Content uploaded by Des Callaghan
Author content
All content in this area was uploaded by Des Callaghan on Mar 20, 2022
Content may be subject to copyright.
Full Terms & Conditions of access and use can be found at
https://www.tandfonline.com/action/journalInformation?journalCode=yjbr20
Journal of Bryology
ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/yjbr20
Population status and ecology of the liverwort
Biantheridion undulifolium (Nees) Konstant. &
Vilnet in England and Wales
Des A. Callaghan
To cite this article: Des A. Callaghan (2022): Population status and ecology of the liverwort
Biantheridion�undulifolium (Nees) Konstant. & Vilnet in England and Wales, Journal of Bryology,
DOI: 10.1080/03736687.2022.2045423
To link to this article: https://doi.org/10.1080/03736687.2022.2045423
Published online: 18 Mar 2022.
Submit your article to this journal
View related articles
View Crossmark data
Population status and ecology of the liverwort Biantheridion undulifolium
(Nees) Konstant. & Vilnet in England and Wales
Des A. Callaghan
Bryophyte Surveys Ltd, Almondsbury, UK
ABSTRACT
Introduction. Biantheridion undulifolium (Nees) Konstant. & Vilnet [Jamesoniella undulifolia
(Nees) Müll.Frib.] is a globally rare liverwort threatened with extinction. This study was
carried out to investigate its population status and ecology in England and Wales, UK.
Methods. Surveys were undertaken at all previously known sites where the species may
currently occur in England and Wales. Geographical coordinates of colonies were recorded
with a GPS unit, and counts made of occupied 1 m grid cells. Habitat and community
composition were recorded by relevés.
Key results. Biantheridion undulifolium has been reported from 16 sites in England and Wales.
It has become extinct at six (38%), and its continued existence at two others is uncertain.
Following 52 h of search effort, 88 occupied 1 m grid cells were found across eight sites.
The estimated true total is 196–433 occupied 1 m grid cells. Only three sites support
sizeable populations; most sites support < 10 occupied 1 m grid cells. The species is
confined to mesotrophic flushes and bogs, mostly occurring on hummocks of Sphagnum
capillifolium s.l. that are moderately to heavily compacted by grazing livestock. Occupied
hummocks tend to be composed of Sphagnum in good health, with few signs of necrosis.
Fertile plants of this dioicous liverwort are rare, and no sporophytes were found.
Conclusions. Biantheridion undulifolium is a ‘competitive perennial stayer’with limited
dispersal ability, and has undergone a significant decline in England, and probably also in
Wales. Adequate grazing pressure appears to be especially important for its survival. Most
sites occur outside protected areas.
KEYWORDS
Anastrophyllaceae; grazing;
Sphagnum
Introduction
Biantheridion undulifolium (Nees) Konstant. & Vilnet
[Jamesoniella undulifolia (Nees) Müll.Frib.] (Jungerman-
niales: Anastrophyllaceae) (Figure 1) is a dioicous
boreal-montane liverwort that appears to be a Pleisto-
cene relict (Damsholt 2002). Before it was placed in its
current monospecific genus, it was included in Jameso-
niella (Spruce) F.Lees together with a group of species
that are now mostly placed within Syzygiella Spruce
(Adelanthaceae) (Feldberg et al. 2010; Vilnet et al.
2010; Söderström et al. 2016). It is rare throughout its
broad range and is considered to be threatened with
global extinction, being included on the world IUCN
Red List as ‘Vulnerable’(Bryophyte Specialist Group
2000).
In Europe, the species has undergone a large
decline and is listed as extant by Schnyder et al.
(2019) only in France, Germany, Russia and the UK,
and as possibly extinct in Austria, the Czech Republic,
Denmark, Finland, Norway, Poland, Slovakia, Sweden
and Switzerland. Encouragingly, there has since been
a recent record from Denmark (Goldberg 2020). Thus,
Biantheridion undulifolium is possibly extinct in eight
(62%) of the European countries from where it has
been known to occur. In Asia, the liverwort is known
from China and Russia, and in North America it is
known from Greenland, Nunavut and Quebec (Schuster
1969; Bryophyte Specialist Group 2000; Damsholt 2002;
Blockeel et al. 2014; Faubert 2016; Ellis et al. 2017;
Ramirez et al. 2021). Reports from Japan and Korea
are referable to Syzygiella autumnalis (Grolle 1964).
In England, the liverwort was first found by George
Stabler (1839–1910) “growing in a bog amongst
Sphagnum”at Barrowfield, Westmorland (v.-c. 69), in
October 1878 (BM000736600), and in Wales it was
first found recently, by Mark Lawley, in a mire in the
Berwyn Mountains, Montgomeryshire (v.-c. 47), in
July 2012. The aim of this study was to investigate
the current population status and ecology of the
species in England and Wales.
Materials and methods
Taxonomy
Taxonomy follows Brinda and Atwood (2021) for bryo-
phytes and Stace (2019) for vascular plants. Because of
well-known problems regarding the morphological
distinction of Sphagnum capillifolium and S. rubellum
and the existence of hybrids (Hill 1976; Cronberg
1989,1998; Shaw et al. 2005), no attempt was made
© British Bryological Society 2022
CONTACT Des Callaghan des.callaghan@outlook.com
JOURNAL OF BRYOLOGY
https://doi.org/10.1080/03736687.2022.2045423
Published online 18 Mar 2022
to separate these taxa during the present study, and
they are here treated together under the name Sphag-
num capillifolium s.l.
