Allelopathy in bryophytes - a review

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Allelopathy in bryophytes - a review
Author(s): James Whitehead, Maria Wittemann and Nils Cronberg
Source: Lindbergia, 41(1)
Published By: Dutch Bryological and Lichenological Society and Nordic Bryological Society
https://doi.org/10.25227/linbg.01097
URL: http://www.bioone.org/doi/full/10.25227/linbg.01097
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1
e plants collectively known as ‘bryophytes’, i.e. mosses
(phylum Bryophyta), liverworts (phylum Marchantiophyta)
and hornworts (phylum Anthocerotophyta) comprise
the second largest group of plants after the angiosperms
(Nozakietal. 2007). Derived from algal ancestors, they rep-
resent the earliest divergent phylogenetic branches among
terrestrial plants. As the rst inhabitants of terrestrial habi-
tats they were by default growing on bare ground or rock and
many species are still primary or secondary colonizers. eir
ancestors have been ghting for space for hundreds of mil-
lions of years, resulting in mechanisms which have evolved
for both exploitive competition (monopolization of light
and nutrients) and interference competition (by chemical
warfare). In general, bryophytes display a low morphologi-
cal complexity, but a high degree of chemical diversication
(Huneck 1983, Asakawaetal. 2013), suggesting that sec-
ondary substances may play an important role in plant-to-
plant interactions. Since bryophytes are abundant in many
ecosystems, it is vital to understand how their production
of allelopathic substances may inuence the composition of
communities.
e term ‘allelopathic chemical’ refers to certain second-
ary metabolites in plants, algae, bacteria, coral and fungi that
are not required for basic metabolism. Such chemicals play
important roles in defense against herbivory, plant–microbe
relations and – as in the case of allelopathy – competition
with other plants (Willis 2007). It should be noted that alle-
lopathic impacts upon lichens are beyond the remit of this
paper. e competitive advantages of allelopathy aect spe-
cies distributions, in extreme cases leading to dominance
of a single species in a natural ecosystem or contributing to
the invasive potential of introduced species (Koochekietal.
2013). is might explain the dominance of bryophytes over
vascular plants under certain conditions (Kato-Noguchi and
Seki 2010).
Allelopathic interactions have been studied in vascular
plants since the beginning of the 20th century, while the
rst studies of allelopathic chemicals in bryophytes followed
several decades later (Watson 1981). Several substances iso-
lated from liverworts were shown to be phytotoxic, inhibit-
ing germination and growth of vascular plants in standard
lab tests (Huneck 1983, Asakawa 1982, 1990, 1995, 2007).
is toxicity inspired the search for economically valuable
compounds, such as antitumor agents (Spjutetal. 1986) or
natural sources of herbicides (Nozakietal. 2007). In this
review we focus on bryophyte–vascular plant and bryophyte–
bryophyte allelopathic interactions and how such interac-
tions may inuence recruitment, competition and ultimately
plant community assembly.
Methodology
e search for literature was non-systematic, but nonethe-
less comprehensive, using bibliographic data-bases includ-
ing Google Scholar and Web of Science. In a second step,
reference lists of retrieved articles were scanned, as well as
manuals of bryophyte chemistry such as Huneck (1983) and
Asakawa (1995, 2007) and Asakawaetal. (2013). e litera-
ture included in the review had to fulll the conditions of
treating the subject of both bryophytes and allelopathy in a
wide sense (including phytotoxicity).
Allelopathy in bryophytes – a review
JamesWhitehead, MariaWittemann and NilsCronberg
J. Whitehead and N. Cronberg, Dept of Biology, Lund Univ., Lund, Sweden. – M. Wittemann (maria.wittemann@bioenv.gu.se), Dept of
Biological and Environmental Sciences, Box 463, SE-405 30 Göteborg, Sweden.
Allelopathy in bryophytes shapes ecosystems by inuencing the species composition of both vascular plants and other bryo-
phytes. Several allelopathically active chemicals in bryophytes have been discovered since the latter half of the 20th century
and laboratory studies have showed their inhibiting impact on germination, growth and establishment of surrounding
plants. However, other studies failed to demonstrate these eects. In the eld, other properties of bryophytes might have
stronger impacts, such as mechanical obstruction or alterations in temperature. In laboratory studies, water might not be an
adequate extractant for active substances, since all of the chemicals claimed to be allelopathic are lipophilic with potentially
longer retention times of the active substances in the soil when compared to water-soluble substances.
