Patterns, Hypotheses and Processes in the Biology of Rare Bryophytes

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors nonprofit publishers academic institutions researchlibraries and research funders in the common goal of maximizing access to critical research

Patterns Hypotheses and Processes in the Biology of Rare BryophytesAuthor(s) Natalie L CleavittSource The Bryologist 108(4)554-566 2005Published By The American Bryological and Lichenological Society IncDOI httpdxdoiorg1016390007-2745(2005)108[0554PHAPIT]20CO2URL httpwwwbiooneorgdoifull1016390007-2745282005291085B05543APHAPIT5D20CO3B2

BioOne (wwwbiooneorg) is a nonprofit online aggregation of core research in the biological ecological andenvironmental sciences BioOne provides a sustainable online platform for over 170 journals and books publishedby nonprofit societies associations museums institutions and presses

Your use of this PDF the BioOne Web site and all posted and associated content indicates your acceptance ofBioOnersquos Terms of Use available at wwwbiooneorgpageterms_of_use

Usage of BioOne content is strictly limited to personal educational and non-commercial use Commercial inquiriesor rights and permissions requests should be directed to the individual publisher as copyright holder

0007-274505$1450

The Bryologist 108(4) pp 554 566Copyright q 2005 by the American Bryological and Lichenological Society Inc

Patterns Hypotheses and Processes in the Biology of Rare Bryophytes

NATALIE L CLEAVITT

Department of Natural Resources Cornell University Ithaca NY 14853-3001 USA e-mail nlc4cornelledu

Abstract Dominant patterns and processes in rare bryophyte ecology are presented withinthe framework of current rarity theory Available evidence suggests that bryophyte conservationshould primarily consider the importance of establishment and habitat requirements for rarespecies Preservation of rare and high quality habitats is essential Future understanding of causesof rarity in bryophytes will benefit most by exploring the ecological drivers that allow species toexpand their ranges Comparisons of rare-common congeners rare species throughout their range(not only where they are rare) and species currently experiencing range expansions or contrac-tions are likely to yield the most robust and relevant data sets

Keywords Moss liverwort dispersal management rarity ecological limitations

Rare bryophyte species are receiving increasedattention as the negative impacts on bryophytesfrom air pollution (Lee amp Caporn 1998 Pearce ampvan der Wal 2002 Tarvainen et al 2003 Wool-grove amp Woodin 1996) eutrophication (Drexler ampBedford 2002 Kooijman 1992) and forestry man-agement (Fenton amp Frego 2005 Frisvoll amp Prestoslash1997 Hazell amp Gustafsson 1999) become clearGeneral under-documentation of occurrences forbryophyte species in many parts of the world re-sults in a data deficit that often makes designationof bryophyte species difficult As a consequenceconservation of bryophyte species is mainly inci-dental and occurs through preservation of habitatfor other reasons Previous papers focusing on rar-ity in bryophytes have largely focused on specificpatterns relating to rare species (eg Laaka-Lind-berg et al 2000 Longton 1992a Longton amp Hed-derson 2000 Vitt amp Belland 1997) and on discus-sions of rare bryophyte conservation efforts (egBisang amp Hedenas 2000 Hodgetts 1992 Slack1992) In this paper I present an overview of rarebryophyte ecology by synthesizing what we knowof the patterns associated with rarity and by con-sidering the available literature on rare bryophyteswithin the framework of current rarity theory

The question lsquolsquoWhat is rarityrsquorsquo can be quitecomplex but in practice the vulnerability of a spe-cies is generally assigned based upon the numberof known occurrences in a given area and the per-ceived population threats associated with extinctionrisk (eg Church et al 2001 Nature Serve 2005)These ranks can be given at several scales typi-cally stateprovincial national and global In thecase of the British Red List for mosses and liver-worts rankings may also take into account popula-tion size or changes in the number of occupied sites

over time (Church et al 2001) In North Americawe lack the detailed baseline information requiredto include these other important criteria into ourranking system Indeed under-collection and datadeficiency in the case of bryophytes continues tobe a problem in assessing the rarity of these organ-isms in North America (Slack 1992)

When we rank species we are almost always re-ferring to morphologically delimited species Inbryophytes where cryptic speciation (genetic iso-lation of morphologically uniform populations)may be common there is an added complication todelineating rare species (Feldberg et al 2004McDaniel amp Shaw 2003 Shaw 2000 2001 Wyatt1992)

Once we do designate species as rare in an areawe often want to understand the types of rare spe-cies Rabinowitz (1981) proposed what has becomethe most widely cited classification of rare plantsbased on abundance range size and habitat speci-ficity Birks et al (1998) examined moss and liv-erwort species of the British flora in relation to Ra-binowitzrsquos (1981) classification and concluded thatlsquolsquomost bryophyte species are not common andmany have a narrow habitat specificityrsquorsquo Classifi-cation of bryophytes into Rabinowitzrsquos (1981) cat-egories emphasizes the diversity of rare species butalso pinpoints a key problem in quantifying raritythat is rarity is relative rather than absolute If thesame quantitative limits are used for all plants todifferentiate lsquolsquosmallrsquorsquo and lsquolsquolargersquorsquo range size orlsquolsquobroadrsquorsquo and lsquolsquonarrowrsquorsquo habitat specificity thenbryophyte species generally considered commonwithin the bryophytes may be rare by objective cri-teria for all plants In addition even within thebryophytes setting objective limits for these sub-

2005] 555CLEAVITT BRYOPHYTE RARITY

FIGURE 1 Leptokurtic relationship shown in many pa-pers from the plant literature from the scale of plots tofloras to latitudinal gradients (eg Gleason 1929 Preston1948) and more recent examples for bryophytes (egDoubt 2001 Longton amp Hedderson 2000 Vitt 1991)

jective categories is problematic (Longton amp Hed-derson 2000)

Rarity is relative not only to the taxonomic groupbeing studied and the criteria set to distinguish cat-egories such as lsquolsquosmallrsquorsquo and lsquolsquolargersquorsquo range sizebut also to the scale at which the designation isbeing made (Murray et al 2002) and the resolutionof the data being used to make the designation(Hartley amp Kunin 2003 Witte amp Torfs 2003) Spe-cies that are locally rare (eg state or provincialscale) may have high local abundance elsewhere intheir range [diffusive rarity of Schoener (1987)somewhere-abundant species of Murray amp Lepschi(2004)] or they may be sparse throughout theirrange [suffusive rarity of Schoener (1987) every-where-sparse species of Murray amp Lepschi 2004)]Considering three scales for a given species thereare nine general relationships (eight of which rep-resent forms of rarity) between species distribution(area of occupancy) and scale (total area consid-ered) (Hartley amp Kunin 2003 Murray et al 2002)with diffusive rarity (rarity at local scale with in-creased abundance at intermediate andor largescales) perhaps being the most common pattern(Murray et al 2002)

We begin then with several caveats 1) ourknowledge on the distributions of bryophyte spe-cies is incomplete and to some extent may alwaysremain so as our delineations of rare and commonare based on the number of known occurrences ofmorphologically delimited species 2) the separa-tion of species into categories of rarity is somewhatsubjective and always relative to how much infor-mation we have regarding species distributions and3) any synthesis of rare species research will tendto lump together different types of rare species be-cause studies are conducted in specific local areasof the species distribution and at varying spatialscales Within these limitations I will discuss rarebryophyte biology with the goals of 1) summariz-ing and distinguishing between the patterns andprocesses involved 2) placing information on rarebryophytes within the framework of current raritytheory and 3) suggesting areas and approaches toincrease our understanding of and ability to con-serve rare bryophytes

PATTERNS

One of the most general and earliest patterns de-scribed for rare species was that rarity is commonand commonness is rare (Raunakierrsquos law of fre-quency Gleason 1929 Preston 1948) that is in agiven area most of the species will be rare (havefew occurrences) while few species will be com-mon (have many occurrences) (Fig 1 species-range size distribution of Storch amp Gaston 2004)

This relationship appears to hold across spatialscales for many taxonomic groups (Gaston 1994Storch amp Gaston 2004) A second well-documentedpattern for rare and common species is the rela-tionship between local abundance and range size(Fig 2 abundance-range size relationship of Storchamp Gaston 2004) This relationship can be general-ized to reflect that species with smaller populationsat the local scale tend to have narrower geographicranges while species with large local populationstend to have broader geographic ranges (Darwin1859 Gaston 1994 Storch amp Gaston 2004) Therelationship can be described by the use of cate-gories or as a continuum (Fig 2) Gaston in partic-ular has championed the latter view (Gaston 1996Gaston et al 1997 Gaston amp Kunin 1997 Thomp-son et al 1998) On the other hand four main cat-egories often used are rare common restricted andsparse (eg Rabinowitz 1981) These categoriescorrespond respectively to terms used in metapop-ulation dynamics satellite core urban and ruralspecies (Hanski 1982 Soderstrom 1989)