Identification
Biantheridion undulifolium is very similar in appearance
to Odontoschisma sphagni, which commonly occupies
the same microhabitat. Their inflorescences differ
markedly, but these are usually absent and therefore
of very limited use regarding identification in the
field. A key difference that can usually be observed in
the field, once a shoot has been carefully extracted
from a Sphagnum colony, is the presence of postical
flagella in O. sphagni; these do not occur in
B. undulifolium. The total number of oil bodies per
leaf cell is a clear distinguishing character: (3)6–14 in
B. undulifolium versus 2–4(5) in O. sphagni (Paton
1999). Shoots of Mylia anomala that lack gemmae
can also look very similar to B. undulifolium; however,
the former has much bigger leaf cells, giving the
plants a more translucent appearance when observed
through a hand lens.
Distribution and abundance
Geographical coordinates follow the Ordnance Survey
National Grid reference system. Grid cells are referred
to by the coordinates of the southwest corner. An
inventory of all locations from which Biantheridion
undulifolium has been reported in England and Wales
was prepared from (i) a review of biological records
within the national recording database of the British
Bryological Society, held by the Biological Records
Centre (Wallingford, UK); (ii) details on vouchers held
in herbaria (BBSUK, BM and NMW); (iii) published and
unpublished literature (Paton 1969; Holyoak 1999,
2000,2004,2006; Callaghan 2012; Holyoak 2012;
Lawley 2013; Porley 2013; Blockeel et al. 2014;
Lansdown 2014; Callaghan 2015); and (iv) correspon-
dence with local experts.
All sites within the subsequent inventory that
retained potential habitat for Biantheridion undulifo-
lium were surveyed during September to November
2021. At each site, a detailed search was made for
the liverwort. For each colony found, a geographical
waypoint was logged with a hand-held GPS unit
(Garmin GPSMAP 64s; Garmin, Olathe, KS, USA),
which consistently reported accuracy of ≤5 m. Way-
points were not logged for colonies < 1 m from a pre-
viously logged colony. Each logged colony is
considered to be a separately occupied 1 m grid cell,
and following Bergamini et al. (2019), each occupied
1 m grid cell is considered to be an ‘individual-equival-
ent’. Once the searching of a site was complete, an
overall population estimate of B. undulifolium was
made, informed by the frequency with which the
species had been detected along the survey route
and the amount of apparently favourable habitat
that was not searched.
Habitat and community composition
In Britain, Biantheridion undulifolium occurs exclusively
within hummocks formed by other bryophytes, almost
always Sphagnum. The identity of the main hummock-
forming species supporting each logged colony of
B. undulifolium was recorded. Relevés were also
recorded to describe habitat conditions and commu-
nity composition of locations occupied by the liver-
wort, generally following the method of Bates (2011).
Sample locations were selected to represent the full
range of conditions occupied by the liverwort.
Relevés measured 50 × 25 cm. Within each, percen-
tage cover of each species of bryophyte, lichen and
vascular plant was estimated. Percentage cover of
dead plant material (‘litter’) and bare ground in each
relevé was also recorded. Shade was recorded accord-
ing to the following index: 1, fully exposed to sunlight
at all times; 2, shaded from direct sunlight for up to half
the day; 3, receiving significant direct sunlight but for
less than half the day; 4, moderately shaded from
direct sunlight (e.g. by a light-medium deciduous
tree canopy; 5, permanently shaded from direct sun-
light but otherwise open to the sky (i.e. with north-
facing aspect); 6, in deep woodland (e.g. coniferous)
shade with no sunflecks; and 7, in perpetual, very
deep shade. Slope was measured with a digital clin-
ometer, and recorded as the mean angle (°) from hori-
zontal in the direction of greatest slope. Using the
previously mentioned GPS unit, aspect was recorded
as the bearing (°) of the relevé.
The health of associated Sphagnum was scored as
follows: 1 –good, with no necrosis evident; 2 –moder-
ate, with occasional necrosis evident; and 3 –poor,
with frequent necrosis evident. The compaction of
Figure 1. Biantheridion undulifolium creeping through Sphag-
num capillifolium s.l. and a small amount of S. papillosum at
Dozmary Pool, East Cornwall (SX192742), 26 October 2021.
Photographed by D. A. Callaghan.
2DES A. CALLAGHAN
associated Sphagnum was scored as: 1, no evident
compaction; 2, moderate compaction evident; and 3,
heavy compaction evident.
Results
Distribution and abundance
Biantheridion undulifolium has been reported from 16
sites in England and Wales (Table 1). It has become
extinct at six (38%), and its continued existence at
two others is uncertain. The present survey confirms
that populations are extant at eight sites (Figure 2).
Following 52 h of search effort, 88 occupied 1 m
grid cells were recorded. It is estimated that the
current total comprises 196–433 occupied 1 m grid
cells across all the sites here considered. Dozmary
Pool (v.-c. 2) supports the largest population (100–250
occupied 1 m grid cells), followed by Carneddau (50–
100) (v.-c. 43) and Nover’sHill(25–30) (v.-c. 40). The
remaining sites all support small populations (< 10).
Figure 3 shows occupancy of Ordnance Survey 10 km
grid cells by B. undulifolium in England and Wales.
Habitat and community composition
Examples of habitat occupied by Biantheridion unduli-
folium are shown in Figure 4. It is confined to meso-
trophic flushes and bogs that are grazed by livestock,
ranging in altitude from 200 to 415 m a.s.l. Of the 88
colonies found during the present survey, 82 (93%)
were on hummocks primarily formed by Sphagnum
capillifolium s.l., four (5%) were on S. papillosum and
two (2%) were on Polytrichum strictum.