Lindbergia 41: linbg.01097, 2018
doi: 10.25227/linbg.01097
© 2018 e Authors. is is an Open Access article
Editor-in-Chief: Nils Cronberg. Accepted 8 December 2017
is work is licensed under the terms of a Creative Commons
Attribution 4.0 International License (CC-BY)  http://
creativecommons.org/licenses/by/4.0/ . e license permits
use, distribution and reproduction in any medium, provided the
original work is properly cited.

2
Pioneering observations during exploration of
bryophyte secondary chemistry
Early studies focused on the detection of the chemical
nature of allelochemicals. In a series of bioassays Huneck
and Schreiber (1972) tested the eects of secondary sub-
stances derived from liverworts (gymnocolin, drimenol, lon-
giborneol, longifolen, lunularic acid and scapanin; Table1.)
on the growth of Lepidium sativum L. (cress) roots, Avena
sativa L. (oat) seedlings and oat coleoptiles. Growth was
compared against controls with no substance added. ey
found that some substances consistently either decreased or
increased the growth relative to controls. Other substances
decreased growth in high concentration (10–3 M) but pro-
moted growth in lower concentrations. e eects of the
substances were not consistent across assays. For example,
the inhibitory eects on growth were more pronounced for
cress than for the other assays, and some substances had
inhibitory eect on cress growth, but promoted growth of
oats, relative to the control. Several other substances have
been subject to standard assays in vitro, which suggest more
or less strongly inhibitory eects. For example, several ses-
quiterpene lactones extracted from the thalloid liverwort
Conocephalum conicum displayed complete inhibitory activ-
ity towards germination and growth of rice at concentra-
tions down to 50–200 ppm (Asakawa and Takemoto 1979).
e sesquiterpenoid (+)-vitrenal isolated from the liverwort
Lepidozia vitrea inhibited growth of leaves and roots on
Oryza sativa L. (rice) seedlings at a concentration of 25 ppm
(Matsuoet al. 1980). Asakawa (1995) showed inhibitory
eects of isobicyclogermacrenal, lepidozanal and (+)-vitre-
nal on rice seedling growth. In a later manual (2007), he
even went as far as to state that almost all crude extracts
which contain “bitter or pungent” substances also have phy-
totoxic properties. In these early studies the replication is
often poor and the data is tabulated without statistical tests.
e results are accordingly dicult to evaluate, especially
considering that the studies do not yet reveal to what extent
the substances are actually released to the environment in
biologically active concentrations.
Indications of bryophyte–bryophyte interactions
Bryophyte species have been shown to inhibit one another
and also conspecics. A ground-breaking experiment was
undertaken by Watson (1981). Based on eld observations,
she proposed that the distribution of six Polytrichum species
was due to “dierential aggressiveness amongst juveniles”
rather than competition between adults. is motivated her
to sow spores of the moss Funaria hygrometrica at dierent
distances on agar plates to observe protonemal development.
She could see that the developing protonema released a “fac-
tor” that prevented dierent clones of conspecic protonema
to grow into each other. is factor gradually accumulated
with protonemal age and spores sown at the same time in
the same spot were subject to minimal amounts of the sub-
stance and therefore grew normally to form a composite
colony. is was the rst concrete evidence of direct nega-
tive interactions between developing bryophytes, taken as
proof of allelopathy, and the growth factor was identied as
“cytokinin-like”, tentatively called factor H. Little is known
about this factor H and one or more factors with similar
eects may exist (Glime 2015) – few modern comparable
studies have been conducted and the documentation is gen-
erally poor.
In the following years similar in-vitro experiments as well
as eld studies were carried out to explore how widespread
such interactions could be. Sporadic observations summa-
rized in Newton and Mishler (1994) suggested that spores
are prevented from germination in mature moss colonies.
Kimmerer (1991) observed that gemmae and spores of the
fugitive species Tetraphis pellucida Hedw. germinated in
patches of bare decaying wood but not in patches occupied
by the competitors Dicranum agellare Hedw. or Hypnum
imponens Hedw. Longton and Miles (1982) noted that con-
specic spores persisted un-germinated but viable for a year
in cushions of the moss Grimmia pulvinata (Hedw.) Sm.
