Biogeography of mosses and allies. Does size matter?

11 Biogeography of mosses and allies: does size matter? Nagore G. Medina , Isabel Draper and Francisco Lara Departamento de Biología (Botánica), Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain 11.1 Introduction Bryophytes are the second largest group of embryophytes, or green land plants, after the very diverse Angiosperms. hey comprise three main lineages (Frey, 2009; Goi net and Shaw, 2009): mosses (Division or Phylum Bryophyta), that are currently estimated to include 12 500–13 000 species; liverworts (Marchantiophyta), that are thought to number 5000 or a few more; and hornworts (Anthocerotophyta), with only 100–150 species. h is adds up to around 18 000 species, although estimates range from 14 000 to 25 000. Bryophytes in general, and especially mosses and liverworts, are highly successful plants. hey display a high level of diversity, are almost universally present in land environments, and play a signiicant role in many terrestrial and freshwater ecosystems (Vanderpoorten and Goi net, 2009). Although often inconspicuous, mosses and liverworts can be found even in the world’s toughest environments, such as freezing and hot deserts. Moreover, in some harsh environments, such as Biogeography of Microscopic Organisms: Is Everything Small Everywhere?, ed. Diego Fontaneto. Published by Cambridge University Press. © The Systematics Association 2011. 210 BIOGEOGR A PHY OF MICROSCOPIC ORG ANISMS the epiphytic stratum of temperate woodlands or the terrestrial ecosystems of the tundra, they are the chief group of organisms, together with lichens. Peatlands, which cover c. 3% of the Earth’s land surface (Limpens et al., 2008), are a particular and outstanding case of habitat where bryophytes generally prevail, commonly with species of Sphagnum as the dominant vegetation element. Even if bryophytes are particularly diverse and luxuriant in tropical montane cloud forests and in humid temperate woodlands, they can be found more or less abundantly in all environments where land plants can survive (Gignac, 2001). Furthermore, in global terms, bryophytes contribute to a signiicant proportion of the production and biomass in a variety of ecosystems (Vanderpoorten and Goi net, 2009). Mosses and their allies are the smallest green land plants. hey can be minute: some leafy liverworts are almost invisible to the naked eye and the tiniest mosses are less than 2 mm tall. At the opposite end, some hepatics reach 30 cm and several mosses can exceed 70 cm in length. he majority of bryophytes, however, measure between 0.5 and 10 cm. hey are reputed to be, both structurally and physiologically, the ‘simplest’ land plants. Actually, bryophytes exhibit a wide range of structural complexity, although they cannot develop complex supporting or conducting tissues because, unlike vascular plants, bryophytes always lack lignin. he bryophyte life cycle is distinguished from that of all other embryophytes in the predominance of the haploid generation, the gametophyte being the photosynthetic phase. Compared with tracheophytes (vascular plants, including ferns and allies, conifers and angiosperms), the gametophyte of bryophytes is therefore very complex. On the other hand, the diploid phase of bryophytes consists of a single sporangium on an unbranched lealess stalk, attached to the gametophyte and nutritionally depending on it. he sporophyte generation of bryophytes is thus the least complicated among the land plants. Bryophytes lack mechanisms and structural systems that allow an efective control of water relations. hey are therefore poikilohydrous, a trait shared with algae and lichens, but uncommon among pteridophytes and angiosperms (Pugnaire and Valladares, 2007). h is characteristic could be interpreted in terms of physiological simplicity, but is actually an alternative and successful life strategy since bryophytes combine poikilohydry with another essential feature: the capacity of maintaining latent life (quiescence) after desiccation, with a high faculty of reviviscence without damage after rehydration (Oliver et al., 2005). In fact, their ability to survive cold and dry conditions is unparalleled in other principal plant groups (Glime, 2007). In the absence of major barriers for gas and water exchange, the hydration state in most bryophytes is dependent on ambient humidity. However, many species have evolved morphological structures or architectural characteristics that modify water uptake and storage rates, and that limit water loss from shoot surfaces. As a consequence, species of bryophytes difer greatly in their evaporative exchange properties (Rice et al., 2001). Since desiccation tolerance and other BIOGEOGR A PHY OF MOSSES AND ALLIES ecophysiological traits also vary among bryophytes (Proctor, 2009), diferent species exhibit a broad range of physiological optima and ecological amplitudes. Bryophytes, like pteridophytes but unlike lowering plants, propagate by means of sexual spores (meiospores). hese are produced in the capsule (sporangium) of the sporophyte and germinate into a protonema that subsequently produces the gametophores or green plants. Gametophytes can be monoecious and then the processes of fertilisation and consequent generation of new sporophytes have no special diiculties. However, among mosses dioecious species are just as common as monoecious ones, and more so among liverworts; in some cases, sporophytes have never been found in certain populations or even species. Bryophyte spores are quite diverse in size, although in general they are small, usually between 10–20 µm in diameter (Frahm, 2008). Hence, they are potentially adequate for wind dispersal, which is indeed the most common dispersal mechanism, although animal and water dispersal also occur (e.g. Porley and Hodgetts, 2005; Marino et al., 2009). here is a tremendous variation in spore production among bryophytes, the number of spores per capsule being