Results from relevés (n= 10; Table 2) show Sphag-
num capillifolium s.l. and P. strictum to be the most
common associates of Biantheridion undulifolium.Aula-
comnium palustre is also a frequent associate, although
usually in small quantity. Bare ground is virtually absent
and plant litter is sparse. Locations are typically exposed
to the sun for all or most of the day. Hummocks on
which B. undulifolium occurs are usually moderately to
heavily compacted by grazing animals, although the
component Sphagnum is generally in good health, nor-
mally with few or no signs of necrosis. The species also
sometimes occupies hummocks uncompacted by live-
stock trampling, but only hummocks that that are
densely formed and grazed (Figure 5). Sphagnum hum-
mocks of loose growth form, typical of flushes and mires
that are ungrazed, are not occupied.
Site accounts
Below are provided details of locations from where
Biantheridion undulifolium has been recorded in
England and Wales, and the results of searches
during the present survey.
West Cornwall (v.-c. 1). Lower Ninnes Bog (SW4534).
Collected here by W. Curnow in 1882, with no sub-
sequent records. The precise location is uncertain,
because ‘Lower Ninnes Bog’is not marked on any
maps; however, it was presumably a mire within the
neighbourhood of Lower Ninnes. No significant areas
of mire habitat presently exist within this vicinity, and
the liverwort was considered by Paton (1969)tohave
become extinct from this location.
Table 1. Abundance of Biantheridion undulifolium in England and Wales.
Site
Population
status
Year of last
record
Search effort during
present survey (person-h)
Count of occupied 1 m grid
cells during present survey
Current population estimate (total
no. of occupied 1 m grid cells)
West Cornwall
Lower Ninnes Bog Extinct 1881 NA NA 0
East Cornwall
Dozmary Pool Extant 2021 6 25 100–250
Red Hill Marsh Extinct 1980 NA NA 0
Red Moor Extinct 1962 3 0 0
Redmoor Marsh Extant 2021 4.5 2 5–10
Witheybrook Marsh Extant 2021 6 2 5–10
West
Gloucestershire
Wigpool Common Extinct 1931 NA NA 0
Shropshire
Catbatch Extinct 2009 4 0 0
Hopesay Hill Extant 2021 3 4 5–10
Nover’s Hill Extant 2021 2 23 25–30
Radnorshire
Carneddau Extant 2021 8 29 50–100
Montgomeryshire
Afon y Dolau
Gwynion
Uncertain 2012 5.5 0 0–5
Cwm Cra Uncertain 2019 4 0 0–5
Westmorland
Barrowfield Extinct 1965 NA NA 0
Hare Hall Extant 2021 2 1 1–3
Helton Fell Extant 2021 4 2 5–10
Total 52 88 196–433
NA, not applicable.
JOURNAL OF BRYOLOGY 3
East Cornwall (v.-c. 2). Dozmary Pool (SX1974). A
mesotrophic bog grazed by cattle, bordering an
ancient natural moorland lake. First found here by
J. A. Paton in May 1963 (NMW.C.2005.019.644) and
refound subsequently on many occasions (Holyoak
2006; Callaghan 2012). The present survey located 25
occupied 1 m grid cells, and it is estimated that the
Figure 2. Survey routes and locations of Biantheridion unduli-
folium recorded during the present survey at Dozmary Pool
(A), Witheybrook Marsh (B), Redmoor Marsh (C), Hopesay Hill
(D), Nover’s Hill (E), Hare Hall (F), Carneddau (G) and Helton
Fell (H). Satellite image © Google, DigitalGlobe.
Figure 4. Habitat and locations (arrowed) of Biantheridion
undulifolium at Dozmary Pool (A), Helton Fell (B), Hare Hall
(C) and Nover’s Hill (D). Photographs by D. A. Callaghan.
Figure 3. Occupancy of Ordnance Survey 10 km grid cell by
Biantheridion undulifolium in England and Wales.
4DES A. CALLAGHAN
total population comprises 100–250 occupied 1 m grid
cells. Both male and female plants were found. The site
is within Dozmary Pool Site of Special Scientific Interest
(SSSI).
Red Hill Marsh (SX1772). First found here by
J. A. Paton in 1979 and recorded again in February
1980. The site was flooded by a reservoir, Colliford
Lake, which was constructed in 1983.
Red Moor (SX0661). First found here among
Sphagnum and Aulacomnium palustre by J. A. Paton
in April 1962 (NMW.C.2001.020.406). A return visit by
J.A.P. in 1993 found that the original location had
been heavily poached by horses, and Biantheridion
undulifolium was not refound (Holyoak 2006). A
further search in 1998 was also unsuccessful (Holyoak
1999), as was a search during the present survey. No
habitat in good condition for the species presently
exists, and it appears the liverwort has become
extinct at this site. The site is within Red Moor SSSI
and is managed as a nature reserve by Cornwall Wild-
life Trust.