Whether one chooses to view the relationship be-tween local abundance and range size as categoriesor a continuum it is important to acknowledge thatfor any species this relationship is not static eitherspatially or temporally In biogeography when con-sidering the global scale speciation is most oftenrecognized as a spatially explicit event (local spe-ciation) in which the new species then spreads froma point of origin (Levin 1993 2000) Implicit inthis view is that no species begins as common Re-gardless of the mode of speciation speciation

556 [VOL 108THE BRYOLOGIST

FIGURE 2 The relationship between species local abundance and range size can be viewed as four main categories(eg Rabinowitz 1981) or as a continuum suggesting a positive relationship between the two variables (eg Gaston1996)

events initially result in smaller range size andabundance compared to that of the progenitor spe-cies (Chown 1997 Gaston 1998) Species begin asrare and must attain wider abundance and distri-bution to become common If this is generally truethen it becomes less surprising that most species atany given point in time appear rare As the rangeof a species changes over time few species mayever attain the local abundance threshold requiredto significantly increase their geographic range Inaddition to remain common over time a speciesmust be able to maintain local abundances to avoidcontraction of its range Although it is generallyagreed that local population processes are criticalfor range expansion we currently know little aboutthe way the range of a species fluctuates over timeand how speciation affects the subsequent ability ofa species to expand its range (Gaston 1998)

What separates those species that are capable ofbecoming common from the vast majority that areless widespread How do species reach the thresh-old level of local abundance requisite for range ex-pansion We might learn the most about rarity byunderstanding how common species become com-mon For this purpose comparative studies betweenrare and common species are better suited thanmany studies of individual rare species As pointedout by Rabinowitz (1981) rare species are quite avariable collection of species Common speciesmay be more alike to one another in their ecologyand population structure if there is some commonecological driver that determines which species be-come and remain common

Humans are accelerating changes to habitat qual-ity and availability on the landscape through directhabitat destruction and alteration of nutrient levels

and climate In response fluctuations in the rangesof species are occurring within the span our lifetimes such as the range expansion by invasive ex-otic bryophytes (Herben 1994 Stieperaere et al1997) and range contraction of bryophytes sensitiveto nitrogen pollution (Lee amp Caporn 1998 Pearceamp van der Wal 2002 Woolgrove amp Woodin 1996)Studies of species experiencing range contractionsor expansions are critical to understanding thethreshold levels required for driving the shifts inlocal abundances of species For example Hasseland Soderstrom (2003) present evidence that recentrange expansion of Pogonatum dentatum (Brid)Brid from highlands into the lowlands in Fennos-candia is linked to the species need for closelyspaced frequently occurring small patches of dis-turbance that have become more common in thelowlands with the building of roads for forestry Atwhat density of roads did the establishment of newpopulations in the lowlands begin to succeed Arebryophyte species with life strategies less adaptedto disturbance (eg perennial stayer or dominant)more likely to be susceptible to range contractions

Within the broader rarity literature the only pat-tern associated with rarity in bryophytes relates tosporophyte production patterns (eg Gaston 1994Murray et al 2002 Thompson et al 1999) Thomp-son et al (1999) claimed lsquolsquoby far the best evidencefor a link between range and dispersal is found inmossesrsquorsquo This claim was based on work by Long-ton (1992a 1994) and Hedderson (1992) Longton(1992a) found evidence that certain reproductivesystems are over-represented in rare British mosseswhen compared to the whole British flora In par-ticular a higher proportion (55) of the rare spe-cies did not produce sporophytes compared to the


total British flora (19) A similar pattern has alsobeen found for British hepatics (Laaka-Lindberg etal 2000) What these authors have done is to matchthe pattern of rarity to patterns of sporophyte pro-duction As Longton (1992a) pointed out any sub-sequent discussion of processes based on this anal-ysis is speculative This pattern may or may not berelated to dispersal ability

In his original paper Longton (1992a) hardlytouched on dispersal limitations and focused in-stead on potential genetic constraints He hypothe-sized that these patterns of sporophyte productionfor rare species may relate to a lack of mates andsexual recombination in dioicous species and erod-ed genetic potential for obligate selfers in monoi-cous species In dioicous (ie unisexual gameto-phyte) species sporophyte production requires bothmale and female individuals present within a shortdistance for the sperm to travel from the antheridiato the archegonia

Hedderson (1992) did make an argument for theconnection between low sporophyte frequency anddecreased dispersal potential however he also rec-ognized the importance of environmental limita-tions in decreasing sporophyte frequency He con-sidered rarity of mosses at their range limits andfound a pattern of increased reliance on asexual re-production for moss species at the edges of theirrange Within his study area he remarked that therare taxa occupied a narrower range of habitats andoccurred in a lower proportion of suitable foreststands which suggested environmental limitationsFurther studies comparing the ecology of species inthe center of their range and at their range limitswould be a welcome addition to the discourse onrare bryophyte biology

Perhaps the greatest challenge in exploring traitsassociated with rarity is posed by the paradox ofwhether a given trait is a cause or consequence ofa speciesrsquo rarity (Fiedler 1986 Fiedler amp Ahouse1992 Gaston amp Kunin 1997) That is did the plantspecies evolve the traits associated with rarity afterbecoming rare or did the speciation event or sub-sequent genetic change result in these traits whichpredisposed the species toward becoming or re-maining rare Is the wider distribution of specieswith greater sporophyte frequency actually a resultof better dispersal potential or to the contrary domore common species produce sporophytes morefrequently because the probability of successful fer-tilization increases for species with high local abun-dances The latter case is arguably supported bythe break-down of the sporophyte frequency-raritypattern in monoicous mosses and liverworts whosesporophyte production is not limited by proximityof male and female plants (Laaka-Lindberg et al2000 Longton 1992a 1994)

Within bryophyte literature the most convincingevidence for a relationship between dispersal abilityand range size comes from the work of van Zantenwith bryophytes of the southern hemisphere (Zan-ten 1978 Zanten amp Gradstein 1988 Zanten amp Pocs1981) In experimental spore viability trials therewas a strong correlation between tolerance ofspores to desiccation freezing and UV exposure(conditions that would be experienced during longdistance dispersal) and the range size of a species(Zanten amp Gradstein 1988 Zanten amp Pocs 1981)In particular spores of species endemic to NewZealand were less tolerant to experimental treat-ments than spores of more wide ranging speciesThis comparison did not differentiate between suf-fusive and diffusive rarity nor consider differencesin local abundance or habitat specificity of the spe-cies Despite this evidence for a link between sporetolerance and range size there remains a disturbingschism in the bryophyte literature on the issue ofestablishment from spores Dispersal by spores hasbeen repeatedly cited as the critical factor explain-ing species distributions yet establishment experi-ments repeatedly demonstrate very low germinationof spores in the field What is the importance ofspores in establishment How many new popula-tions are established from sexual versus asexualpropagules

Bryologists have tried to reconcile this conflict-ing evidence by suggesting that asexual reproduc-tion is more important for maintaining local popu-lations while spores are important for chance longdistance dispersal events (eg Longton 1994)However we still know remarkably little about theestablishment of new bryophyte populations despiteits crucial role in local and therefore regional ex-pansion of a species The importance of spores inestablishment of mosses seems to vary greatly de-pending on life strategy (During 1997 Miles ampLongton 1990 Roads amp Longton 2003) Experi-mental sowing of spores in the field has resulted inno or very low establishment (Keever 1957 Milesamp Longton 1990) for all but the weediest of species(eg Funaria hygrometrica Hedw) and the largerrole of asexual reproduction in bryophyte ecologyhas gained wide acceptance (Newton amp Mishler1994 Slack 1997) Several authors (Li amp Vitt 19941995 Longton 1994 Mishler amp Newton 1988Watson 1981) have suggested that chemical inhi-bition may explain the lack of spore germination inthe field Concurrent manipulation of spores andasexual propagules in establishment experiments isneeded to understand their relative roles in estab-lishing new populations under varying circumstanc-es

Other patterns that have been associated with rar-ity in bryophytes relate to life history strategies and


TABLE 1 Current biological hypotheses that have been proposed to explain positive interspecific local abundance-global range size relationships (based largely on Gaston et al 1997) and their implicationspredictions for rare speciesrelative to common species

Hypothesis name(source) Pattern

Process(es) compared to commonspecies

Gene pool-niche inter-action (Stebbins1980)

rare species have limited adaptive poten-tial for new environments

rare species have lower genetic diversity

Resource breadth(Brown 1984)

rare species have narrower fundamentalniche breadths than common species

rare species have narrower physiologicaltolerance

Habitat selection(OrsquoConnor 1987)

rare species have narrower realized nichesrelative to their fundamental niches

inability of rare species to overcome intra-or inter-specific competitive effects