Cronbergetal. (2006) analyzed the clonal identity of all
shoots in a large colony of Hylocomium splendens (Hedw.)
Schimp. known to have produced spores annually for at
least ve years and found that the whole colony consisted of
Table 1. Examples of allelopathic chemicals in bryophytes. A somewhat larger number of substances have been claimed to have phytotoxic
effects, but we have chosen to include those that have a comparatively solid documentation.
Aromatics Flavonoids vitexin, apigenin, apigenin-7-O-triglycoside,
luteolin-7-O-neohesperidoside, saponarine,
lucenin-2, bartramiaflavone
Basileetal. 2003
Bibenzyl derivative lunularic acid Huneck and Schreiber 1972
Phenolics not specified Soudzilovskaiaetal. 2010
Terpenoids Diterpenoids gymnocolin, scapanin, 16α-kaurenol Huneck and Schreiber 1972
perottetianal Asakawa 1990
momilactone A and B Nozakietal. 2007
Sesquiterpenoids drimenol, longiborneol, longifolene Huneck and Schreiber 1972
Sesquiterpenoids, drimanes polygodial Asakawa 1982, 1990
Sesquiterpenoids germacrane, isobicycliogernacrenal, lepidozane,
lepidozenal, (+)-vitrenal
Ando and Matsuo 1984
Sesquiterpene lactones,
eudesmanolides
guaianolides, deoxyzaluzanin, Asakawa and Takemoto 1979
diplophyllolide, 7α-hydroxydiplophyllolide,
3-oxodiplophyllin, frullanolide
Asakawa 1982, 1990
Sesquiterpene lactones,
germacranolides
zaluzanin C, zaluzanin D, 8α-acetoxyzaluzanin
C, 8α-acetoxyzaluzanin D,
Asakawa 1982, 1990
Sesquiterpene
secoaromadendrane-type
plagiochiline A, plagiochiline C, ovalifolienal,
ovalifolienalone, 9α-acetoxyovalifolienal
Ando and Matsuo 1984
Trinorsesquiterpenoid 3-hydroxy-β-ionone Kato-Noguchi and Seki 2010

3
no more than three clones that were only distantly related.
Spore germination may be prevented because the mature
shoot is monopolizing available nutrients, but several obser-
vations suggest that some form of more advanced chemical
interaction is involved.
In an important study, Mishler and Newton (1988)
documented strong inhibition of both spore germination
and fragment growth in a material consisting of several
species of the genus Tortula (since then transferred to the
genus Syntrichia as S. ruralis (Hedw.) F. Weber & D. Mohr,
S. princeps Mitten, S. norwegica Weber and S. laevipila
Bridel) when applied onto living clumps of either Tortula
itself or onto the unrelated species Dicranum scoparium
Hedw. ey were able to repeat the results when lter-
sterilized water extracts of each species were applied onto
spores on agar. Patterns of inhibition were similar to the
preceding experiment, suggesting that the eects were
mediated by chemical interaction rather than physical
properties of the moss clumps. Attempts to document the
presence of bioactive chemicals by application of substances
dissolved from mature moss shoots on germinating spores
rendered unclear results. is could have several dierent
explanations, amongst them that the chemical leachate may
be labile and have to be produced continuously to exert an
eect (Newton and Mishler1994).
Recent research suggests that bryophytes discriminate
between species in their allelopathic reaction. Many mosses
belonging to several unrelated lineages have a breeding sys-
tem involving tiny dwarf males, which cling onto the shoots
of normal-sized females where they assist in fertilization of
the females. Rosengren and Cronberg (2015) showed by
experimental application of spores that female shoots of the
pleurocarpous moss Homalothecium lutescens allowed ger-
mination and development of dwarf males from conspecic
spores as well as spores of the closely related species H. seri-
ceum (Hedw.) Schimp., whereas spores of the unrelated spe-
cies Isothecium alopecuroides (Dubois) Isov. failed to develop
dwarf males. In theory, this selective development of dwarf
males could be related to e.g. dierences in pH, but more
likely some more complex allelopathic recognition system is
involved. With this breeding system the female is actually
promoting germination of conspecic male spores, in con-
tradiction to the cases cited above which suggest that game-
tophytes in general suppress spore germination whether
conspecic or not.