Redmoor Marsh (SX2378). A mesotrophic bog and
flushes grazed by cattle. First found here by
D. T. Holyoak in December 2003. A survey in August
Table 2. Percentage cover of plant species and environmental data from relevés occupied by Biantheridion undulifolium at sites in
England and Wales.
a
Variable
Relevé (% cover)
b
1234 5678910
Lichens
Cladonia portentosa 2
Liverworts
Biantheridion undulifolium 3 4 0.1 0.5 0.5 0.5 0.1 2 5 5
Calypogeia fissa 11
Cephalozia connivens 0.1 0.1
Cephaloziella hampeana 0.1 0.1
Fuscocephaloziopsis macrostachya var. macrostachya 0.1
Lophozia ventricosa var. ventricosa 0.1 0.1 0.1 0.1
Mylia anomala 5
Odontoschisma sphagni 52
Mosses
Aulacomnium palustre 0.1 10 3 1 1 5 0.1 0.5
Calliergonella cuspidata 0.1
Dicranum scoparium 10 0.1
Hylocomium splendens 0.5
Hypnum jutlandicum 0.1
Pleurozium schreberi 0.1 0.1 0.1 3
Polytrichum commune 2 0.5
Polytrichum strictum 0.1 3 4 60 10 5 10 0.5 5 10
Rhytidiadelphus loreus 0.1 0.5
Sphagnum capillifolium s.l. 60 50 10 50 70 50 40 0.1 95 50
Sphagnum cuspidatum 21
Sphagnum fallax 415 1
Sphagnum fuscum 10
Sphagnum palustre 5
Sphagnum papillosum 0.1 5 1 30 95 0.1
Thuidium delicatulum 0.1
Vascular plants
Agrostis stolonifera 0.5
Calluna vulgaris 10 10
Carex demissa 0.5 0.5
Carex panicea 13
Drosera rotundifolia 0.1
Erica tetralix 0.5 1
Eriophorum angustifolium 2 3 0.5 0.1
Festuca ovina 30.123 55 5
Galium saxatile 3
Holcus lanatus 0.5 1 1 2
Juncus effusus 3
Juncus squarrosus 55 3
Molinia caerulea 55 4
Polygala serpyllifolia 2
Potentilla erecta 2 0.5 3 0.5 0.2
Trifolium repens 0.5
Vaccinium myrtilis 11
Bare ground (%) 2
Litter (%) 1 3 1 1 2 1 1 1 5
Sphagnum compaction
c
222 2 333 31 2
Sphagnum health
c
111 2 311 22 3
Shade index
c
111 1 111 12 1
Aspect (°) 60 60 56 170 229 84 95 138 149 136
Slope (°) 2 2 7 10 12 2 1 7 20 6
a
Empty cells indicate 0% cover.
b
1 and 2 = Dozmary Pool, 3 = Witheybrook Marsh, 4 = Carneddau, 5 = Hopesay Hill, 6 and 7 = Nover’s Hill, 8 = Hare Hall, 9 and 10 = Helton Fell.
c
See text for definitions of scores.
JOURNAL OF BRYOLOGY 5
2011 found five occupied 1 m grid cells (Callaghan
2012), and during the present survey Biantheridion
undulifolium was found in two occupied 1 m grid
cells, comprising only sterile plants. There is a relatively
small amount of potential habitat for the liverwort,
largely limited to scattered diffuse flushes around the
edge of the bog. The total population is estimated to
be 5–10 occupied 1 m grid cells. The site is not
within any SSSI.
Witheybrook Marsh (SX2472). A mesotrophic bog
and flushes grazed by cattle. First found here by
J. A. Paton in 1980. Although Biantheridion undulifo-
lium has been refound subsequently on several
occasions, it has always been in small quantity and
some searches have been unsuccessful (Holyoak
2006; Callaghan 2012). The present survey located
two occupied 1 m grid cells, and it is estimated that
the total population comprises 5–10 occupied 1 m
grid cells. Only sterile plants were found. The site is
not within any SSSI.
West Gloucestershire (v.-c. 34). Wigpool Common
(SO6519). Collected from here by H. H. Knight in Sep-
tember 1929 (NMW.44.66.615), October 1929
(NMW.44.66.616) and October 1931 (NMW.44.66.617).
There are no subsequent records. The mire habitat of
the common has been mostly destroyed by conifer
plantations, largely established in the 1960s. Lansdown
(2014) reports that drainage and other modifications
have made the site unsuitable for Biantheridion
undulifolium.
Shropshire (v.-c. 40). Catbatch (SO4196). A small
mesotrophic flush grazed by sheep and ponies.
First found here by M. Lawley in August 2009
(NMW.C.2011.012.2), when it was seen on a single
Sphagnum hummock (Lawley 2009). It could not be
refound during a return visit by M.L. or during two sub-
sequent searches by Callaghan (2015). The precise
location of the original record was visited in the
company of M.L. during the present survey. The orig-
inal flush no longer provides suitable habitat for
Biantheridion undulifolium, with very little Sphagnum
remaining and the vegetation dominated by grasses
(Festuca ovina) and rushes (Juncus effusus). Given that
there have been several detailed and unsuccessful
searches for the liverwort in Catbatch during recent
years, it appears as though it has become extinct.
The site is within Long Mynd SSSI.
Hopesay Hill (SO3983). A small mesotrophic flush
grazed by cattle. First found here in very small quantity
by D. Wrench in September 2004 (NMW.C.2006.006.65)
and seen again the following month. A survey of all the
springs and flushes of Hopesay Hill in September 2012
refound it at the original location but nowhere else
(Eades et al. 2013). The present survey found four occu-
pied 1 m grid cells at the original location. There is very
little suitable habitat within the site, and it is estimated
that the total population comprises 5–10 occupied 1 m
grid cells. Only sterile plants were found. The site is not
within any SSSI but is managed for nature conservation
purposes by the National Trust.
Nover’s Hill (SO4595). A mesotrophic flush grazed by
cattle and sheep, bordering a small moorland pool.
First found here by M. Lawley in March 2009. In May
2013, it occupied eight 10 m grid cells (Callaghan
2015). The present survey found 23 occupied 1 m
grid cells, and it is estimated that the total population
comprises 25–30 occupied 1 m grid cells. Only sterile
plants were found. The site is within Long Mynd SSSI.