in the interval of 104 to 106 for most species (Vanderpoorten and Goi net, 2009). In addition, mosses and allies propagate through vegetative structures. Asexual propagules can be undiferentiated (fragments of gametophyte structures) or more or less specialised reproductive bodies (brood bodies or gemmae), and have various sizes and shapes. It is suspected that vegetative propagation plays an essential role in the dispersal of bryophytes and it has a chief importance for colony expansion when the plants have already initiated its establishment (Glime, 2007). Many of the characteristics of bryophytes enumerated above (size, way of life, dispersal mechanisms, etc.) suggest that these organisms are excellent candidates for corroborating Baas Becking’s hypothesis of ‘Everything is everywhere’ (Baas Becking, 1934). In fact, traditional thoughts revolve around the assumptions that (1) bryophytes display no major dispersal restrictions because of their minute wind-transported diaspores (spores or vegetative structures for dispersal) and (2) since they are small their distributions are largely depending on the microenvironment rather than on macroclimatic characteristics (cf. Schuster, 1983). In the following, we intend to show to what extent this idea is valid nowadays. We use both a classical approach, based on morphological concepts of taxa, and a phylogeographic approach, based on molecular data. 11.2 The classical approach In classical biogeography the analysis of distribution ranges has been a keystone in the attempts to disentangle the relative importance of the major factors afecting bryophyte distributions. 211 212 BIOGEOGR A PHY OF MICROSCOPIC ORG ANISMS 11.2.1 Wide distribution ranges Bryophytes tend to show wider distribution ranges than lowering plants. Many species have geographic ranges that include more than one continent, and cosmopolitan distributions are said to be relatively frequent (Shaw and Goi net, 2000; Frahm, 2008; Vanderpoorten and Goi net, 2009). At the family and generic level, worldwide distributions are more or less the rule. hus, more than 75% of the families of bryophytes are widespread in both hemispheres (Tan and Pócs, 2000). However, at the species level, extremely wide distributions are not as common as could be expected. here are no accurate data on how many cosmopolitan bryophyte species there are in total, but based on regional Holarctic bryoloras we can get some insights. Among European liverworts and hornworts the level of cosmopolitan species ranges from 3.1% (Frey et al., 2006) to 5.1% (Dierssen, 2001), for a lora of 453 species (Grolle and Long, 2000). For mosses, following the broad criterion of Dierssen (2001), 93 European species are considered to be cosmopolitan, which represents 7.2% of the 1292 species known from this continent (Hill et al., 2006). Finally, in eastern North America, Crum and Anderson (1981) considered only ive mosses out of 765 to be cosmopolitan. Although the number of cosmopolitan species depends on the dei nition of the concept (the data on European mosses include several species regarded as cosmopolitan that are not considered so in the lora of eastern North America), the rates obtained are not very high in any case. Considering that the provided data were gathered from two well-known continents, it can be assumed that most of the world’s cosmopolitan bryophytes are included. If this is true, the global percentage of cosmopolitan bryophytes might be far below 1%. he idea that very wide distributions are rare is supported by the fact that most bryophyte species are limited to certain regions, even if their ranges are usually larger than the ones found among other terrestrial plants. he question is whether these distributions are restricted because of environmental factors or if there are other meaningful biogeographic constraints. To illustrate what we mean, let us look at the European species with ai nities for a Mediterranean climate. If we assume that bryophytes are wide-ranging plants in which transcontinental dispersal is common, it should be expected that species with marked Mediterranean ai nity in Europe occur in other parts of the world with a similar climate type. In an unpublished study of the European species with a Mediterranean ai nity we found that 62 out of 117 (61.5%) species are restricted to the Palaearctic. Of the remaining species, 23 (19.7%) are also present in California, 11 (9.4%) are recorded in South Africa, seven (6.0%) occur in Chile, four (3.4%) are present in Australia, and only one species is present in all Mediterranean climate zones. Interestingly, many of the species from the Mediterranean basin have not established successful populations in other continents, even if they produce high quantities of small BIOGEOGR A PHY OF MOSSES AND ALLIES spores (down to less than 18 μm), as is the case for Orthotrichum philibertii or Anomobryum lusitanicum. Despite their apparently having the means for spreading over long distances, a high percentage of the bryophytes show distributions with strong geographic constraints. Wide distribution patterns can arise from diferent mechanisms, such as stepping-stone or long-distance dispersal. Stepping-stone dispersal is a result of numerous efective short-distance dispersal events and therefore requires connections (present or past) between landmasses for range expansion and possibly implies long periods of time to attain wide ranges. Consequently, some of the ranges discussed above, including the Mediterranean–South American disjunctions are diicult to explain solely by the stepping-stone mechanism. If longdistance dispersal is responsible for wide species ranges, dispersal could have occurred in recent times, after the separation of landmasses. h is requires that species produce small spores and have access to adequate dispersal agents (e.g. air currents). Whereas the transport of spores to the new locality is necessary this is not suicient for colonisation: spore survival, establishment and persistence are also essential. hus, for the Mediterranean species it appears that several biological or ecological features can prevent species from efective dispersal (including both transport and establishment) across long distances. 