Experimental studies on bryophyte–vascular plant
interactions
Further investigations of bryophytes showed that allelopathy
targets not only other bryophytes, but also the germination
of seeds of vascular plants (Hein 1966, van Tooren 1990,
Basileet al. 2003, Löbel et al. 2006, Soudzilovskaiaetal.
2010). Many of these studies appear to be triggered by the
search for plants that produce substances that could poten-
tially be used as natural herbicides, e.g. a number of Chinese
articles (reviewed by Liu 2014). e studies are typically
undertaken by soaking bryophytes in water and subject-
ing the seeds to water extracts. In many cases such water
extracts produce results that are dicult to interpret or
counterintuitive.
Huneck and Meinunger (1990) used a very basic
approach. ey added seeds of kress to fresh, moistened
bryophytes (52 mosses and 29 liverworts) and measured the
lengths of the kress roots and shoots after ve days at room
temperature. ey found three dierent kinds of reactions: 1)
bryophytes that promote growth of the shoot, 2) bryophytes
that promote growth of the root and 3) bryophytes that
retard growth of both roots and shoots. Frahmetal. (2012)
noted that there was a risk that the reactions were caused
by microorganism associated with the bryophytes rather
than the bryophytes themselves. To avoid this problem,
they prepared liquid extracts by soaking some bryophytes
(Porella platyphylla, Eurhynchium striatum, Dicranodontium
denudatum and Brachythecium rutabulum in tap water and
distilled water for 12 h prior to germination tests involving
kress and Lactuca sativa (lettuce). e bryophytes had been
stored in a dry condition before the experiment, which may
have inuenced the leaking of substances. Like Huneck and
Meinunger they found indications of both negative and pos-
itive inuence on the germinating seeds, but the eects were
sometimes indierent to variations in concentration of the
extracts. Extracts in distilled water gave the strongest eect,
which was explained by higher dissolving capacity. ey
made a second experiment where they compared extracts
from the liverwort Bazzania trilobata when soaked in water
and in ethanol. ey found somewhat stronger reactions
with ethanol than with water when the same concentrations
were compared.
Yet more sophisticated, Tsubota et al. (2006) used an
assay called the sandwich technique to test Dicranum japoni-
cum, Hypnum plumaeforme, Racomitrium japonicum and
Sphagnum palustre for allelopathic activity at germination of
lettuce seeds. ey dried the moss material either at room
temperature (with silica gel) or at 80°C, ground the dry
mosses to a rough powder and embedded powders of indi-
viduals species within agar in micro-well plates, with a sec-
ond agar layer atop to avoid direct contact between the moss
tissue and the seed. ey found signicantly reduced Lactuca
radicle elongation compared to the control for all species
with exception for R. japonicum, with D. japonicum showing
the strongest eect. Hypocotyl elongation was unaected or
promoted for all species with exception for D. japonicum,
which again showed a strong inhibitory eect. e eects
(positive or negative) were in general somewhat stronger for
replicates dried by silica gel as compared to replicates dried
in 80°C, suggesting that potential allelopathic substances
were mildly sensitive to heat.
Basileet al. (2003) studied the impacts of gametophyte
extracts of the moss Tortula muralis upon conspecic spore
germination and protonemal development as well as on
seed germination and root development of the angiosperm
Raphanus sativus L. Seven avonoids were extracted (Table 1)
and it was found that each one of these induced a slow-down
of the growth of Tortula and a signicant decrease in germi-
nation percentage of its spores. Interestingly, both of these
inuences were found to be dosage dependent. Other signs
of retarded protonemal growth occurred in relation to avo-
noid presence; swollen tips as well as swollen and shortened
intercalary cells were seen, particularly during the rst days
of culture. Early occurrence of brood cells on protonemal
laments, a common response to environmental stress, was

4
also seen in Tortula. Similar to Tortula, the percentage of R.
sativus seeds germinating was reduced by avonoid presence.
Root elongation and root hair growth were also inhibited,
with the avonoid saponarin having the most dramatic
eect.