Radnorshire (v.-c. 43). Carneddau (SO0654). A series
of mesotrophic flushes grazed by sheep. First found
here by M. Lawley in May 2013. In the present survey
it was recorded in 29 1 m grid cells, and it is estimated
that the total population comprises 50–100 occupied
1 m grid cells. Only sterile plants were found. The site
is not within any SSSI.
Montgomeryshire (v.-c. 47). Afon y Dolau Gwynion,
near (SJ0221). A fairly extensive mesotrophic flush
system grazed by sheep. First found here by
Figure 5. Examples of Sphagnum capillifolium s.l. hummocks
occupied by Biantheridion undulifolium, including an
untrampled but grazed hummock at Carneddau (A) and a
heavily trampled and grazed hummock at Nover’s Hill (B).
Photographed by D. A. Callaghan.
6DES A. CALLAGHAN
M. Lawley in July 2012, when a single tiny patch was
located. Shortly after its discovery, there was an unsuc-
cessful attempt to refind it (Bosanquet 2013) and the
present survey also failed. There is very little suitable
habitat currently, and it is estimated that the total
population comprises 0–5 occupied 1 m grid cells.
The site is within Berwyn SSSI.
Cwm Cra (SN9998). A small mesotrophic flush grazed
by sheep. First found here by M. Lawley in June 2019.
There are no subsequent records, and it was not
refound during the present survey, in the company
of M.L. There is very little suitable habitat currently,
and it is estimated that the total population comprises
0–5 occupied 1 m grid cells. The site is not within any
SSSI.
Westmorland (v.-c. 69). Blockeel et al. (2014) map the
historic presence of Biantheridion undulifolium in
hectad SD69, based on a record by G. Stabler in
October 1882 when it was found on a shady dry
bank by the River Lune. This is a mistake, the original
material comprising Syzygiella autumnalis
(BM00736601), as correctly determined by Stabler
(1898).
Barrowfield (SD4890). First found here by G. Stabler in
October 1872, including both male and female plants
with sporophytes, growing with Mylia anomala among
Sphagnum (BM000736600; Stabler 1898). It was refound
in September 1961 (NMW.C96.17.480) and October
1965 (NMW.C96.17.478). During a visit in September
1965, it was present in small quantity (Appleyard 1966).
The site was planted with conifers by 1970 and the
habitat destroyed.
Hare Hall (SD2192). A small mesotrophic flush
grazed by sheep. First found here by W. A. Nelson
and S. Thomas in August 2009. The present survey
located a single occupied 1 m grid cell, and it is esti-
mated that the total population comprises 1–3 occu-
pied 1 m grid cells. Only sterile plants were found.
The site is not within any SSSI.
Helton Fell (NY4020). A fairly extensive mesotrophic
flush system grazed by sheep. First found here by
G. P. Rothero in October 2004 and seen again in April
2012. The present survey located two occupied 1 m
grid cells. There was little potential habitat within the
area surveyed, and it is estimated that the total popu-
lation comprises 5–10 occupied 1 m grid cells. Female
plants were frequent in one of the colonies found. The
site is not within any SSSI.
Discussion
Most of the populations of Biantheridion undulifolium
censused during the present study were small, com-
prising < 10 occupied 1 m grid cells. Only three popu-
lations were sizeable, at Dozmary Pool (100–250
occupied 1 m grid cells), Carneddau (50–100) and
Nover’s Hill (25–30). In Scotland, surveys of the liver-
wort were undertaken in 1996, 2005 and 2012
(Rothero 2013). The census method involved counts
of occupied Sphagnum hummocks. Although there
can be problems regarding the definition of such
count units in the field, for example when adjacent
hummocks are undergoing coalescence, or when a
large hummock is undergoing fragmentation, the
total counts from such a census are likely to be
broadly similar to the those which would be derived
by the present survey method (i.e. counts of occupied
1 m grid cells).
Three populations were found in Scotland, all in
lowland sites (5–15 m a.s.l.) nearby to one another
on the coast of Argyll. During the most recent census
count in 2012, the number of occupied hummocks
totalled 122 (Ardifuir), 35 (Bagh Ban) and 33
(Auchoshin) (Rothero 2013), which appears to be
broadly similar to the largest populations found
during the present survey in England and Wales.
There seem to be no population census data for any
other sites within the global range of the species. If
suitable data become available, it would be especially
interesting to compare the size of populations in
Britain with those from the Massif Central of France,
which appears to be a European hotspot for the
species and where it is occurs at 1000–1300 m a.s.l.
(Hugonnot 2012), much higher than in Britain.
The results of the present study clearly indicate that
Biantheridion undulifolium has undergone a significant
historic decline in England, having been lost from six of
its 13 known sites. The trend in Wales is difficult to
judge, because B. undulifolium has only recently been
detected in the country; however, it seems likely that
it has been overlooked in the past and that a similar
historic decline has occurred. Factors that are known
to have caused extinctions at former sites include
reservoir construction, establishment of conifer planta-
tions, drainage of land for agricultural reasons, and
changes in site management practice, especially
regarding livestock grazing. These factors continue to
operate on mires and flushes in the uplands of
England and Wales, which is a particular concern for
B. undulifolium because it often occurs on sites where
nature conservation is not a focus of land manage-
ment. For example, six of the eight sites where it was
found during the present study are not protected by
SSSI designations. Regarding the three most important
populations, two are protected within SSSIs and its
habitat is managed favourably within them, at
Dozmary Pool and Nover’s Hill. The other population,
at Carneddau, is unprotected, although current
grazing management appears to be favourable.