Metapopulation dy-namics (Hanski1991)

rare species have less ability for popula-tion expansion

rare species have poorer dispersal abilities

Vital rates (Holt et al1997)

rare species have lower maximum popula-tion growth

rare species have lower reproduction andor higher mortality

habitat usage Vitt and Belland (1997) found acro-carpous growth form and a stress tolerant life strat-egy were over-represented in the rare species floraof Alberta when compared to the occurrence ofthese characteristics in the non-rare moss flora Inthe British moss flora rare species were more likelyto be colonist or shuttle species (ie stress avoid-ers) (Longton 1992a Longton amp Hedderson 2000)Given the conflicting patterns for life strategy andrarity in the Albertan and British floras any patternrelating rarity to life history strategies appears un-resolved In addition to a life strategy pattern Vittand Belland (1997) found that rare species weremore likely to reside in alpine habitats The patternthat rare species use resources that are rare on thelandscape has been formulated by Hanski et al(1993) and termed the resource availability hypoth-esis Additional floristic studies on bryophytes fromwestern North America have also supported thispattern at regional scales (Doubt 2001 Heinlen ampVitt 2003) Vitt and Belland (1997) argued thatprevalence of alpine habitat for rare Alberta mossesrelated to habitat restrictions of these mosses how-ever this restricted distribution pattern does notclarify whether the species are limited by abiotic orbiotic factors This pattern could result from a num-ber of different processes and should not be takento imply physiologically-based habitat specificity

HYPOTHESES AND PROCESSES

From the prior section some processes suggestedto be important in rare bryophyte biology includegenetic potential for adaptation to new environ-ments dispersal ability and habitat restrictions In-teractions between these processes may also be im-portant as recognized by Stebbins (1980) in hisgene pool-niche interaction theory This hypothesissuggests that rare species specifically endemicsare the result of an interaction between localized

environmental conditions lack of genetic diversity(which inhibits expansion into surrounding envi-ronments) and the effects of past climate on pop-ulation distributions One of the basic predictionsof this hypothesis is that rare species will have low-er genetic diversity than common species (Table 1)

The largest group of hypotheses relevant to stud-ies of rarity has developed in an attempt to explainthe positive relationship between local abundanceand range size In their comprehensive review Gas-ton et al (1997) described hypotheses that havebeen proposed to explain the positive local abun-dancendashrange size relationship (Table 1) For a morein depth discussion of these hypotheses the readeris referred to Gaston et al (1997) For the purposesof this paper I present the hypotheses in abbrevi-ated form along with the implicit ecological traitsof rare species based on each hypothesis (Table 1)Overall rare-common differences have been hy-pothesized to stem from differential 1) genetic po-tential 2) habitat tolerances 3) competitive abili-ties 4) dispersal abilities and 5) reproductive andsurvival rates These hypotheses emphasize the im-portance of understanding the ecology of a speciesto explore why it is rare or common

Genetic potential Genetic variation in rare andcommon vascular plants has been reviewed by anumber of authors based on isozyme data sets forcongeners (Cole 2003 Gitzendanner amp Soltis 2000Karron 1987) and they have found reduction ingenetic variation as measured by some parametersbut not all Most recently Cole (2003) demonstrat-ed that rare vascular plants have significantly re-stricted gene flow compared to common congenersCompared to vascular plants there is limited datapublished for bryophytes Wyatt (1992) comparedmembers in section Rosulata of the genus Plagiom-nium He found the globally rare narrowly distrib-uted species had lower genetic diversity than the


common widespread species Stenoslashien and Flatberg(2000) reported that the rare (only known from fivelocalities in central Norway) Sphagnum troendelag-icum Flatberg had a similar amount of genetic var-iability as the much more common S fallax HKlinggr Population genetics patterns for S troen-delagicum suggest multiple hybrid origins of thespecies which has been confirmed by subsequentwork showing this species to be an allopolyploidof more widespread S tenellum (Brid) Brid and Sbalticum (Russow) C E O Jensen (Sastad et al2001) With the amount of molecular work cur-rently taking place in bryology a much more com-prehensive comparison of genetic potential in rareand common bryophytes should soon be forthcom-ing For instance Shaw has reported data on thepopulation genetics of several rare heavy metalmosses (Shaw 1993 2000 Shaw amp Schneider1995)

Habitat tolerances As noted earlier by Birkset al (1998) bryophytes tend to have lsquolsquonarrowrsquorsquohabitat specificity In contrast to vascular plants forbryophytes habitat specificity is often associatedwith disjunct distribution patterns rather than en-demism (Schofield amp Crum 1972) For instance therare and widely disjunct lsquolsquoheavy metalrsquorsquo mosses arespecific to substrates with high heavy metal con-centrations (Persson 1956 Shaw 1993) Because ofthe advantages of comparative studies within gen-era monographic works currently provide the bestmeans of evaluating the resource breadth hypothe-sis for bryophytes Shaw (1981) and Horton (1988)suggested that rare moss species tend to have nar-rower edaphic requirements than more commonspecies For propaguliferous Pohlia species Shaw(1981) noted a correlation between lsquolsquoecological am-plitudersquorsquo (which seems comparable to nichebreadth) geographic distribution and the degree ofmorphological variability I analyzed data presentedfor soil chemistry in Horton (1988) by separatingrare and common species based on Horton (1983)This analysis demonstrated that common Encalyptaspecies had significantly wider average nichebreadths for pH and organic matter content thanrare species (Mann Whitney U p5 0006 and0035 respectively) Heegaard (1997) also foundthis general pattern for Andreaea species in Nor-way although the number of Andreaea species in-cluded in his study that are rare on a broad scalewas limited (Heegaard pers comm)

While patterns of habitat specificity are well doc-umented in bryophytes the link to experimentallydemonstrated physiological tolerances is often lack-ing There is accumulating evidence that habitat tol-erances in bryophytes are related to establishmentrequirements (Cleavitt 2001 2002a Furness amp Hall1981 Li amp Vitt 1994 1995 Wiklund 2003 Wik-

lund amp Rydin 2004) and mosses seem to be par-ticularly sensitive to substrate chemistry during es-tablishment (eg Cleavitt 2001 Thomas et al1994 Wiklund amp Rydin 2004) Furness and Hall(1981) linked the appearance of the British Red-listed Physcomitrium sphaericum (C F Ludw)Furnr after extended summer droughts to the spe-ciesrsquo requirement for high temperatures (19ndash328C)and light exposure for germination In a comparisonof three rare-common pairs of bryophyte speciesthe species with narrowest substrate breadths forpH and percent organic matter were the most sen-sitive to substratum chemistry during establishment(Cleavitt 2001) However this did not fall strictlyalong lines of rare and common species as one ofthe species was rare at the local and global scalesbut the second was not Wiklund (2003) concludedthat the rare moss Buxbaumia viridis required ei-ther logs with constant high moisture or logs withlower moisture but higher pH and phosphorus lev-els For two species of moss included on the RedList in Europe B viridis (suffusive rarity) andNeckera pennata (diffusive rarity more common inNorth America) there was a complex interactionbetween water potential substratum pH spore ger-mination and protonematal growth (Wiklund amp Ry-din 2004) Low occupation of apparently suitablesites may result from the low quality of those sitesfor establishment (Wiklund amp Rydin 2004)

Competitive ability Earlier observers of bryo-phyte communities hypothesized a minimal role forcompetition in structuring bryophyte communities(Slack 1990) This view can be traced to the overallruderal and stress tolerant strategies of bryophytesand the inherent dominance of disturbance in con-trolling the distribution of species However indi-vidual moss species do have varying capacity forusing temporally available resources which impliessome species would be better competitors than oth-ers (Grime et al 1990) and competition betweenbryophytes has been documented in relatively sta-ble habitats such as grasslands and peatlands (Ry-din 1997 Zamfir amp Goldberg 2000) In more dy-namic habitats Lloret (1991) found that the patchlongevity for Tayloria tenuis (With) Schimp waslimited through overgrowth by pleurocarpousmosses This moss is rare in at least parts of itsrange (Church et al 2001)