Highlighting specific bioactive substances
Over time research progressed from mostly eect-oriented
studies to characterizing the chemicals. e rst allelochemi-
cal compounds to be described in mosses were claimed to be
the terpenes momilactone A and B in a study by Nozakietal.
(2007; Table 1). Momilactone A and B were previously
known as allelopathic chemicals from Oryza sativa (rice).
Nozakiet al. realized that H. plumaeforme, like liverworts,
contains oil bodies in the leaf cells, while mosses at this point
were thought to be devoid of distinct oil bodies. is led
them to examine inhibitory eects of ethyl acetate extracts of
Hypnum plumaeforme on dierent plant species (Arabidopsis
thaliana (L.) Heynh., Nicotiana tabacum L., Jungermannia
subulata A. Evans, Physcomitrella patens (Hedw.) Bruch &
Schimp. and H. plumaeforme itself) and comparing them
with the eects of momilactone B. Both extracts and momi-
lactone B showed inhibition of other species, but not of
H. plumaeforme itself, pointing explicitly to an allelochemi-
cal eect of momilactone B.
Sharmaetal. (2009) used aqueous and two dierent lipo-
philic extracts of eight bryophytes in order to nd out more
about the chemical nature of allelochemicals. e studied
bryophytes were Targionia hypophylla, Marchantia polymor-
pha, Plagiochasma appendiculatum, Brachythecium bucha-
nanii, Leucodon secundus, Timmiella anomala, Rhodobryum
roseum and Plagiomnium integrum, the eected plant was
Bidens biternata (Lour.) Merr. & Sherrif. ey found that
inhibition of germination of the vascular plant was stron-
gest in methanol extract, followed by acetone extract, while
eects of the aqueous extract were minor. e lack of hydro-
philic allelochemicals is surprising at rst as the chemicals
could be released (via volatilization, leaching, decomposition
of residues and root exudation) far more easily if they were
hydrophilic (Sharmaetal. 2009). However, they would also
leach faster from the soil, which could be a possible disad-
vantage for the allelopathic activity and thus an explanation
for their hydrophobic chemical nature.
3-hydroxy-β-ionone was stated to be another allelopathi-
cally active chemical. Rhynchostegium pallidifolium inhibited
cress grown on agar medium stronger at close proximity to
the moss tissue than at a more remote position. is corre-
lates with higher values of 3-hydroxy-β-ionone closer to the
moss tissue (Kato-Noguchi and Seki 2010). Furthermore,
3-hydroxy-β-ionone applied exogenously showed inhibitory
eects on cress. is suggests that the chemical is in fact alle-
lopathically active.
Relating allelopathy to ecological aspects
Recent research brought progress in connecting eects of
chemical compounds in bryophytes to ecological aspects.
Van Tooren (1990) found that the numbers of emerg-
ing seedlings of angiosperms were reduced up to 30% in
the presence of a bryophyte layer, both in eld conditions
and under controlled conditions in a greenhouse. is result
could partially be explained by changed light environment
in the moss carpet, increased risk for mortality of seed due to
fungal infections or monopolization of nutrients by the high
ion exchange capacity of bryophytes. However, allelopathic
interaction was put forward as a supplementary explanation.
When studying the regeneration niche of Pinus sylvestris
(Scots pine) in boreal forest, Steijlenet al. (1995) found
reduced recruitment from seeds in sites dominated by Pleu-
rozium schreberi as compared to sites dominated by Cladina
spp. In a follow-up lab experiment they found observed sig-
nicant inhibition of P. sylvestris seeds when grown in petri
dishes in contact with living shoots of P. schreberi. However,
this eect was lost when pre-germinated seedlings (with
1-mm radicles) were tested and when they attempted to
germinate seeds with water extracts from the moss. ey
interpreted that the negative inuence of P. schreberi is a
combined eect of moisture factors, chemical interaction
and its ability to monopolize nutrients.
One important aspect of allelopathy is the way in which
it is modied by environmental variation. Löbeletal. (2006)
observed at periodically dry grasslands on Öland an increase in
species richness of bryophytes at the expense of vascular plant
cover. Of course, this may have been due simply to environmen-
tal conditions favouring bryophytes, but some further evidence
pointed to stronger eects of allelopathy under dry conditions.