The most typical plant community occupied by
Biantheridion undulifolium in England and Wales corre-
sponds with M6 Carex echinata–recurvum/auriculatum
mire, a common type of soligenous mire in the
JOURNAL OF BRYOLOGY 7
uplands of Britain, typically occurring in wet hollows,
hillside flushes, and along the margins of streams
and pools (Rodwell 1991). The liverwort has never
been found in strongly oligotrophic conditions, such
as M18 Erica tetralix–Sphagnum papillosum bogs, or
in strongly calcareous conditions, such as some of
the more basic M10 Carex dioica–Pinguicula vulgaris
flushes. The vegetation of sites occupied by the liver-
wort in Scotland, as described by Rothero (2013), also
includes M6 vegetation, in addition to an association
close to the M10a Carex viridula ssp. oedocarpa–
Juncus bulbosus subcommunity, the least basic type
of M10 vegetation. Habitat conditions in France
appear to be broadly similar, with B. undulifolium
seeming to avoid the more ombrotrophic bogs and
largely favouring soligenous systems with slight
mineral enrichment (Hugonnot 2012).
The present study suggests a close association
between Biantheridion undulifolium and hummocks
of Sphagnum capillifolium s.l. in England and Wales.
Only rarely was the liverwort found on hummocks
of S. papillosum, and careful searching of many
hummocks of S. subnitens, which occurs frequently
at some of the surveyed sites and can seem to
provide a favourable microhabitat, revealed no
B. undulifolium. Similarly, in Scotland it is most fre-
quently found on hummocks of S. capillifolium and
S. papillosum (Rothero 2013). Outside Britain, it is
unclear which Sphagnum species are especially impor-
tant for B. undulifolium, although S. capillifolium hum-
mocks are known to be occupied (Meinunger and
Schröder 2007; Hugonnot 2012), and it is also associ-
ated with various other species. For example, in
France it has also been found among S. compactum,
S. fuscum,S. palustre and S. papillosum (Hugonnot
2012). Pocock and Duckett (1985) suggest that the
liverwort is totally restricted to living Sphagnum
shoots and indicated the possibility that it may be par-
tially parasitic on Sphagnum. However, it is sometimes
found growing among bryophytes other than Sphag-
num, for example on hummocks composed entirely
of Polytrichum strictum during the present study, and
among Aulacomnium palustre,Campylopus flexuosus
and Leucobryum glaucum in Scotland (Rothero 2013).
There is also a remarkable recent record from
Denmark, where it was found growing on sandy soil
alongside a path through coastal dune heath (Gold-
berg 2020).
Damsholt (2002) states that Biantheridion undulifo-
lium is frequently reported with sex organs and peri-
anths, and Paton (1999) describes the liverwort as
‘fairly often fertile’in Britain. This does not correspond
with the present survey results. Of the 88 occupied 1 m
grid cells recorded, fertile plants were seen in only two,
including male and female within a grid cell at
Dozmary Pool and female only within a grid cell at
Helton Fell. Paton (1999) describes sporophytes as
very rare in Britain and mature sporophytes as
unknown. No sporophytes were encountered during
the present survey, but Rothero (2013) found them
at Ardifuir, occurring in some of the larger patches
during autumn, including dark capsules nearing
maturity in October. Given that the species does not
produce specialised asexual propagules and that spor-
ophyte production appears to be rare, the dispersal
capacity of the liverwort will be limited. At least in
part, this could help to explain the general rarity of
the species throughout its range, as suggested by
Schuster and Konstantinova (1996), although relatively
low and episodic regional spore production may be
sufficient to maintain global populations of some
long-lived bryophyte species (Hedenäs and Bisang
2019).
Unlike some other liverworts that inhabit Sphag-
num hummocks, such as Kurzia pauciflora and Odon-
toschisma fluitans,Biantheridion undulifolium is unable
to differentiate new geotropic axes and simply
follows the ascendant movement of actively
growing Sphagna, leaving old axes buried in peat
layers (Hugonnot et al. 2015). Hugonnot et al.
(2015) sampled cores from Sphagnum hummocks
up to a depth of 30 cm and found B. undulifolium
at depths of up to 25 cm. In favourable environ-
mental conditions, it therefore appears that individual
shoots of B. undulifolium could potentially live for a
long time, at least decades and perhaps much
longer. Regarding life-history strategies (sensu
During 1992), Dierssen (2002) categorised
B. undulifolium as a ‘colonist’. However, it appears
as though the category of ‘competitive perennial
stayer’is better assigned to this species, given its
low reproductive investment, the potentially long life-
span of individuals, and its successful competition for
space within the highly competitive environment of
Sphagnum colonies.
All the locations found to be occupied by Bianther-
idion undulifolium during the present study were
grazed by livestock, including cattle, ponies and
sheep. Hummock-building species of Sphagnum tend
to produce denser hummocks under such conditions.
Without grazing pressure, hummocks tend to have a
looser composition, within which B. undulifolium was
never found. Reasons for the absence of
B. undulifolium from looser hummocks are unclear
and deserve investigation. However, dense hummocks
presumably provide a more stable substrate and a
more constant water supply, which may be especially
important during spore germination and the early
establishment of colonies. The growth rate of Sphag-
num shoots could also be reduced under trampling
and grazing pressure, helping B. undulifolium to
compete for space at the hummock surface. Rothero
(2013) also observed a close link between the liverwort
and livestock grazing at sites in Scotland, noting its
8DES A. CALLAGHAN
absence from loose Sphagnum hummocks in ungrazed
locations. Similar observations have been noted in
France (Hugonnot 2012).