In general the limited research on competitiveeffects among adult bryophytes has indicated thatfor mosses competitive interactions may be mostinfluential during the establishment stage (Li amp Vitt1995 Rydin 1986 1997 Slack 1997) and bioticchemical inhibition may play an important role(Newton amp Mishler 1994 Watson 1981) Compe-tition during the establishment stage can take manyforms including differential diaspore production


diaspore longevity or diaspore sensitivity to thepresence of other species (and perhaps their chem-ical exudates) For instance in a bryophyte colo-nization experiment the number of diaspores pro-duced by a species per unit time was determined tobe the most important factor explaining which spe-cies became dominant in permanent plots (Toorenamp During 1988a) Through experiments usingbryophyte fragments Zamfir and Goldberg (2000)reported the existence of a competitive hierarchyfor seven grassland moss species Bates (1993)compared the growth increments of Pallavicinialyellii (Hook) Carruth [diffusive raritymdashincludedon the British Red list (Church et al 2001) yet com-mon in eastern North America] and Pellia epiphylla(L) Corda a much more common species Al-though not congeners in his comparison of thesetwo species of thalloid liverworts Bates found thatthe common P epiphylla had three times the lengthincrease of P lyellii The rare species seemed to belimited by competition to drier sites where the com-mon species was absent (Bates 1993) In additionP lyellii had a stricter coupling between thallusgrowth and occurrence of warm temperatures in thesummer months

The work of Marino (1991) is perhaps the mostcomprehensive comparative study of bryophytesand demonstrated that competitive interactions forfour entomophilous moss species establishing fromspores on dung varied with the moisture level ofthe substratum In his two congeneric pairs Tetra-plodon mnioides (Hedw) Bruch amp Schimp andSplachnum luteum Hedw are much less commonthan T angustatus (Hedw) Bruch amp Schimp andS ampullaceum Hedw yet competitive abilities ofcongeneric species were symmetrical that is for agiven species growth in species mixes did not differfrom growth alone This result may in part be anartifact of the location of the study in a regionwhere the local abundances of T mnioides and Sluteum may exceed that of T angustatus and Sampullaceum despite the fact that the latter two aremore common at the continental scale (Marino1991) It would be instructive to test competitiveabilities of these four species in another part of theirrange Although comparative studies between rareand common species hold much promise for rarebryophyte biology in order to be truly informativefor the purposes of conservation they require con-sideration of issues such as the types of rarity (suf-fusive versus diffusive) and scale limitations (Mur-ray et al 2002)

Overall there is little data for comparing thecompetitive abilities of rare and common bryo-phytes in either establishment or adult stages In mywork with three rare-common species pairs I in-vestigated competition during both life stages

(Cleavitt 2002a 2004a) The establishment stageexperiments compared establishment of apical ga-metophyte fragments in monospecific plots withthat of fragments in plots with mixed species at aconstant density [similar to the design of Marino(1991) with spores] Adult stage experiments in-cluded colony mapping and colony neighbor en-counter tallies (sensu Kimmerer 1994) For twopairs of rare-common species regeneration was notsignificantly affected by neighbor identity regard-less of whether the species were rare or common(Cleavitt 2002a 2004a) that is competitive abili-ties appeared symmetric as in the studies by Marino(1991) However if congeners are less likely to ex-hibit competition during establishment then thisnegative result may be partially explained by theexperimental design A more thorough examinationof the comparative competitive abilities of rare andcommon bryophyte species during establishmentshould also address the hypothesis that rare specieswill be selected for increased inter-specific com-petitive ability while common species will be se-lected for greater intra-specific competitive ability(Holt 1997 Orians 1997)

As part of the same study I used colony expan-sion the number of neighbor encounters and theoutcome of those encounters to evaluate relativecompetitive abilities of the rare-common pairs inthe adult stage Colonies of rare and common bryo-phytes had a similar percentage of colonies that ex-panded (Fig 3) and similar neighbor contact fortwo pairs (Fig 4a) For the third pair Bryum por-sildii (I Hagen) C J Cox amp Hedd had signifi-cantly more colonies that had expanded over threeyears (Fig 3) and lower frequency of neighbor en-counters than its common congener B pseudotri-quetrum (Hedw) P Gaertn B Meyer amp Schreb(Fig 4a) When the front of contact between twoneighbor colonies was dissected and scored as awin (study species overgrew neighbor) tie (bothspecies equally intermingled or loss (study speciesovergrown by neighbor) there was no differencebetween rare-common pairs (Fig 4b) These com-parisons were all made in situ and show that inhabitats where the species were present there wasno difference in competitive ability of the rare andcommon species More detailed experiments with apair of rare-common species in the genus Mniumdemonstrated that the rare species was limited fromexpanding to lower elevations in the boreal zone bycompetition from Hylocomium splendens (Hedw)Schimp (Cleavitt 2004a) We need experiments de-signed to compare the competitive abilities of rareand common mosses in several life stages and avariety of habitats to test whether competition par-tially explains restriction of many rare species tospecialized habitats


FIGURE 3 Scores of mapped rare-common bryophytecolonies taken after three years (reproduced from Cleavitt2002a) Rare species abbreviations are in bold and theyare to the left of their common partner The species areBryum porsildii B pseudotriquetrum Didymodon johan-senii D rigidulus Hedw var gracilis (Hook amp Grev) RH Zander Mnium arizonicum and M spinulosum Bruchamp Schimp Letters given above the bars represent post-hoc subsets (a 5 005) for colony expansion while lettersbelow the bars denote post-hoc subsets for colony disap-pearance Because disturbance of Didymodon rigiduluscolonies resulted in disappearance of all marked coloniesover three years data for another group of colonies takenover a four-month period is also presented Colony sizechanges were evaluated using photographs of marked col-onies taken in 1998 and 2000

FIGURE 4 Differences in the frequency of a) neighborencounter and b) the outcomes of those encounters for sixmoss species three rare-common pairs with 150 scoredcolonies for each species (reproduced from Cleavitt2002a) Rare species abbreviations are in bold and theyare to the left of their common partner The species areBryum porsildii B pseudotriquetrum Didymodon johan-senii D rigidulus var gracilis Mnium arizonicum and Mspinulosum Letters represent post-hoc subsets (a 5 005)In 4b the subsets denote significant differences in en-counter losses Bryum porsildii was not included in thisanalysis because encounter intersections could not beevaluated by colony dissection due to the limited numberof colonies and risk of colony loss from the rock faceswith such disturbance

Dispersal ability The work of van Zanten de-scribed earlier remains the cornerstone in our un-derstanding of dispersal ability and species rangesize in bryophytes (Zanten 1978 Zanten amp Grad-stein 1988 Zanten amp Pocs 1981) In this work apositive relationship between the ability of sporesto remain viable after conditions simulating longdistance dispersal and the species range size wasreported for New Zealand bryophytes RecentlyShaw et al (2002) reported congruence between theexperimental results of van Zanten and molecularevidence regarding the long distance dispersal po-tential of several species Experiments such asthose by van Zanten have yet to be performed withasexual propagules or for continental floras Rarebryophyte species may rely more on asexual repro-duction than common species (Hedderson 1992Laaka-Lindberg et al 2000 Longton 1992) andtherefore comparison of dispersal ability of asexualpropagules is necessary for a complete comparisonof dispersal ability In a comparison of dispersalpotential of apical gametophyte fragments for threepairs of rare and common species pairs the rarespecies had higher (two pairs) or equivalent (onepair) desiccation tolerance than common speciesand maintained 80 or higher viability after 120days dry storage (Cleavitt 2002b) The ecologicalsignificance of propagule storage experiments isunknown without further understanding of the

range of dispersal mechanisms for bryophyte prop-agules In particular future research should expandon the work such as Tooren and During (1988b)with earthworms and Kimmerer and Young (1995)with slugs to further examine the role of animals inbryophyte diaspore dispersal (see also review byLaaka-Lindberg et al 2003)

Dispersal may not only occur over space butthrough time as many species have propagules and


spores that maintain viability in a diaspore bank(analogous to the seed bank) The diaspore bankhas been documented in grassland and forest sys-tems (During 1997 During amp ter Horst 1983 Jons-son 1993) and it may allow species with long-liveddiaspores that are able to survive in situ to respondfaster to small-scale disturbances than species with-out long-lived propagules Bryophyte diaspores notonly include spores but also a vast array of asexualpropagules such as plant fragments gemmae rhi-zoidal fragments protonematal fragments bubilsand specialized fragile leaf tips Physcomitriumsphaericum a moss included on the British RedList has been documented as relying on persistenceof a spore bank (Furness amp Hall 1981)

Reproduction and establishment In generalthere has been very little research on moss repro-ductive limitations (During amp van Tooren 1987Longton 1994) Moss sperm usually only travel afew centimeters in terrestrial situations althoughsplash cups may increase this distance to a meter(Longton amp Schuster 1983 Wyatt amp Anderson1984) and invertebrate transport may be importantfor lipid containing sperm masses (Paolillo 1981)For bryophytes in general the paucity of special-ized gamete transfer mechanisms together with theprevalence of asexual reproduction makes a pri-mary reproductive limitation less likely than inflowering plants that have complex pollinator rela-tionships This relates again to the interpretation ofthe patterns documented by Longton (1992a) be-tween sporophyte production and rarity of specieswhich highlights the need for comparative studieson the relative contribution of sexual and asexualpropagules in establishing new populations

