One important factor is the weather conditions. The laminar layer during daytime in roughweather is less than a millimeter whereas it during calm weather at night is much thicker. Spores released at midday have a better chance of being transported far away. Conditions of low humidity tend to be correlated with turbulence. (Ingold 1974)

The Gaussian plume model (GPM) has been used for estimating concentrations of gases and particles up to 10 km from a point source. Spijkerboer et al. (2002) calibrated the model with the weighted least-squares method. They estimated the escape fraction outside the canopy to 64 +- 17% from a experiment where spores of Lycopodium clavatum were released and trapped with 35 samplers up to 100 m in a potato field. Katul et al. (2005) used a mechanistic analytical model which has an asymptotic power law tail with an exponent of -3/2 and tested it on datasets on seeds from trees, shrubs and herbs.

Conclusions

Many species with small diaspores produce a large number of diaspores which can constitute a strong source for LDD even if only a small proportion of the diaspores is transported far away from the mother plant. The studies that have been performed give somewhat contradictory answers how effective these species are as long-distance dispersers. On which temporal and spatial scale that species are dispersal limited needs further investigation.

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