11.2.2 Endemic ranges As we have seen, many bryophytes have geographically limited but relatively large distribution areas. here are also endemic bryophytes with very restricted distributions (narrow endemisms); among many others, good examples are Vandiemenia ratkowskiana, a liverwort endemic to Tasmania and only known from two localities that are separated by c. 70 km (Furuki and Dalton, 2008), or Renauldia lycopodioides, a moss known from a few localities in Tanzania and Kenya (O’Shea, 2006). Nonetheless, bryophytes show low levels of endemism in most regions. Low incidence of endemism is usually understood as an indicator of the relevance of long-distance dispersal. On the other hand, a high percentage of endemism is interpreted as indicative of a high degree of isolation of a given lora, both in time and space, and can be related to the prevalence of shortdistance dispersal in most of the included species. Due to the high dispersal capacity of many species, a large number of bryophytes could potentially maintain the genetic connectivity between populations, even if they grow in localities that are several thousand kilometres apart. Under such a scenario, allopatric speciation should be relatively rare among bryophytes. In agreement with this idea, bryophytes show signiicantly lower rates of endemism than lowering plants. Some islands in the Mediterranean Sea that are known to have nearly 10% endemic vascular plants, such as Corsica and Sardinia, have just one endemic moss (Sotiaux et al., 2009). Other good examples are the Canary Islands, where 213 214 BIOGEOGR A PHY OF MICROSCOPIC ORG ANISMS Table 11.1. Percentage of endemic bryophytes in selected areas of high endemicity level. Territories Moss Liverwort Source of the data Hawai 29 48 Staples et al., 2004; Staples and Imada, 2006 New Caledonia 50 48 Morat, 1993 New Zealand 23 50 Fife, 1995; Engel and Glenny, 2008 Madagascar 39 ? O’Shea, 2006 Andean mountain range 31 ? Churchill, 2009 more than 21% of the vascular plants are endemic (Machado, 2002) compared with only 1.4% of the mosses (González-Mancebo et al., 2008). In the Iberian Peninsula the rate of vascular plants endemism exceeds 25% (Sáinz Ollero and Moreno Saiz, 2002), but less than 1% of the bryophyte species are endemic. In the Galapagos Islands only 15 liverworts and six mosses are ‘proven’ endemics (Porley and Hodgetts, 2005). Even if the rate of endemism among bryophytes is lower than that found in larger organisms, there are however many cases around the world where the rates of endemism indicate isolation of the loras. Typical examples are those areas that exhibit the world’s highest endemism rates for vascular plants (exceeding 70%) and that also present corresponding rates of liverwort and moss endemism, ranging from 23% to 50% (Table 11.1). From such data we can infer that biogeographic barriers can have diferent signiicance for bryophytes and lowering plants. Short sea distances, such as the ones that separate the Mediterranean islands from the continent, or mountain ranges comparable to the Pyrenees, appear not to represent true barriers for bryophyte dispersal, whereas they are obviously limiting the distributions of a number of lowering plants. However, this does not mean that there are no obstacles at all to bryophyte dissemination and there are many examples that indicate the existence of barriers (not always physical). hus, the ecologically isolated Andean region has a signiicant level of bryophyte endemism, while New Zealand, New Caledonia and Hawaii are equally unique in this respect as a consequence of their strong geographic isolation. Several species are potentially capable of maintaining transcontinental connectivity between populations through long-distance dispersal, which could prevent population diferentiation even in remote islands, but it is clear that there are a number of cases in which isolation and allopatric speciation occur. How important then is long-distance dispersal in relation to endemism? Surprisingly, only one of the eight endemic mosses of the British Isles produces BIOGEOGR A PHY OF MOSSES AND ALLIES Fig 11.1 he epiphytic moss Orthotrichum handiense growing on the branches of Asteriscus sericeus. sporophytes (Smith, 2004; Porley and Hodgetts, 2005), which indicates the relevance of the lack of sexual reproduction and spore production for maintaining isolation. Although seemingly remarkable, the case above is relatively untypical and many endemic species do indeed produce sporophytes and high quantities of small spores and could potentially connect even distant populations. For example, Orthotrichum handiense is a moss restricted to a small area on Fuerteventura (Canary Islands) and represents an outstanding example of local endemism (Figs 11.1, 11.2) because it has a population that is relatively rich in individuals and a high production of sporophytes (Lara et al., 2003). h is shows that when evaluating the relevance of dispersal capacity and connectivity among populations, not only lack of spore production, but also many other factors can hamper the efectiveness of dispersal, such as accessibility to transport means, survival and establishment success. In a set of experiments on spore viability in New Zealand mosses, spores of endemic species were found to have low survival rates after desiccation, freezing and UV exposure (van 215 216 BIOGEOGR A PHY OF MICROSCOPIC ORG ANISMS Fig 11.2 Location (star) of the known population of O. handiense. Zanten and Pócs, 1981; van Zanten and Gradstein, 1988), pointing out the paramount importance of spore endurance to survive the harsh conditions during long-distance dispersal. Equally critical but less