In terms of sexual reproductive limitations di-oicous mosses could face limitations related to thedistance between male and female plants whilemonoicous mosses may experience problems basedon the increased likelihood of self-fertilization(Roads amp Longton 2003) The evidence for the lim-itation of sexual reproduction in monoicous mossesis much weaker than for dioicous mosses (Longton1994) There are many dioicous species that are notknown to produce sporophytes anywhere and oftenthese species occur in highly disjunct populationscontaining only female or male plants (Longton1992a Longton amp Schuster 1983) The increaseddifficulty of sexual reproduction in dioicous mossesmay explain why specialized asexual propagulesare more frequent in dioicous mosses (Imura 1994Longton 1992a) although this pattern does not holdfor liverworts (Laaka-Lindberg et al 2000)

American populations of the rare moss Scope-lophila cataractae (Mitt) Broth where sporophyteproduction is unknown and all populations are ei-ther male or female present an interesting case in

point (Shaw 1993 1995) Shaw (1993) suggestedthat the most likely explanation for this pattern waslong distance dispersal of asexual diaspores (in thiscase plant fragments) for two reasons First thespecies does not produce sporophytes in NorthAmerica but moss fragments of the species can re-main dormant for several years and second thespecies occurs on substrates such as mine tailingsthat have only been available for colonization inrecent history (Shaw 1993) Despite the likely asex-ual origin of the S cataractae populations theywere shown to possess a great deal of morpholog-ical and physiological variability when grown ondifferent soil types

Survival rates The main causes of mortality inbryophytes are thought to include overgrowth byneighbors physical disturbance and grazing (Kim-merer 1994 Oslashkland 1995 2000) Overgrowth byneighbors was discussed under competition in thispaper Disturbance may represent the most preva-lent cause of colony death in bryophytes especiallyfor those with few neighbors Although rhizoidsmay help in stabilization bryophyte species lackroots to secure them to their substrate and are ofteninfluenced by small-scale disturbances such asthose produced by small rodents The importanceof small-scale disturbances to the establishment ofmosses on logs has been demonstrated by Kim-merer and Young (1996) Disturbance may also betied to apparent habitat restrictions during estab-lishment For instance Didymodon johansenii (RS Williams) H A Crum a rare moss restricted tosubstrata characterized by a layer of fine silt wasfound to have an initial physical rather than phys-iological limitation (Cleavitt 2002c) Rather thanincreasing survivorship or growth of fragments rel-ative to fragments grown on plots without silt themain effect of the silt layer was to increase thenumber of fragments adhering to the plots on thelogs

Generally bryophytes are not viewed as havingmany natural enemies and evidence for herbivoryon bryophytes when compared to lichens or vas-cular plants appears inconsequential (Longton1992b) There is good evidence that gametophoreherbivory is limited by chemical defenses partic-ularly polyphenolics in the cell walls (Davidson etal 1990 Gerson 1982) Sporophytes especially inimmature stages are more liable to predation byants (Gerson 1982) and slugs (Davidson et al1990) The restricted moss species Mnium arizon-icum Amann appears to suffer from low sporo-phyte production and high sporophyte predation(Cleavitt 2004b) Given the energetic trade-offs be-tween sexual and asexual reproduction recentlydocumented in several bryophytes (Bisang amp Ehr-len 2002 Ehrlen et al 2000 Pohjamo amp Laaka-


Lindberg 2004 Rydgren amp Oslashkland 2003) sporo-phyte herbivory could serve as a selective pressurefavoring reliance on asexual modes of reproductionand might thereby lower the dispersal ability of aspecies if spores were key in establishing new pop-ulations in currently uncolonized habitats

CONCLUDING REMARKS

The tendency of rare species to occupy habitatsthat are rare on the landscape suggests that conser-vation of rare bryophytes must be undertakenthrough preservation of rare and high quality hab-itats (Berglund amp Jonsson 2001 Doubt 2001 Hein-len amp Vitt 2003 Pharo amp Beattie 2001) In mostregions (perhaps excluding Britain and parts ofScandinavia) continued floristic documentation re-mains more critical than studies of individual rarespecies for gaining the information base necessaryto make informed decisions on habitats that are inneed of protection To this end bryophyte conser-vation at the larger scale would benefit greatly fromthe creation of a distribution map repository andstandardization of the scales used for creating spe-cies distribution maps

Events in the establishment stage especially therestriction of species to habitats that are optimal forestablishment are the most prevalent ecological ex-planations for the distribution patterns of rare bryo-phyte species based on current evidence These es-tablishment restrictions result from a number offactors including physiological limitations escapefrom competition and mediation of or dependenceon disturbance In contrast common species seemcapable of occupying and reproducing in both op-timal and sub-optimal habitats (Cleavitt 2002ab)

Rare species biology will benefit from under-standing ecological drivers that allow species to ex-pand their ranges such as those by Hassel for Po-gonatum dentatum in Fennoscandia (Hassel amp Sod-erstrom 2003 Hassel et al 2005) and those on in-vading bryophyte species in Europe [egCampylopus introflexus (Hedw) Brid Hassel ampSoderstrom 2005 Orthodontium lineare SchwagrHerben 1994 Hassel amp Soderstrom 2005 Lopho-colea semiteres (Lehm) Mitt Stieperaere et al1997] These studies currently favor the importanceof disturbance in species expansion By the samelogic the vulnerability of bryophyte species mayvary depending upon their ability to adapt to dis-turbances (based on their innate life history char-acteristics) and these should be taken into accountwhen making species designations

ACKNOWLEDGMENTS

This paper expands upon my introduction to the sym-posium lsquolsquoBiology of rarity Conservation of Bryophytes

and Lichensrsquorsquo at the Botany 2004 meetings in SnowbirdUT I thank Nancy Slack for the opportunity to introducethe symposium and the ABLS for financially supportingmy participation in the symposium This paper benefitedgreatly from the critically constructive comments of Jen-nifer Doubt Royce Longton Nancy Slack and Lars Sod-erstrom

LITERATURE CITED

BATES J W 1993 Comparative growth patterns of thethalloid liverworts Pallavicinia lyellii and Pellia epi-phylla at Silwood Park southern England Journal ofBryology 17 439ndash445

BERGLUND H amp B G JONSSON 2001 Predictability ofplant and fungal species richness of old-growth borealforest islands Journal of Vegetation Science 12 857ndash866

BIRKS H J B E HEEGAARD H H BIRKS amp B JONS-GARD 1998 Quantifying bryophyte-environment re-lationships pp 305ndash319 In J W Bates N W Ashtonamp J G Duckett (eds) Bryology for the Twenty-firstCentury Maney Publishers and British BryologicalSociety Leeds

BISANG I amp L HEDENAS 2000 How do we select bryo-phyte species for conservation and how should weconserve them Lindbergia 25 62ndash77

mdashmdashmdash amp J ERHLEN 2002 Reproductive effort and costof sexual reproduction in female Dicranum polysetumTHE BRYOLOGIST 105 384ndash397

BROWN J H 1984 On the relationship between abun-dance and distribution of species American Naturalist124 255ndash279

CHOWN S L 1997 Speciation and rarity separating causefrom consequence pp 91ndash109 In W E Kunin amp KJ Gaston (eds) The Biology of Rarity Chapman ampHall New York

CHURCH J M N G HODGETTS C D PRESTON amp N FSTEWART 2001 British Red Data Books Mosses andLiverworts Joint Nature Conservation Committee Pe-terborough

CLEAVITT N L 2001 Disentangling moss species limi-tations the role of substrate specificity for six speciesoccurring on substrates with varying pH and percentorganic matter THE BRYOLOGIST 104 59ndash68

mdashmdashmdash 2002a Relating rarity and phylogeny to the aut-ecology of mosses a comparative study of three rare-common species pairs in the Front Ranges of AlbertaCanada PhD thesis University of Alberta Edmon-ton

mdashmdashmdash 2002b Stress tolerance of rare and common mossspecies in relation to their occupied environments andasexual dispersal potential Journal of Ecology 90785ndash795

mdashmdashmdash 2002c A test of physical limitation to specificsubstrata during establishment for Didymodon johan-senii a rare moss Journal of Bryology 24 197ndash206

mdashmdashmdash 2004a Comparative ecology of a lowland and asubalpine species of Mnium in the northern RockyMountains Plant Ecology 174 205ndash216

mdashmdashmdash 2004b Controls on the distribution of Mnium ar-izonicum along an elevation gradient in the FrontRanges of the Rocky Mountains Alberta Journal ofthe Torrey Botanical Society 131 150ndash160