Zamr (2000) investigated the way in which environmental
variation inuenced the germination of seeds in ‘bryophyte
carpets’ in a series of greenhouse experiments. Despite some-
what varying results, Zamr concluded that there was a general
trend towards bryophyte mats inhibiting seedling emergence
of some grassland species (particularly Veronica), this tendency
being exaggerated under dry conditions. Although these nd-
ings were placed in the context of allelopathy, Zamr admits
that the physical properties of the diering substrates may also
have had a large inuence on seed germination. In a contradic-
tion of Zamr’s ndings, Otsus and Zobel (2004) reported a
positive eect of removal of bryophytes on vascular plant ger-
mination only in moister conditions.
Soudzilovskaiaet al. (2010) studied eects of bryophyte
traits, including release of phenolics (in a wide sense), on the
germination of vascular plant seeds. ey focused on dier-
ences between six bryophyte species (Barbilophozia lycopo-
dioides, Ptilidium ciliare, Dicranum scoparium, Hylocomium
splendens, Pleurozium schreberi and Polytrichum strictum) in
their eect on 10 vascular plant species (Dryas octopetala L.,
Empetrum nigrum L., Vaccinium myrtillus L., Betula pubescens
Erh., Pinus sylvestris, Epilobium angustfolium L., Silene dio-
ica (L.) Clairv., Solidago virgaurea L., Carex rostrata Stokes
and Deschampsia exuosa (L.) Trin.) from a subarctic heath-
woodland. In a eld experiment, they collected cushions of
the bryophyte species, replanted them and sowed seeds of the
dierent species of vascular plants under the moss cushions.
A laboratory experiment accompanied the eld experiment,
growing the bryophytes on glass ber lters and analyzing the
lters for total phenolic content using the Fiolin–Ciocalteu
method. In the laboratory experiment they found that germi-
nation of vascular plants diered between bryophyte species
and was reduced in relation to concentrations of phenolics.
Bryophytes suppressed germination also in the eld experi-
ment, but not in relation to concentration of phenolics since

5
no dierence was found between bryophytes species. e dif-
ferences in seed germination were actually best explained by
early spring soil temperature mediated by the insulating eect
of bryophyte mats and their thicknesses. e discrepancy
between the laboratory study and the eld study regarding the
phenolics may partially be explained by dierent approaches
to collect the phenolic substances and possible degradation
occurring in the eld experiment. e authors highlight the
diculties of drawing conclusions about complex ecological
processes based solely on laboratory experiments.
Lettetal. (2017) used the same Fiolin–Ciocalteu method
to estimate total content of phenols in eight bryophytes in
a study which compared performance of young seedlings
of pine and birch under conditions simulating temperature
conditions at the alpine tree line in current (7.0°C) and near
future expected (9.2°C) temperature averages. ey found
that the amounts of phenols in water extracts from the bryo-
phytes diered signicantly between species with the highest
amounts measured in Pleurozium schreberi and Hylocomium
splendens. However, the variation was uncorrelated (birch)
or positively correlated (pine) with the response variables
(biomass, N-uptake), especially at the higher temperature. If
anything a high content of phenols seemed to favour seed-
ling growth, but other bryophyte traits appeared to be more
important, similar to the conclusions in Soudzilovskaiaetal.
(2010). e authors noted that seedlings and seeds might
respond dierently to bryophyte traits.
Michel et al. (2011) could connect the eect of bryo-
phyte chemicals on vascular plants shown in a laboratory
experiment to eld conditions. ey tested the eects of 17
species of bryophytes (Supplementary material Appendix 1
Table A1) on three species of vascular plants (Lactuca sativa,
Melicytus ramiorus J. R. Forst & G. Forst. and Fuchsia
excorticate (J. R. Forst & G. Forst) L.f.). Leachates soluble
in water were obtained from dried bryophytes and their
inuences on seed germination and seedling growth were
measured. e inuence of the leachates was very variable
between the three vascular plant species. e impact on seed
germination ranges from minor (L. sativa) to both stimu-
latory and inhibitory depending on the bryophyte species
(M. ramiorus) and inhibitory eects (F. excorticata). Radicle
growth was inhibited in all three species, but for L. sativa
only after reaching a critical concentration of bryophyte
leachates. In the eld, patterns of seedling occurrence were
investigated. ey found that seedling density on bryophyte
cushions varied between the bryophyte species being lowest
in stands of Dendrohypopterygium liculiforme. Micheletal.
related their observations to allelopathy, however, they failed
to take other properties of bryophytes into account as done
by Soudzilovskaiaetal. (2010).