explored is the establishment phase. It is thought that establishment of new shoots from spores germinating under natural conditions depends on a complex set of factors and may occur only rarely (e.g. Boatman and Lark, 1971; Miles and Longton, 1990; but see discussion in Sundberg and Rydin, 2002). Another unknown factor is how easily diaspores can access the agents of dispersal, which might be especially relevant for the isolation in small organisms that are found in speciic microenvironments. Some bryophyte species occupy sheltered microhabitats where wind transport is very unlikely. A good example of this is the so-called ‘rockhouses’, in the Southern Appalachian Mountains (USA). hese are deep narrow gorges that harbour a remarkably isolated bryolora with several endemic mosses and a relatively high number of species that have their closest relatives in the tropics (Billings and Anderson, 1966; Farrar, 1998). he greatest concentration of endemism occurs near waterfalls and in sheltered microenvironments where conditions are stable and spore dissemination by wind may be prevented by the surface tension of water in a permanently wet environment. he result is a humid and mild refugium for certain bryophytes, isolated from major air currents. BIOGEOGR A PHY OF MOSSES AND ALLIES 11.2.3 Disjunct ranges Up to here, we have looked at insights provided by analyses of continuous ranges. However, perhaps more than wide ranges and rates of endemism, the paradigmatic examples that summarise the controversy on the relative importance of the main processes determining species geographic ranges are the disjunctions. Discontinuous distribution ranges can be interpreted either as the result of fragmentation of ancient continuous distributions or as consequences of long-range dispersals. Supporting the hypothesis of relict ranges is the fact that most bryophyte disjunct distributions are highly congruent with the continental drift hypothesis (Schoield and Crum, 1972; Schuster, 1983). Indeed, the bryophyte disjunctions parallel those found in spermatophytes, which suggests that the historic events that shaped species distribution for lowering plants are also relevant for bryophytes. Schoield (1988) analysed the disjunctions between Europe and North America and concluded that the western North American–western European bryophyte disjunctions have a relict origin. He based his conclusion on inferences made from the biological and ecological characteristics of the disjunct species. h is kind of analysis gives indirect but consistent results regarding the importance of past geologic and climatic events in causing the observed disjunct patterns. If we accept the relict origin of the disjunctions we have to assume that some species have remained unchanged (at least morphologically) for very long periods of time. At the population level there is evidence for the ability of bryophytes for long-term survival. For example, the perennial species Anastrophyllum saxicola is known for producing extensive populations of clones that likely survived a minimum of 2000 years (Longton and Schuster, 1983). h is could indicate that some species are capable of persisting, even under suboptimal conditions, as living fossils (Hallingbäck, 2002). It is unknown how common these rates of survival are and, in any case, to assume species stability at a geologic time scale is a very diferent matter. Although records of old fossils are scarce within bryophytes, there are a few remarkable examples of morphological stability, and at least some species have remained unchanged for more than 45 million years (cf. Taylor et al., 2009). However, to provide evidence for the African–Tropical American or Pangaea n distributions, species need to remain without apparent changes for more than 100 and 180 millions of years respectively. Certain intriguing disjunct distributions that are diicult to interpret under a historic and geologic perspective provide support for the long-distance dispersal hypothesis. Perhaps the best examples are the bipolar disjunctions, distributions that include boreal or temperate regions in both hemispheres but with an absence from the landmasses in between. here are 18 bryophytes species in Antarctica that are known to have this type of distribution (Ochyra et al., 2008). In most cases, species with bipolar disjunctions have a predominantly Holarctic distribution and 217 218 BIOGEOGR A PHY OF MICROSCOPIC ORG ANISMS a few isolated populations in the southern hemisphere and therefore they probably originated by long-distance dispersal from source populations in the northern hemisphere (Ochyra and Buck, 2003). In spite of their support for the long-distance dispersal hypothesis, erratic and unconnected distributions such as bipolar disjunctions are infrequent among bryophytes. Most species show geographic ranges that are congruent with general loristic patterns and therefore diferent biogeographic units (kingdoms, subkingdoms, regions etc.) can be recognised (e.g. Schoield, 1992). he general patterns of vascular plants and bryophytes are analogous, suggesting that the historical and biological mechanisms shaping the species distributions are similar in both groups (Schoield, 1992). Because of the low likelihood of a repetition of a unidirectional stochastic event, it has been argued that the concordant bryoloras are a proof of the lack of importance of neutral long-dispersal events in shaping species distributions (Schuster, 1983). However, it has been increasingly understood that wind dispersal is not just a stochastic neutral process. On the contrary, intercontinental dispersal events by wind are considered part of a directional, congruent and consistent process which could give rise to patterns of concordant loras (McDowall, 2004; Muñoz et al., 2004; Cook and Crisp, 2005), especially in groups of high dispersal potential such as bryophytes. Despite the latter, the similarity across loristic realms presents a picture highly concordant with historic connectivity and appears diicult to explain solely by wind connectivity. For example, Pócs (1998) analysed the phytogeographic ai nities of the bryophyte lora of the Arc Mountains in eastern Africa showing how the old crystalline mountains of this cordillera host a signiicantly higher number of Lemurian (Madagascan) elements, than the neighbouring younger mountains do. Furthermore, even if nowadays the Eastern Arch is not the closest area to Madagascar, it contains the highest number of Lemurian bryophytes in continental Africa. h is strongly relects ancient links between Eastern Africa and Madagascar, two dissected parts of Gondwanaland. 