COLE C T 2003 Genetic variation in rare and commonplants Annual Review of Ecology Evolution andSystematics 34 213ndash237

DARWIN C 1859 On the Origin of Species by Means of


Natural Selection or the Preservation of FavouredRaces in the Struggle for Life John Murray London

DAVIDSON A J J B HARBORNE amp R E LONGTON 1990The acceptability of mosses as food for generalist her-bivores slugs in Arionidae Botanical Journal of theLinnean Society 104 99ndash113

DOUBT J C 2001 Distribution patterns of moss conser-vation value with implications for conservation man-agement A case study of Waterton Lakes NationalPark MSc thesis University of Alberta Edmonton

DREXLER J Z amp B L BEDFORD 2002 Pathways of nu-trient loading and impacts on plant diversity in a NewYork peatland Wetlands 22 263ndash281

DURING H J 1997 Bryophyte diaspore banks Advancesin Bryology 6 103ndash134

mdashmdashmdash amp B TER HORST 1983 The diaspore banks ofbryophytes and ferns in chalk grassland Lindbergia 957ndash64

mdashmdashmdash amp B F VAN TOOREN 1987 Recent developmentsin bryophyte population ecology Trends in Ecologyand Evolution 2 89ndash93

ERHLEN J I BISANG amp L HEDENAS 2000 Costs of spo-rophyte reproduction in the moss Dicranum polyse-tum Plant Ecology 149 207ndash217

FELDBERG K H GROTH R WILSON A SCHAFER-VER-WIMP amp J HEINRICHS 2004 Cryptic speciation in Her-bertus (Hebertaceae Jungermanniopsida) range andmorphology of Herbertus sendtneri inferred fromnrITS sequences Plant Systematics and Evolution249 247ndash261

FENTON N J amp K A FREGO 2005 Bryophyte (moss andliverwort) conservation under remnant canopy in man-aged forests Biological Conservation 122 417ndash430

FIEDLER P L 1986 Concepts of rarity in vascular plantspecies with special reference to the genus Calochor-tus Pursh (Liliaceae) Taxon 35 502ndash518

mdashmdashmdash amp J J AHOUSE 1992 Hierarchies of cause to-ward an understanding of rarity in vascular plant spe-cies pp 23ndash47 In P L Fiedler amp S K Jain (eds)Conservation Biology The Theory and Practice ofNature Conservation Preservation and ManagementChapman amp Hall New York

FRISVOLL A A amp T PRESToslash 1997 Spruce forest bryo-phytes in central Norway and their relationship to en-vironmental factors including modern forestry Ecog-raphy 20 3ndash18

FURNESS S B amp R H HALL 1981 An explanation ofthe intermittent occurrence of Physcomitrium sphaer-icum (Hedw) Brid Journal of Bryology 11 733ndash742

GASTON K J 1994 Rarity Chapman amp Hall Londonmdashmdashmdash 1996 Species-range size distributions patterns

mechanisms and implications Trends in Ecology andEvolution 11 197ndash201

mdashmdashmdash 1998 Species-range size distributions productsof speciation extinction and transformation Philo-sophical Transactions of the Royal Society of LondonB 353 219ndash230

mdashmdashmdash T M BLACKBURN amp J H LAWTON 1997 Inter-specific abundance-range size relationships an ap-praisal of mechanisms Journal of Animal Ecology 66579ndash601

mdashmdashmdash amp W E KUNIN 1997 Concluding comments pp262ndash272 In W E Kunin amp K J Gaston (eds) TheBiology of Rarity Chapman amp Hall London

GERSON U 1982 Bryophytes and invertebrates pp 291ndash332 In A J E Smith (ed) Bryophyte EcologyChapman amp Hall London

GITZENDANNER M A amp P S SOLTIS 2000 Patterns of

variation in rare and widespread plant congenersAmerican Journal of Botany 87 783ndash792

GLEASON H A 1929 The significance of Raunkiaerrsquos lawof frequency Ecology 10 406ndash408

GRIME J P E R RINCON amp B E WICKERSON 1990Bryophytes and plant strategy theory Botanical Jour-nal of the Linnean Society 104 175ndash186

HANSKI I 1982 Dynamics of regional distribution thecore and satellite species hypothesis Oikos 38 210ndash221

mdashmdashmdash 1991 Single-species metapopulation dynamicsmdashconcepts models and observations Biological Journalof the Linnean Society 42 17ndash38

mdashmdashmdash J KOUKI amp A HALKKA 1993 Three explanationsof the positive relationship between distribution andabundance of species pp 108ndash116 In R Ricklefs ampD Schluter (eds) Historical and Geographical Deter-minants of Community Diversity University of Chi-cago Press Chicago

HARTLEY S amp W E KUNIN 2003 Scale dependency ofrarity extinction risk and conservation priority Con-servation Biology 17 1559ndash1570

HASSEL K B PEDERSEN amp L SODERSTROM 2005 Chang-es in life-history traits in an expanding moss speciesphenotypic plasticity or genetic differentiation a re-ciprocal transplantation experiment with Pogonatumdentatum Ecography 28 71ndash80

mdashmdashmdash amp L SODERSTROM 2003 Life history variation ofPogonatum dentatum (Brid) Brid in contrasting hab-itats Journal of the Hattori Botanical Laboratory 93215ndash222

mdashmdashmdash amp mdashmdashmdash 2005 The expansion of alien mossesOrthodontium lineare and Campylopus introflexus inBritain and continental Europe Journal of the HattoriBotanical Laboratory 97 183ndash193

HAZELL P amp L GUSTAFSSON 1999 Retention of trees atfinal harvestmdashevaluation of a conservation techniqueusing epiphytic bryophyte and lichen transplants Bi-ological Conservation 90 133ndash142

HEDDERSON T A 1992 Rarity at range limits dispersalcapacity and habitat relationships of extraneous mossspecies in a boreal Canadian national park BiologicalConservation 59 113ndash120

HEEGAARD E 1997 Ecology of Andreaea in western Nor-way Journal of Bryology 19 527ndash636

HEINLEN E R amp D H VITT 2003 Patterns of rarity inmosses of the Okanogan Highlands of WashingtonState An emerging coarse filter approach to rare mossconservation THE BRYOLOGIST 106 34ndash52

HERBEN T 1994 Local rate of spreading and patch dy-namics of an invasive moss species Orthodontium li-neare Journal of Bryology 18 115ndash125

HODGETTS N G 1992 Measures to protect bryophytes inGreat Britain Biological Conservation 59 259ndash264

HOLT R D J H LAWTON K J GASTON amp T M BLACK-BURN 1997 On the relationship between range sizeand local abundance back to basics Oikos 78 183ndash190

HORTON D G 1983 A revision of the Encalyptaceae(Musci) with particular reference to the North Amer-ican taxa Part II Journal of the Hattori Botanical Lab-oratory 54 353ndash532

mdashmdashmdash 1988 Microhabitats of new world Encalyptaceae(Bryopsida) distribution along edaphic gradientsBeiheft zur Nova Hedwigia 90 261ndash282

IMURA S 1994 Vegetative diaspores in Japanese mossesJournal of the Hattori Botanical Laboratory 77 177ndash232

JONSSON B G 1993 The bryophyte diaspore bank and


its role after small-scale disturbance in a boreal forestJournal of Vegetation Science 4 819ndash826

KARRON J D 1987 A comparison of levels of geneticpolymorphism and self-compatibility in geographical-ly restricted and widespread plant congeners Evolu-tionary Ecology 1 47ndash58

KEEVER C 1957 Establishment of Grimmia laevigata onbare granite Ecology 38 422ndash429

KIMMERER R W 1994 Ecological consequences of sex-ual versus asexual reproduction in Dicranum flagel-lare and Tetraphis pellucida THE BRYOLOGIST 97 20ndash25

mdashmdashmdash amp C C YOUNG 1995 The role of slugs in dis-persal of the asexual propagules of Dicranum flagel-lare THE BRYOLOGIST 98 149ndash153

mdashmdashmdash amp mdashmdashmdash 1996 Disturbance regime and the re-generation niche non-equilibrial coexistence in anepixylic bryophyte community Bulletin of the TorreyBotanical Club 123 16ndash24

KOOIJMAN A M 1992 The decrease of rich fen bryo-phytes in the Netherlands Biological Conservation 59139ndash143

LAAKA-LINDBERG S T A HEDDERSON amp R E LONGTON2000 Rarity and reproductive characters in the Britishhepatic flora Lindbergia 25 78ndash84

mdashmdashmdash H KOPELAINEN amp M POHJAMO 2003 Dispersalof asexual propagules in bryophytes Journal of theHattori Botanical Laboratory 93 319ndash330