Ingerpuu and Vellak (2013) investigated interspecic
impacts in growth and morphology among three Sphagnum
species S. magellanicum, S. teres and S. wulanum. Only S.
wulanum showed signicant changes in its morphology
when grown together with neighbours (reduced height,
higher weight, smaller capitula, and a denser branch arrange-
ment). e authors came to the conclusion that this response
is non-adaptive as the altered morphology conveyed no com-
petitive advantage. A low competitive strength might explain
the rarity of this moss; even in suitable habitats it has a sparse
distribution. ey discuss that this observation may explain
why some bryophytes (such as S. wulanum) with a wide
distribution range are still restricted to a few places within
their respective ranges.
Buetal. (2017) examined three common peatland moss
species from the northern hemisphere; Polytrichum strictum,
Sphagnum palustre and S. magellanicum. Polytrichum strictum
is showing an increased presence in peatlands in China. ey
aimed to discover whether this was due to higher initial ger-
mination rates, or to allelopathy. In a laboratory experiment
spores were stored in hummocks of all other mosses, after
which germination success was assessed. ey conclude that it
was indeed allelopathy that conveyed the competitive advan-
tage for two reasons. Firstly, P. strictum was found to be highly
allelopathic, to the extent that even its own spores grow bet-
ter in Sphagnum hummocks than in P. strictum hummocks.
Secondly, P. strictum showed lower germination rates than
S. palustre. It should however be considered that P. strictum
produces more spores than S. paulstre and S. magellanicum.
Sphagnum magellanicum was shown to have the weakest allelo-
pathic eect of the three. Buetal. (2017) also investigated the
eect of the water table upon germination, higher germina-
tion was found in the treatment with lower water availability.
ey suggest one possible explanation for this could be that
allelopathic impacts are reduced in dryer conditions. is has
interesting implications for future peatland development as
many peatlands face water loss due to climate change.
Discussion
e impact of allelopathy on ecosystems is important to
understand when assessing species distribution and competi-
tive interactions. Despite this, there is still much work to be
done on understanding to what extent allelopathic chemicals
in bryophytes exert a relevant impact in the eld. Although
there are many other factors that inuence the competitive
ability of a plant species, it does not take long to nd stud-
ies where the impact of allelopathic chemicals is neglected.
For example, Rydin (1997) used morphological traits such as
shoot size, shoot density and branching type to explain how
dierent Sphagnum species became dominant under various
environmental conditions. In the light of ndings such as
those of Watson (1981) about allelopathic interactions upon
moss recruitment or those of Ingerpuu and Vellak (2013)
about interspecic impact on morphology in peat mosses,
it seems possible that elements of interference competi-
tions through allelopathy is equally important as the more
apparent and experimentally tractable eects of exploitation
competition. Vice versa, the ignoring of certain factors in
laboratory experiments decreases the use of the ndings in
the eld. For example Micheletal. (2011) claim to be able
to relate their results from the laboratory to eld conditions,
however they did not take into account the mechanical and
physical obstructions that bryophyte-cushions can represent
for vascular plant seedlings, such as the eects of tempera-
ture demonstrated by Soudzilovskaiaetal. (2010).
Apart from the study by Huneck and Meinunger (1990) –
which sampled a broad number of species for a rather narrow
experimental scope – a small and strongly taxonomically biased
group of bryophytes have been tested for allelopathy so far
(Supplementary material Appendix 1 Table A1). Forexample,

6
Hypnales, Polytrichales and Sphagnales are overrepresented
in the articles reviewed here. is attention could probably
be explained by the fact that these orders contain many spe-
cies that are dominant in the bottom layer of various habitats.
However, more knowledge about representatives from other
bryophyte lineages could bring interesting new insights and
reveal to what extent the allelopathic substances are unique or
diverse relative to the phylogenetic diversity.