Although Biantheridion undulifolium is a very rare
species in England and Wales, further sites no doubt
remain to be discovered. There is a clear need to
obtain a more complete inventory of occupied sites,
especially given the need for adequate grazing and
possible conflicts regarding such management of
land. For example, there are presently major initiatives
in the uplands of England and Wales to plant trees to
help sequester carbon emissions and to rewild the
landscape, both of which can involve a large reduction
or complete cessation of livestock grazing across large
areas of land. Targeted survey work in regions such as
the Cambrian Mountains, Dartmoor, Exmoor and the
Lake District could be successful and may help
prevent the inadvertent loss of unknown but impor-
tant populations of B. undulifolium as land manage-
ment practices change.
Acknowledgements
Many thanks to the following for various generous assist-
ance: Sam Bosanquet (Natural Resources Wales), Steffen
Caspari (DLR Projektträger), Jonathan Cox (Natural
England), Iain Diack (Natural England), Jan Eckstein (Göttin-
gen, Germany), Len Ellis (BM), Jean Gagnon (Québec City,
Canada), Irina Goldberg (Aarhus University), Claire Halpin
(Llanfrynach, Wales, UK), Vincent Hugonnot (Blassac,
France), Jan Kucera (University of South Bohemia), Andrew
Perry (National Trust), Katherine Slade (NMW), Oliver
Pescott (BRC, Wallingford, England, UK), Neil Sanderson
(Woodlands, England, UK) and Justin Wynns (Natural
History Museum of Denmark). Mark Lawley (Ludlow,
England, UK) was especially helpful with fieldwork assistance
at some of the sites surveyed.
Disclosure statement
No potential conflicts of interest were disclosed by the
author.
Funding
Funding for this work was provided by Natural England and
Natural Resources Wales.
Notes on contributor
Des Callaghan is a consultant bryologist operating under
Bryophyte Surveys Ltd, working throughout Britain and
further afield. His research is focused on threatened
species, taxonomy and conservation ecology.
ORCID
Des A. Callaghan http://orcid.org/0000-0002-0415-1493
References
Appleyard J. 1966. The summer meeting, 1965. Transactions
of the British Bryological Society. 5:209–211.
Bates JW. 2011. BBS Bryophyte Ecology Group. Bryophyte
habitats survey. Recorders’instructions –revised
September 2011.Unpublished report, The British
Bryological Society.
Bergamini A, Bisang I, Hodgetts N, Lockhart N, van Rooy J,
Hallingbäck T. 2019. Recommendations for the use of criti-
cal terms when applying IUCN red-listing criteria to bryo-
phytes. Lindbergia. 42:1–5.
Blockeel TL, Bosanquet SDS, Hill MO, Preston CD. 2014. Atlas
of British and Irish bryophytes. Newbury: Pisces
Publications.
Bosanquet SDS. 2013. Rare liverworts by the Afon y Dolau
Gwynion. Unpublished report to Natural Resources Wales.
Brinda JC, Atwood JJ. 2021. The bryophyte nomenclator.
Draft version. [accessed 2021 Dec 8]. https://www.
bryonames.org.
Bryophyte Specialist Group. 2000.Jamesoniella undulifolia.
The IUCN Red List of Threatened Species 2000:
e.T39199A10169513. [downloaded 2021 Jun 28].
Callaghan DA. 2012. Rare and scarce bryophytes in SW
England. Unpublished report to Natural England.
Callaghan DA. 2015. Bryophyte survey and assessment of The
Long Mynd, Shropshire. Unpublished report to Natural
England.
Cronberg N. 1989. Patterns of variation in morphological char-
acters and isoenzymes in populations of Sphagnum capilli-
folium (Ehrh.) Hedw. and S. rubellum Wils. from two bogs in
southern Sweden. Journal of Bryology. 15:683–696.
Cronberg N. 1998. Population structure and interspecific
differentiation of the peat moss sister species Sphagnum
rubellum and S. capillifolium (Sphagnaceae) in northern
Europe. Plant Systematics and Evolution. 209:139–158.
Damsholt K. 2002. Illustrated flora of Nordic liverworts and
hornworts. Lund: Nordic Bryological Society.
Dierssen K. 2002. Distribution, ecological amplitude and phy-
tosociological characterization of European bryophytes.
Bryophytorum Bibliotheca, Band 56. Stuttgart:
Schweizerbart Science Publishers.
During HJ. 1992. Ecological classification of bryophytes and
lichens. In: Bates JW, Farmer AM, editors. Bryophytes and
lichens in a changing environment. Oxford: Oxford
Scientific Publications.
Eades P, Tratt R, Shaw S. 2013.Habitats Directive Annex 1 fen
survey: Devon, Somerset and Shropshire. Unpublished
report to Natural England.
Ellis LT, AlataşM, AleffiM, Alegro A, Šegota V, Ozimec S,
VukovićN, KoletićN, PrlićD, Bontek M, et al. 2017. New
national and regional bryophyte records, 52. Journal of
Bryology. 39:285–304.
Faubert J. 2016. Bryoquel: spécimens de bryophytes de
l’herbier de la Société Québécoise de Bryologie. Version
8.5. Société Québécoise de Bryologie. Occurrence
dataset https://doi.org/10.5886/4ga8rngp. [accessed via
GBIF.org 2021 Dec 8]. https://www.gbif.org/occurrence/
1045009786.
Feldberg K, Váňa J, Hentschel J, Heinrichs J. 2010. Currently
accepted species and new combinations in
Jamesonielloideae (Adelanthaceae, Jungermanniales).
Cryptogamie, Bryologie. 31:141–146.