11.2.4 Diversity patterns As we have seen, bryophytes show a wide variety of distribution patterns, from very extensive to very narrow ranges, including both continuous and disjunct distributions. Bryophyte distributions frequently parallel those of lowering plants, which suggests that both groups were inluenced by the same factors. However, a detailed analysis of their distribution patterns shows important discrepancies which could have resulted from the fact that bryophytes are smaller than vascular plants, that they have a more ancient origin, and/or that they have diferent modes of dispersal. In some respects these diferences make bryophytes more similar to other small-sized organisms with passive wind dispersal. We will now focus on bryophyte diversity patterns to explore whether these are shared with vascular plants or with microorganisms. BIOGEOGR A PHY OF MOSSES AND ALLIES he latitudinal gradient of species richness has traditionally been thought to be one of the few general rules in biogeography (Hawkins et al., 2003). he decrease in species richness towards the poles is consistent across a wide variety of organisms with high levels of organisation. h is latitudinal gradient is lacking in some microorganisms, which has raised doubts about the generality of the pattern. For bryophytes it has repeatedly been stated that the tropics harbour the richest bryoloras of the world (e.g. Argent, 1979; Frahm et al., 2003). However, recently published global maps of moss (Mutke and Barthlott, 2005) and liverwort (von Konrat et al., 2008) species richness do not show unambiguous evidence of such a latitudinal gradient. Tropical regions in South America are consistently richer in moss species than regions at higher latitudes. his pattern is not so clear in liverworts, and some countries of tropical Africa show remarkably low species richness for both mosses and liverworts. Furthermore, in a study of moss species richness in the tropical Andes, Churchill (2009) suggested that the global pattern of richness in bryophytes is probably the opposite of that observed in other groups. In his study he argues that the richest areas of the world are the temperate and boreal forests of the northern hemisphere. Although the compilation efort made is huge in both the studies of Mutke and Barthlott (2005) and von Konrat et al. (2008), it is important to note that the information on bryophytes species richness is far from complete, and some of the observed patterns may be lawed by knowledge gaps and uneven sampling eforts, as already noted by the authors. A good example of this is that many tropical African countries, such as Guinea Bissau and he Gambia, still have just one species recorded (O’Shea, 2006). In addition, both Mutke and Barthlott (2005) and von Konrat et al. (2008) based their overviews on geopolitical units (countries and states), which clearly oversimpliies the species richness patterns and can produce misleading results (Mutke and Barthlott, 2005). h is problem of too coarse units, as well as the bias caused by gaps in knowledge, could also have inluenced the conclusions by Shaw et al. (2005). hese authors published one of the few attempts of statistically quantifying the latitudinal gradient in mosses, and failed to show a strong relationship between species richness and latitude. Despite the lack of a general unambiguous pattern in liverworts, the Lejeunaceae, one of the largest liverwort families, is clearly most speciose in the tropical regions of the world (von Konrat et al., 2008). An analysis of beta diversity of pleurocarpous mosses showed a higher species turnover in the tropics than in temperate and boreal regions, indicating the existence of a latitudinal gradient of moss diversity (Hedenäs, 2007). In addition, the hot spots proposed by Tan and Pócs (2000) are generally found in the same areas that are traditionally considered to have a high diversity for vascular plants. At present we must therefore conclude that it is not yet possible to infer whether bryophytes really lack a latitudinal diversity gradient or if such suggestions are due to incomplete data at the global scale. 219 220 BIOGEOGR A PHY OF MICROSCOPIC ORG ANISMS he diferences in diversity patterns among taxonomic groups can also be addressed in terms of species–area relationships. Species–area curves are one of the most frequently cited correlations in geographic ecology. With some exceptions (e.g. Kimmerer and Driscoll, 2000) bryophytes show a strong relationship between area size and species richness (Tangney et al., 1990; Ingerpuu et al., 2001; Nakanishi, 2001; Virtanen and Oksanen, 2007). However, the slope of the curve is supposedly less steep in bryophytes than in vascular plants and other large organisms (Ingerpuu et al., 2001; Peintinger et al., 2003). Bryophytes therefore seem to occupy an intermediate position between microorganisms, for which a species–area relationship is rarely found (Fenchel and Finlay, 2004), and large organisms, where the slope is steeper. hese results support the hypothesis that less steep species–area slopes are found in small organisms (Drakare et al., 2006) and suggest that the greater dispersal abilities of the latter (Mouquet and Loreau, 2002; Hovestadt and Poethke, 2005) lead to lower