Despite these limitations, a picture of the usage of allelo-
chemicals by bryophytes is starting to emerge. Since the
beginning of research into this topic several chemicals with
eects under lab conditions on both other bryophytes and
vascular plants have been identied. Allelopathic eects could
be induced by hormones or hormone-like substances such
as “factor H” (Watson 1981) that are actively or passively
released to the surroundings. Such substances are likely to
exert a similar inuence on conspecic and alien shoots. More
ecient would be production of substances that are speci-
cally targeted against alien plants, such as in the case of momi-
lactone B and Hypnum plumaeforme (Nozakietal. 2007). At
present, most of the substances claimed to have allelopathic
eects are not known as plant hormones. e fact that some
observations point to a promoting eect in low concentrations
but a retarding or inhibitory eect in high concentrations may
indicate that these substances behave like hormones.
All of the putatively allelochemical substances in the
papers reviewed here are lipophilic and the amounts released
from the plants to the soil can vary with environmental con-
ditions. Otsus and Zobel (2004) suggest that inhibition of
vascular plants by bryophytes is increased by moist condi-
tions. is appears to be contradictory to the ndings of
Löbeletal. (2006) and Zamr (2000) who propose allelopa-
thy is accelerated by drought. However, the eects of the rst
study could be due to non-allelopathic obstructions (with
bryophyte cushions growing bigger and tighter in moist
conditions). Furthermore, the latter found allelopathy to be
exacerbated when followed by heavy rain. Bryophytes are
well known to be poikilohydric (unable to regulate cytosol
water content under dry conditions) and a rain following a
drought episode can wash an excess of secondary chemicals
into the soil (Micheletal. 2011). In the soil the lipophilic
nature of the substances may be advantageous as such sub-
stances are far less mobile than hydrophilic compounds. As a
result they may reside longer in the soil and remain closer to
the releasing plant. From this perspective, it is unfortunate
that it has been common practice to use aqueous extracts
in the assessment of allelopathic chemicals, especially since
Sharma et al. (2009) showed that polarity of the extract-
ing medium actually mattered. Soudzilovskaiaetal. (2010)
found a way to reproduce close-to-natural conditions by
using living plants and collecting the exudates in lters that
they used as substrates for growth. It might be interesting to
try to bring experiment designs even closer to natural condi-
tions by inclusion of variation in water accessibility. Such
experiments might reveal the conditions that promote leak-
age of allelopathic substances.
e research covered in this review is of great potential
practical interest, since observations of bryophyte allelopa-
thy could lead to novel natural herbicides for agricultural
use. To some extent, the optimism in this respect seems to
have faded, herbicidal eects are only briey mentioned in
recent compilations of bryophyte secondary chemistry, e.g.
Asakawaetal. (2013), maybe because of somewhat conict-
ing results and the fact that high and low concentrations of
many substances appear to have divergent eects on growth
of vascular plants. On the other hand, Frahmetal. (2012)
points to another potentially interesting use in the commer-
cial seed industry, in which bryophyte allochemicals may
serve the double function of promoting seed germination
and providing protecting against fungal attack.
An area not covered in this review is the growing evidence
that bryophyte growth and development is inuenced by
symbiotic or otherwise associated fungi and other microor-
ganisms. It should be noted that such hidden interactions
could have profound eects on experimental studies. To con-
trol for this, it is necessary to perform experiments under
axenic conditions, which is tractable for bryophytes since
sterile cultures are possible to obtain from surface-sterilized
spore capsules (Duckettetal. (2004).
Conclusions
Bryophytes produce a wide array of secondary substances,
some of which have been shown to have phytotoxic activity
even in low concentrations. Given this fact, allelopathy remains
relatively understudied. ere is documented knowledge
about the impact of bryophyte allelopathic chemicals on some
vascular plants under laboratory conditions, but less about
impacts upon other bryophytes. Research in this area has just
begun in the last years and focused on a few related groups. In
particular, we know little about the mechanisms controlling
selective spore germination of conspecic and alien spores in
contact with mature gametophytes or developing protonema.
It is necessary to undertake both in-vitro studies in controlled
environments and well-designed eld experiments in order to
understand the importance of allelopathic substances in rela-
tion to other bryophyte traits. As demonstrated most research
so far focused on a few related groups of bryophytes. erefore
another scope for future research would be to investigate the
less well studied majority of bryophyte groups.
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Supplementary material (available online as Appendix
L-1097 at  www.lindbergia.org/readers/appendix ).
Appendix 1.