LEE J A amp S J M CAPORN 1998 Ecological effects ofatmospheric reactive nitrogen deposition on semi-nat-ural terrestrial ecosystems New Phytologist 139 127ndash134

LEVIN D A 1993 Local speciation in plants the rule notthe exception Systematic Botany 18 197ndash208

mdashmdashmdash 2000 The Origin Expansion and Demise ofPlant Species Oxford University Press Oxford

LI YENHUNG amp D H VITT 1994 The dynamics of mossestablishment temporal responses to nutrient gradi-ents THE BRYOLOGIST 97 357ndash364

mdashmdashmdash amp mdashmdashmdash 1995 The dynamics of moss estab-lishment temporal responses to a moisture gradientJournal of Bryology 18 677ndash687

LLORET F 1991 Population dynamics of the corprophil-ous moss Tayloria tenuis in a Pyrenean forest Hol-arctic Ecology 14 1ndash8

LONGTON R E 1992a Reproduction and rarity in Britishmosses Biological Conservation 59 89ndash98

mdashmdashmdash 1992b The role of bryophytes and lichens in ter-restrial ecosytems Pp 32ndash76 In J W Bates amp A MFarmer (eds) Bryophytes and Lichens in a ChangingEnvironment Oxford University Press New York

mdashmdashmdash 1994 Reproductive biology in bryophytes thechallenge and the opportunities Journal of Hattori Bo-tanical Laboratory 76 159ndash172

mdashmdashmdash amp T A HEDDERSON 2000 What are rare speciesand why conserve them Lindbergia 25 53ndash61

mdashmdashmdash amp R M SCHUSTER 1983 Reproductive biologypp 386ndash462 In R M Schuster (ed) New Manual ofBryology Vol 1 Hattori Botanical Laboratory Ni-chinan

MARINO P 1991 Competition between mosses (Splach-naceae) in patchy habitat Journal of Ecology 791031ndash1046

MCDANIEL S F amp A J SHAW 2003 Phylogeographicstructure and cryptic speciation in the trans-Antarcticmoss Pyrrhobryum mnioides Evolution 57 205ndash215

MILES C J amp R E LONGTON 1990 The role of sporesin reproduction in mosses Botanical Journal of theLinnean Society 104 149ndash173

MISHLER B D amp A E NEWTON 1988 Influences of ma-ture plants and desiccation on germination of sporesand gametophyte fragments of Tortula Journal ofBryology 15 327ndash342

MURRAY B R amp B J LEPSCHI 2004 Are locally rarespecies abundant elsewhere in their geographicalrange Austral Ecology 29 287ndash293

mdashmdashmdash P H THRALL A M GILL amp A B NICOTRA 2002How plant life-history and ecological traits relate tospecies rarity and commonness at varying spatialscales Austral Ecology 27 291ndash310

NATURE SERVE 2005 Compilation of listed species web-site httpwwwnatureserveorg

NEWTON A E amp B D MISHLER 1994 The evolutionarysignificance of asexual reproduction in mosses Jour-nal of the Hattori Botanical Laboratory 76 97ndash103

OrsquoCONNOR R J 1987 Organization of avian assemblag-esmdashthe influence of intraspecific habitat dynamics pp163ndash183 In J H R Gee amp P S Giller (eds) Orga-nization of communities past and present BlackwellScientific Publications Oxford

OslashKLAND R H 1995 Population biology of the clonalmoss Hylocomium splendens in Norwegian borealspruce forests 1 Demography Journal of Ecology 83697ndash712

mdashmdashmdash 2000 Population biology of the clonal moss Hy-locomium splendens in Norwegian boreal spruce for-ests 5 Vertical dynamics of individual shoots Oikos88 449ndash469

ORIANS G H 1997 Evolved consequences of rarity pp190ndash209 In W E Kunin amp K J Gaston (eds) TheBiology of Rarity Chapman amp Hall London

PAOLILLO D J 1981 The swimming sperm of land plantsBioScience 31 367ndash373

PEARCE I S K amp R VAN DER WAL 2002 Effects ofnitrogen deposition on growth and survival of mon-tane Racomitrium lanuginosum heath Biological Con-servation 104 83ndash89

PERSSON H 1956 Studies in the lsquolsquocopper mossesrsquorsquo Jour-nal of the Hattori Botanical Laboratory 17 1ndash18

PHARO E J amp A J BEATTIE 2001 Management of foresttypes as a surrogate for vascular plant bryophyte andlichen diversity Australian Journal of Botany 49 23ndash30

POHJAMO M amp S LAAKA-LINDBERG 2004 Reproductivemodes in the epixylic hepatic Anastrophyllum heller-ianum Perspectives in Plant Ecology Evolution andSystematics 6 159ndash168

PRESTON F W 1948 The commonness and rarity of spe-cies Ecology 29 254ndash283

RABINOWITZ D 1981 Seven forms of rarity pp 205ndash217In H Synge (ed) The Biological Aspects of RarityJohn Wiley amp Sons New York

ROADS E amp R E LONGTON 2003 Reproductive biologyand population studies in two annual shuttle mossesJournal of the Hattori Botanical Laboratory 93 305ndash318

RYDGREN K amp R H OslashKLAND 2003 Short-term costs ofsexual reproduction in the clonal moss Hylocomiumsplendens THE BRYOLOGIST 106 212ndash220

RYDIN H 1986 Competition and niche separation inSphagnum Canadian Journal of Botany 64 1817ndash1824

mdashmdashmdash 1997 Competition among bryophytes Advancesin Bryology 6 135ndash168

SASTAD S M H K STENoslashIEN K I FLATBERG amp S BAK-KEN 2001 The narrow endemic Sphagnum troende-lagicum is an allopolyploid derivative of the wide-


spread S balticum and S tenellum Systematic Botany26 66ndash74

SCHOFIELD W B amp H A CRUM 1972 Disjunctions inbryophytes Annals of the Missouri Botanical Garden59 174ndash202

SCHOENER T W 1987 The geographical distribution ofrarity Oecologia 74 161ndash173

SHAW A J 1981 Ecological diversification among ninespecies of Pohlia (Musci) in western North AmericaCanadian Journal of Botany 59 2359ndash2378

mdashmdashmdash 1993 Population biology of the rare copper mossScopelophila cataractae American Journal of Botany80 1034ndash1041

mdashmdashmdash 1995 Genetic biogeography of the rare copper-moss Scopelophila cataractae (Pottiaceae) Plant Sys-tematics and Evolution 197 43ndash58

mdashmdashmdash 2000 Molecular phylogeography and crypticspeciation in the mosses Mielichhoferia elongata andM mielichhoferiana (Bryaceae) Molecular Ecology9 595ndash608

mdashmdashmdash 2001 Biogeographic patterns and cryptic speci-ation in bryophytes Journal of Biogeography 28 253ndash261

mdashmdashmdash S F MCDANIEL O WERNER amp R M ROS 2002New frontiers in bryology and lichenology Phylo-geography and phylodemography THE BRYOLOGIST

105 373ndash383mdashmdashmdash amp R E SCHNEIDER 1995 Genetic biogeography

of the rare copper moss Mielichhoferia elongata (Bry-aceae) American Journal of Botany 82 8ndash17

SLACK N G 1990 Bryophyte and ecological niche the-ory Botanical Journal of the Linnean Society 104187ndash213

mdashmdashmdash 1992 Rare and endangered bryophytes in NewYork state and eastern United States current status andpreservation strategies Biological Conservation 59233ndash241

mdashmdashmdash 1997 Niche theory and practice bryophyte stud-ies Advances in Bryology 6 169ndash204

SODERSTROM L 1989 Regional distribution patterns ofbryophyte species on spruce logs in northern SwedenTHE BRYOLOGIST 92 349ndash355

STEBBINS G L 1980 Rarity of plant species a syntheticviewpoint Rhodora 82 77ndash86

STENoslashIEN H K amp K I FLATBERG 2000 Genetic vari-ability in the rare Norwegian peat moss Sphagnumtroendelagicum THE BRYOLOGIST 103 794ndash801

STIEPERAERE H O HEYLEN amp N PODOOR 1997 Differ-ences in species composition of the bryophyte layerof some Belgian and Dutch pinewoods with and with-out the invading hepatic Lophocolea semiteres(Lehm) Mitt Journal of Bryology 19 425ndash434

STORCH D amp K J GASTON 2004 Untangling ecologicalcomplexity on different scales of space and time Ba-sic and Applied Ecology 5 398ndash400

TARVAINEN O A M MARKKOLA amp R STROMMER 2003Diversity of macrofungi and plants in Scots pine for-ests along an urban pollution gradient Basic and Ap-plied Ecology 4 547ndash556