species turnover and thus to more similar communities across regions. In agreement with this, Hillebrand et al. (2001) found that the decay in community similarity with distance is slower for small than large organisms, which corroborates the importance of dispersal ability in small organisms in shaping communities. Bryophytes do not completely fuli l the expectations regarding this tendency. For example, a meta-community analysis by Löbel et al. (2006) showed a strong spatial aggregation in bryophytes and, more signiicantly, a study of spatial structure in communities of mosses and other taxonomic groups demonstrated that the distance decay in similarity for bryophytes was comparable to that in wind-dispersed vascular plants (Nekola and White, 1999). Although these results are not conclusive, other works that do not directly address the structure of communities have also highlighted the aggregated distribution of bryophytes (Hedenäs et al., 1989; Söderström and Jonsson, 1989; Kuusinen and Penttinen, 1999). h is kind of pattern suggests the existence of similar processes shaping communities of vascular plants (where spatial aggregation is a well-known pattern) and bryophytes. 11.3 The phylogeographic approach In bryology, as in other ields of biology, the use of molecular techniques has become increasingly common during the last 20 years. hese techniques have especially been applied in phylogenetic studies, but also in taxonomy and biogeography (cf. Shaw et al., 2002; Vanderpoorten and Goi net, 2009; Heinrichs et al., 2009a). In many cases molecular analyses have coni rmed earlier hypotheses based on morphological data. However, there are also numerous examples where taxonomical units dei ned by molecular similarity are incongruent with BIOGEOGR A PHY OF MOSSES AND ALLIES morphologically dei ned taxa. h is has led both to the recognition of cryptic species and to the synonymisation of taxa, and has re-opened the species concept debate (see e.g. Mishler, 2009 vs. Zander, 2007). In some cases, molecular-based taxonomic units show clear biogeographic patterns that allow more or less uncontroversial interpretations, but there are also studies in which the biogeographic history of clades is diicult to assess. here are even cases where contradictory conclusions can be drawn from similar molecular data sets. Molecular studies have revealed variation not only between, but also within morphologically dei ned bryophyte species (morphospecies). In some cases the molecular variation within morphologically stable species is even larger than among morphologically clearly diferent taxa. h is has led to the recognition of cryptic bryophyte species (see revision in Shaw, 2001, and Heinrichs et al., 2009a). When morphological studies were carried out after the molecular variation was detected, this has sometimes led to the description of new species (e.g. Szweykowski et al., 2005; Hedenäs et al., 2009) or to the re-establishment of previously synonymised taxa (e.g. Rycroft et al., 2004; Cano et al., 2005; Hedenäs, 2008; Oguri et al., 2008; Draper and Hedenäs, 2008, 2009). On the contrary, there are also examples where taxonomically problematic bryophyte morphotypes were impossible to distinguish on the basis of the studied markers. herefore some taxa, both at the infraspeciic and speciic levels, have been synonymised based on molecular evidence. h is has especially happened for endemic taxa that were described mostly on the basis of their isolated occurrences (e.g. Heinrichs et al., 2004a, 2004b; Werner et al., 2009). In spite of all the mentioned taxonomic changes, the number of described bryophyte species remains approximately constant. h is sharply contrasts with the tendency observed in other groups of small organisms, where the introduction of molecular techniques has meant a cut-across classic taxonomy and has multiplied the estimated number of species up to ten times (e.g. Foissner, 1999). he diference between the two categories probably lies in that the number of morphological characters available for species delimitation is much higher in bryophytes than in many other small organisms. Among microorganisms, the DNA information has revealed a vast molecular diversity within relatively few morphologically recognised species that are globally distributed (Spratt et al., 2006). If molecular techniques are useful, although not revolutionary for our understanding of bryophyte taxonomy at the species level, they are more widely used for understanding bryophyte phylogeny and they have, in many cases, revealed unsuspected relationships (cf. Renzaglia et al., 2007). Since phylogenetic relationships relect the evolutionary history, these can also be used to infer dispersal and colonisation histories at various taxonomic levels. As an example, the geographic distributions of haplotypes within morphospecies allow us to infer species origins and/or diversiication areas, as well as their dispersal routes. 221 222 BIOGEOGR A PHY OF MICROSCOPIC ORG ANISMS 11.3.1 Phylogeography of endemics Molecular techniques have a great potential to elucidate the geographic history for both widely and narrowly distributed species, and have often conirmed endemics as distinct taxonomic entities. A nice example of the latter among bryophytes is found in the genus Echinodium (Stech et al., 2008). his genus was earlier thought to comprise six species, four restricted to the Macaronesian archipelago and two to the Australasian and Paciic regions. It has now been demonstrated that this is an artiicial group consisting of an endemic Macaronesian genus (Echinodium s.str., three species), one Macaronesian Isothecium species and two Australasian members possibly in connection with hamnobryum that show convergent morphological evolution. Stech et al. (2008) not only elucidate the taxonomy and phylogeny of this group of species, but they also clarify the biogeography of a vicariance that is otherwise diicult to explain. Studies of molecular variation involving endemic taxa in a phylogenetic framework can also lead to conclusions regarding speciation processes. hus, Vanderpoorten and Long (2006) interpreted the nested position of the Azorean endemic liverwort Leptoscyphus azoricus within populations of the Neotropical L. porphyrius as an example of recent speciation caused by a long-distance dispersal. Similarly, Hedderson and Zander (2007) postulated that the South African endemic moss Triquetrella mxinwana originated during the Pliocene–Pleistocene as a result of long-distance dispersal, on the basis of low molecular divergence levels and a chronology consistent with the existence of the niche where it grows. 