Goldberg I. 2020. Årets fund af mosser. URT. 44:28–31.
Grolle R. 1964.Jamesoniella carringtonii –eine Plagiochila in
Nepal mit Perianth. Transactions of the British
Bryological Society. 4:653–663.
JOURNAL OF BRYOLOGY 9
Hedenäs L, Bisang I. 2019. Episodic but ample sporophyte
production in the moss Drepanocladus turgescens
(Bryophyta: Amblystegiaceae) in SE Sweden. Acta Musei
Silesiae. Scientiae Naturales. 68:83–93.
Hill MO. 1976. A critical assessment of the distinction
between Sphagnum capillaceum (Weiss) Schrank and
S. rubellum Wits. in Britain. Journal of Bryology. 9:185–191.
Holyoak DT. 1999. Surveys of bryophyte on mires in East
Cornwall 1999, especially for Marsh Earwort Jamesoniella
undulifolia. Unpublished report to English Nature.
Holyoak DT. 2000. Surveys of bryophyte on mires in East
Cornwall 2000, especially for Marsh Earwort Jamesoniella
undulifolia. Unpublished report to English Nature.
Holyoak DT. 2004. Research on Jamesoniella undulifolia
and other bryophytes of mires on Bodmin Moor,
Cornwall, during 2003–2004. Unpublished report to
English Nature.
Holyoak DT. 2006. The status and conservation of
Jamesoniella undulifolia in Cornwall in 2005–2006.
Unpublished report to Natural England.
Holyoak DT. 2012. A bryophyte flora of Cornwall and the Isles
of Scilly. http://www.cisfbr.org.uk.
Hugonnot V. 2012.Biantheridion undulifolium (Nees)
Konstant. & Vilnet [Jamesoniella undulifolia (Nees)
K. Müller] (Jamesoniellaceae) in the Pyrenees –distri-
bution, ecology and conservation in south-western
Europe. Nova Hedwigia. 94:471–477.
Hugonnot V, Balluet G, Celle J. 2015. Aerial and underground
biomasses of three Sphagnum-dwelling liverworts. Journal
of Bryology. 37:247–249.
Lansdown RV. 2014. A provisional Red Data book of
Gloucestershire bryophytes. The Gloucestershire
Naturalist Special Issue No. 25. Gloucester:
Gloucestershire Naturalists’Society.
Lawley M. 2009. A bryological survey of selected areas of wet
ground on The Long Mynd, Shropshire, in 2009.
Unpublished report to Natural England.
Lawley M. 2013. The mosses and liverworts of Shropshire.
Privately published.
Meinunger L, Schröder W. 2007. Verbreitungsatlas der Moose
Deutschlands. Regensburg: O. Dürhammer für die
Regensburgische Botanische Gesellschaft.
Paton JA. 1969. A bryophyte flora of Cornwall. Transactions of
the British Bryological Society. 5:669–756.
Paton JA. 1999. The liverwort flora of the British Isles.
Colchester: Harley Books.
Pocock K, Duckett JG. 1985. On the occurrence of branched
and swollen rhizoids in British hepatics: their relationships
with the substratum and associations with fungi. New
Phytologist. 99:281–304.
Porley RD. 2013. England’s rare mosses and liverworts.
Princeton: Princeton University Press.
Ramirez J, Watson K, Thiers B, McMillin L. 2021. The New York
Botanical Garden Herbarium (NY). Version 1.41. The
New York Botanical Garden. Occurrence dataset https://
doi.org/10.15468/6e8nje. [accessed via GBIF.org 2021
Dec 8]. https://www.gbif.org/occurrence/1930727128.
Rodwell JS, editor. 1991. British plant communities. Vol. 2,
Mires and heaths. Cambridge: Cambridge University Press.
Rothero GP. 2013. Surveillance of priority bryophytes in
Scotland 2010–2013: Jamesoniella undulifolia.
Unpublished report to Scottish Natural Heritage.
Schnyder N, Bisang I, Caspari S, Hedenäs L, Hodgetts N,
Kiebacher T, Kučera J, ŞtefănuţS, Vana J. 2019.
Biantheridion undulifolium. The IUCN Red List of
Threatened Species 2019: e.T87486156A87732368. [down-
loaded 2021 Jun 28.]
Schuster RM. 1969. The Hepaticae and Anthocerotae of North
America east of the hundredth meridian. Vol. 2. Chicago
(IL): Field Museum of Natural History.
Schuster RM, Konstantinova NA. 1996. Studies on the distri-
bution of critical arctic/subarctic Hepaticae with special
reference to taxa found in Russia. Lindbergia. 21:26–48.
Shaw AJ, Cox CJ, Boles SB. 2005. Phylogeny, species delimita-
tion, and recombination in Sphagnum section Acutifolia.
Systematic Botany. 30:16–33.
Söderström L, Hagborg A, von Konrat M, Bartholomew-
Began S, Bell D, Briscoe L, Brown E, Cargill DC, Costa DP,
Crandall-Stotler BJ, et al. 2015. World checklist of horn-
worts and liverworts. PhytoKeys. 59:1–828.
Stabler G. 1898. On the Hepaticae and Musci of Westmorland.
The Naturalist. 23:341–348.
Stace. 2019. New flora of the British Isles. 4th ed. Cambridge:
Cambridge University Press.
Vilnet AA, Konstantinova NA, Troitsky AV. 2010. Molecular
insight on phylogeny and systematics of the
Lophoziaceae, Scapaniaceae, Gymnomitriaceae and
Jungermanniaceae. Arctoa. 19:31–50.
10 DES A. CALLAGHAN