THOMAS P A M C F PROCTOR amp E MALTBY 1994The ecology of severe moorland fire on the North YorkMoors chemical and physical constraints on moss es-

tablishment from spores Journal of Ecology 82 457ndash474

THOMPSON K K J GASTON amp R S BAND 1999 Rangesize dispersal and niche breadth in the herbaceous flo-ra of central England Journal of Ecology 87 150ndash155

mdashmdashmdash J G HODGSON amp K J GASTON 1998 Abun-dance-range size relationships in the herbaceous floraof central England Journal of Ecology 86 439ndash448

TOOREN B F VAN amp H J DURING 1988a Early succes-sion of bryophyte communities on Dutch forest earth-banks Lindbergia 14 40ndash46

mdashmdashmdash amp mdashmdashmdash 1988b Viable plant diaspores in theguts of earthworms Acta Botanica Neerlandica 37181ndash185

VITT D H 1991 Distribution patterns adaptive strate-gies and morphological changes of mosses along ele-vational and latitudinal gradients on South Pacific is-lands pp 205ndash233 In P L Nimis amp T J Crovello(eds) Quantitative approaches to phytogeographyKluwer Academic Publishers Dordrecht

mdashmdashmdash amp R J BELLAND 1997 Attributes of rarity amongAlberta mosses patterns and predictions of species di-versity THE BRYOLOGIST 100 1ndash12

WATSON M A 1981 Chemically mediated interactionsamong juvenile mosses as possible determinants oftheir community structure Journal of Chemical Ecol-ogy 7 367ndash376

WIKLUND K 2003 Phosphorus concentration and pH indecaying wood affect establishment of the red-listedmoss Buxbaumia viridis Canadian Journal of Botany81 541ndash549

mdashmdashmdash amp H RYDIN 2004 Ecophysiological constraintson spore establishment in bryophytes FunctionalEcology 18 907ndash913

WITTE J-P M amp P J J F TORFS 2003 Scale dependencyand fractal dimension of rarity Ecography 26 60ndash68

WOOLGROVE C E amp S J WOODIN 1996 Effects of pol-lutants in snowmelt on Kiaeria starkei a characteristicspecies of late snowbed bryophyte dominated vege-tation New Phytologist 133 519ndash529

WYATT R 1992 Conservation of rare and endangeredbryophytes input from population genetics BiologicalConservation 59 99ndash107

mdashmdashmdash amp L E ANDERSON 1984 Population genetics ofbryophytes in relation to their reproductive biologypp 39ndash64 In A F Dyer amp J G Duckett (eds) Theexperimental biology of bryophytes Academic PressLondon

ZAMFIR M amp D E GOLDBERG 2000 The effects of initialdensity on interactions between bryophytes at individ-ual and community levels Journal of Ecology 88243ndash255

ZANTEN B O VAN 1978 Experimental studies on trans-oceanic long-range dispersal of moss spores in theSouthern Hemisphere Journal of the Hattori BotanicalLaboratory 44 455ndash482

mdashmdashmdash amp S R GRADSTEIN 1988 Experimental dispersalgeography of neotropical liverworts Beihefte zurNova Hedwigia 90 41ndash94

mdashmdashmdash amp T POCS 1981 Distribution and dispersal ofbryophytes Advances in Bryology 1 479ndash562

ms received March 7 2005 accepted June 17 2005

0007-274505$1450

The Bryologist 108(4) pp 554 566Copyright q 2005 by the American Bryological and Lichenological Society Inc

Patterns Hypotheses and Processes in the Biology of Rare Bryophytes

NATALIE L CLEAVITT

Department of Natural Resources Cornell University Ithaca NY 14853-3001 USA e-mail nlc4cornelledu

Abstract Dominant patterns and processes in rare bryophyte ecology are presented withinthe framework of current rarity theory Available evidence suggests that bryophyte conservationshould primarily consider the importance of establishment and habitat requirements for rarespecies Preservation of rare and high quality habitats is essential Future understanding of causesof rarity in bryophytes will benefit most by exploring the ecological drivers that allow species toexpand their ranges Comparisons of rare-common congeners rare species throughout their range(not only where they are rare) and species currently experiencing range expansions or contrac-tions are likely to yield the most robust and relevant data sets

Keywords Moss liverwort dispersal management rarity ecological limitations

Rare bryophyte species are receiving increasedattention as the negative impacts on bryophytesfrom air pollution (Lee amp Caporn 1998 Pearce ampvan der Wal 2002 Tarvainen et al 2003 Wool-grove amp Woodin 1996) eutrophication (Drexler ampBedford 2002 Kooijman 1992) and forestry man-agement (Fenton amp Frego 2005 Frisvoll amp Prestoslash1997 Hazell amp Gustafsson 1999) become clearGeneral under-documentation of occurrences forbryophyte species in many parts of the world re-sults in a data deficit that often makes designationof bryophyte species difficult As a consequenceconservation of bryophyte species is mainly inci-dental and occurs through preservation of habitatfor other reasons Previous papers focusing on rar-ity in bryophytes have largely focused on specificpatterns relating to rare species (eg Laaka-Lind-berg et al 2000 Longton 1992a Longton amp Hed-derson 2000 Vitt amp Belland 1997) and on discus-sions of rare bryophyte conservation efforts (egBisang amp Hedenas 2000 Hodgetts 1992 Slack1992) In this paper I present an overview of rarebryophyte ecology by synthesizing what we knowof the patterns associated with rarity and by con-sidering the available literature on rare bryophyteswithin the framework of current rarity theory

The question lsquolsquoWhat is rarityrsquorsquo can be quitecomplex but in practice the vulnerability of a spe-cies is generally assigned based upon the numberof known occurrences in a given area and the per-ceived population threats associated with extinctionrisk (eg Church et al 2001 Nature Serve 2005)These ranks can be given at several scales typi-cally stateprovincial national and global In thecase of the British Red List for mosses and liver-worts rankings may also take into account popula-tion size or changes in the number of occupied sites

over time (Church et al 2001) In North Americawe lack the detailed baseline information requiredto include these other important criteria into ourranking system Indeed under-collection and datadeficiency in the case of bryophytes continues tobe a problem in assessing the rarity of these organ-isms in North America (Slack 1992)

When we rank species we are almost always re-ferring to morphologically delimited species Inbryophytes where cryptic speciation (genetic iso-lation of morphologically uniform populations)may be common there is an added complication todelineating rare species (Feldberg et al 2004McDaniel amp Shaw 2003 Shaw 2000 2001 Wyatt1992)

Once we do designate species as rare in an areawe often want to understand the types of rare spe-cies Rabinowitz (1981) proposed what has becomethe most widely cited classification of rare plantsbased on abundance range size and habitat speci-ficity Birks et al (1998) examined moss and liv-erwort species of the British flora in relation to Ra-binowitzrsquos (1981) classification and concluded thatlsquolsquomost bryophyte species are not common andmany have a narrow habitat specificityrsquorsquo Classifi-cation of bryophytes into Rabinowitzrsquos (1981) cat-egories emphasizes the diversity of rare species butalso pinpoints a key problem in quantifying raritythat is rarity is relative rather than absolute If thesame quantitative limits are used for all plants todifferentiate lsquolsquosmallrsquorsquo and lsquolsquolargersquorsquo range size orlsquolsquobroadrsquorsquo and lsquolsquonarrowrsquorsquo habitat specificity thenbryophyte species generally considered commonwithin the bryophytes may be rare by objective cri-teria for all plants In addition even within thebryophytes setting objective limits for these sub-






PATTERNS









































































CONCLUDING REMARKS




ACKNOWLEDGMENTS



LITERATURE CITED























































































































































PATTERNS









































































CONCLUDING REMARKS




ACKNOWLEDGMENTS



LITERATURE CITED























































































































































































































CONCLUDING REMARKS




ACKNOWLEDGMENTS



LITERATURE CITED
















































































































































































































CONCLUDING REMARKS




ACKNOWLEDGMENTS



LITERATURE CITED








































































































































































































CONCLUDING REMARKS




ACKNOWLEDGMENTS



LITERATURE CITED















































































































































































CONCLUDING REMARKS




ACKNOWLEDGMENTS



LITERATURE CITED








































































































































































CONCLUDING REMARKS




ACKNOWLEDGMENTS



LITERATURE CITED


































































































































































CONCLUDING REMARKS




ACKNOWLEDGMENTS



LITERATURE CITED




























































































































































CONCLUDING REMARKS




ACKNOWLEDGMENTS



LITERATURE CITED




















































































































































CONCLUDING REMARKS




ACKNOWLEDGMENTS



LITERATURE CITED


















































































































































































































































































































































































































Documents

Patterns, Hypotheses and Processes in the Biology of Rare Bryophytes