11.3.2 Phylogeography of widely distributed taxa Haplotype diversity and molecular variation in species distributed throughout large and more or less continuous areas have been used by several authors to infer possible areas of origin, glacial refugia and migration routes. Hedenäs and Eldenäs (2007) hypothesised that the two cryptic species of Hamatocaulis vernicosus complex occurring in Europe diverged before the last periods of glaciations, based on their occurrence also in America. he species occurring in southern Europe could have survived somewhere in the northern Mediterranean region, from where it re-colonised earlier glaciated or periglacial areas in central and northern Europe. Hedderson and Nowell (2006) deduced that glacial refugia for Homalothecium sericeum occurred both in southern Europe (Balkan and Italian peninsulas) and in the British islands and adjacent mainland, on the basis of the greater haplotype diversity and occurrence of unique haplotypes in these areas. As a i nal example, Hedenäs (2009a) used molecular data and fossil evidence to postulate a late Tertiary origin of ancestral haplotypes of Scorpidium cossonii in cold pockets in a then partly sparsely forest-covered Arctic. Subsequently, haplotypes evolved adaptations to warmer climates and that allowed colonisation of temperate wetlands and also gave rise to the morphospecies S. scorpioides. BIOGEOGR A PHY OF MOSSES AND ALLIES Analyses of molecular variation among populations have also been used to address the origin of disjunct distributions. If disjunctions originated as a consequence of recent or repeated and continuing long-distance dispersal events, we should expect that molecular sequences from separate populations are rather similar. On the other hand, if an original distribution area was fragmented and populations remained isolated for a long period thereafter diferent mutations should have accumulated in the respective areas. In the latter case molecular diferentiation between populations should be relatively higher (e.g. Shaw et al., 2002). In bryophyte studies both fragmentation and long-distance dispersal have been proposed to explain extant species disjunctions. McDaniel and Shaw (2003) analysed the distribution of diferent chloroplast haplotypes of the subantarctic moss Pyrrhobryum mnioides. hey found evidence for recent or ongoing migration across the Tasman Sea but not for intercontinental dispersal between Australasia and South America or along the Andes between Patagonia and the Neotropics. From the degree of molecular diferentiation, they concluded that Australasian and South American populations have been isolated for approximately 80 million years, after the Gondwanan fragmentation. Likewise, Stech and Dohrmann (2004) found a strong geographic structure in haplotype distribution in the widespread moss Campylopus pilifer, which they interpreted as a probable result of divergent evolution of the populations, after the segregation of Gondwana. However, they also assumed long-range dispersal or introduction events to explain anomalous positions of some haplotypes that deviate from the general pattern. As a third example, Heinrichs et al. (2006) suggested that the current distribution of the liverwort family Plagiochilaceae is the result of the breakup of Gondwana, in combination with short-distance and rare long-distance dispersal events. Other studies suggest long-distance dispersal to be the main process to explain disjunct distributions, such as Vanderpoorten et al. (2008), Shaw et al. (2003) and Werner et al. (2003) for several moss species occurring both in North America and Europe, and Shaw et al. (2008) for several taxa in Australasia and South America. For liverworts, long-distance dispersal was proposed to explain especially tropical American–African disjunctions (e.g. Feldberg et al., 2007; Heinrichs et al., 2009b). Most of these cases exhibit a low degree of molecular diferentiation among populations. As mentioned above, this probably relects either recent divergence or repeated and continuing dispersal events. In addition, the molecular dating estimates for some liverworts, such as Marchesinia brachiata, support an Oligocene (that is, post-Gondwanan) divergence (Heinrichs et al., 2009b). Also the biogeography of Herbertus cannot be solely explained by Gondwanan divergence (Feldberg et al., 2007), since extremely low mutation rates would need to be assumed. All these examples except one (cf. Shaw et al., 2003) show some geographic structure in their haplotype distributions, since European, African and American samples are more closely related within than between continents. hus, 223 224 BIOGEOGR A PHY OF MICROSCOPIC ORG ANISMS barriers to gene low must exist at the continental scale and this probably indicates that intercontinental gene low is not necessarily a continuous, repeated and/or currently ongoing process. It can now be concluded that disjunct distributions in bryophytes probably originated from diferent processes, and that it is not possible to infer a general pattern that is valid for all species. In line with the idea that each species has an individual history, it is especially signiicant that the distributions of congeneric species are sometimes explained by diferent processes. Hentschel et al. (2007) found that the extant distribution patterns of the Porella species P. swartziana, P. cordaeana and P. platyphylla, are probably a result of long-distance dispersal events. On the other hand, Freitas and Brehm (2001) concluded that the present distribution of P. canariensis is the result of a fragmentation of an originally larger continuous area, and they interpreted the geographic structure of the studied haplotypes as indicating a lack of present-day gene low among regions. In some cases, similar data on a single species can be interpreted in conlicting ways. Based on the demonstrated low capacity for long-distance dispersal of spores in the moss Lopidium concinnum (van Zanten, 1978), Frey et al. (1999) interpreted the molecular similarity among populations from New Zealand, Brazil and Chile as indicating a Gondwanan origin and slight molecular divergence and speciation in geological times (stenoevolution). McDaniel and Shaw (2003) and Shaw et al. (2008) considered that a Gondwanan origin for this moss would imply unacceptable rates for chloroplast sequences evolution, and that recent or ongoing dispersal is a more likely explanation for the species’ present distribution. Whether one or the other interpretation is more plausible could be approached by dating the molecular phylogenies. Although this method, if used properly, can be extremely useful, it is sometimes diicult to assess divergence times precisely (Cook and Crisp, 2005; Heads, 2005). For bryophytes the fossil record is relatively incomplete compared with the situation for some other organisms and only a few such studies therefore exist for this group. he problems can be illustrated by the survey on Plagiochila by Heinrichs et al. (2006), who used a single fossil specimen to date their phylogeny. Since the specimen could not be unequivocally assigned to a single node, they explored several possible scenarios to minimise the efect of incorrect assignments and concluded that resolving the diversiication time-frame is critical to understand the historical biogeography of their study group. Another example that shows how the dating of phylogenies is decisive for unravelling biogeographic patterns is that of Huttunen et al. (2008). heir phylogeny recovered for the moss genus Homalothecium shows a strong phylogeographic signal that suggested two main lineages, one including only American species and the other one with Western–Palaearctic species. Such a strong geographic structure is usually interpreted as indicating lack of long-distance dispersal events. he authors estimated the divergence time for the two lineages by using absolute rates of molecular BIOGEOGR A PHY OF MOSSES AND ALLIES evolution from the literature and factoring uncertainties around those estimates using probabilistic calibration priors. he diferent scenarios that could be reconstructed from their dating suggested that the a priori probable Laurasian origin would involve unsustainable nucleotide substitution rates and they therefore suggested that the present distribution is instead a result of transoceanic long-distance dispersal. A similar conclusion was reached by Devos and Vanderpoorten (2009) to explain the present distribution of the liverwort genus Leptoscyphus, also based on diferent calibration points depending on several assumptions. hese dated phylogenies suggest that long-distance dispersal did probably play an important role in shaping the distribution patterns of some bryophyte species or lineages. However, one should not forget that when such species or haplotypes show clear geographic structures, this only indicates that dispersal between the areas occurred at a certain more or less remote moment in time. Finally, it should also be considered that in bryophytes the study of diferent gene regions has sometimes led to incongruent phylogenetic topologies. As was already discussed by Hedenäs (2009b) this should be taken into account, since molecular phylogenies based on too few specimens per taxon may not relect the actual complexity and can lead to misleading conclusions. Moreover, the biogeographic patterns inferred by diferent analysis techniques or diferent molecular markers can be completely divergent. Even when molecular techniques provide much interesting and valuable information on bryophyte biogeography, care and further work are needed before more dei nitive conclusions are possible. 11.4 Concluding remarks As a summary of the numerous studies published, some main conclusions arise: several distribution patterns are found among the bryophytes, and diferent processes can explain each of them. Long-distance dispersal by wind has apparently played a chief role in at least some cases, whereas most of the known distribution patterns are better explained if other mechanisms, such as continental drift, stepping-stone migration and dispersal by anthropogenic or other agents, are also taken into account. Bryophytes are an ancient group of land plants and have had time enough to reach a very high level of diversiication. hey are remarkably heterogeneous from many points of view, such as structurally, physiologically and ecologically. Allorge (1947) stated that among mosses and allies, as well as in most plants, species greatly difer in their ecological amplitude; the same can be said about their dispersal capacity and their evolutionary potential. Given the complexity of the matter in hand, it seems that not a single hypothesis will be enough to explain the intricacy of the observed patterns. Biogeography 225 226 BIOGEOGR A PHY OF MICROSCOPIC ORG ANISMS of bryophytes more likely depends on a complex set of interacting phenomena, including both long-distance dispersal and efective stepping-stone propagation acting across long periods of time. Finally, bryophytes are small plants and their distribution areas are in general larger than those of lowering plants. 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