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Journal of Applied Botany and Food Quality 85, 129 - 133 (2012)
1
Agroscope Reckenholz-Tänikon Research Station ART, Ecological Farming Systems, Zürich, Switzerland
2
Universidad Católica de Temuco, Facultad de Recursos Naturales, Escuela de Agronomía, Temuco, Chile
3
Zurich-Basel Plant Science Center, Institute of Botany, University of Basel, Basel, Switzerland
4
Institute of Plant Production and Agroecology in the Tropics and Subtropics, University of Hohenheim, Stuttgart, Germany
Ambispora reticulata,
a new species in the Glomeromycota from mountainous areas
in Switzerland and Chile
1*
Fritz Oehl,
2
Claudia Castillo,
3
David Schneider,
1
Verena Säle,
4
Ewald Sieverding
(Received May 5, 2012)
*
Corresponding author
Summary
A new glomeromycotean fungus,
Ambispora reticulata
, was
found in the Swiss Alps and in the Chilean Andes. Only acaulo-
ambisporoid spores were detected so far, 87-131 x 125-150 µm in
diameter and having a three-layered, yellow-brown to brown outer
wall, a bi-layered, hyaline middle wall and a generally three-layered,
hyaline inner wall. The middle wall has a characteristic reticulate
outer surface with irregular triagonal to octagonal (usually tetra-
to hexagonal) pits that are surrounded by ridges. As known for all
Ambispora
species with acaulo-ambisporoid spore formation, the
middle wall is a substantial part of the pedicel which connects the
spore with the mycelium. The new species is a frequent member
of arbuscular mycorrhizal fungal communities in mountainous
and subalpine grasslands of the Swiss Alps at 1000-2100 m above
sea level. It occurred less frequent in high alpine grasslands and
at altitudes below 1000 m, where the fungus was found in a con-
servation tillage and a low-input tillage system. It was also detected
in evergreen and in deciduous forests in the Andes of Southern Chile
at elevations of 550-1600 m.
Introduction
In the last two decades, biodiversity studies have worldwide been
intensi ed. This is especially true for arbuscular mycorrhizal fungi
(AMF) of the Glomeromycota (e.g.
BŁASZKOWSKI,
1993;
VESTBERG,
1995;
CASTILLO
et al., 2006, 2010;
SÁNCHEZ-CASTRO
et al., 2011;
BEZERRA
et al., 2011;
SOUZA
et al., 2012). While until 1990, only
ca. 130 glomeromycotean species were described (
SCHENCK
and
PÉREZ,
1990), today we count approximately 250 species. Also
remarkably, the more recently published new AMF species (e.g.
GAMPER
et al., 2009;
FURRAZOLA
et al., 2011;
RODRIGUEZ
et al.,
2011) have been described by an steadily increasing number of
research groups (
STÜRMER
, 2012).
High AMF species and genus diversities were for instance revealed
in Central Europe (
JANSA
et al., 2002, 2003;
GAMPER
et al., 2004;
OEHL
et al., 2005a, 2010) even up to the highest altitudes and
harshest environments in the Swiss Alps where higher plants live
(
OEHL
et al., 2011a;
KÖRNER
, 2011). While several species were
found in all habitats investigated, others were characteristic for
speci c soils (
OEHL
et al., 2003, 2005b), soil depths (
OEHL
et al.,
2005a), land use practices (
OEHL
et al., 2009) or altitudes (
OEHL
et al., 2006, 2011e, 2012).
One unknown AMF species was mainly found in mountainous
to subalpine grasslands of the Swiss Alps at 1000-2100 m above
sea level (a.s.l.). It was simultaneously found also in mountainous
forests in the Andes of Southern Chile (
CASTILLO
et al., 2006). It
is here published under the epithet
Ambispora reticulata
. The new
species did not reproduce in single spore bait cultures. It is described
from spore morphological characters as these are clearly indicating
that the species belong to
Ambispora
in the Archaeosporales,
Archaeosporomycetes (
SPAIN
et al., 2006;
WALKER
et al., 2008;
OEHL
et al., 2011c).
Materials and methods
Study sites and soil sampling
Soil samples were taken between March 2000 and April 2009 all
over Switzerland from about 100 tillage and conservation tillage
farming sites in the lowlands, and from in total > 400 grassland
sites in the lowlands, mountainous and alpine areas from altitudes
between 300 and 3000 m a.s.l. The soils have developed on different
geological bedrocks from nutrient poor Jurassic sandstones over
granite and gneiss rocks to carbonatic Loess sediments, limestones
and ultrabasic serpentinites (e.g.
OEHL
et al., 2005b, 2010, 2011a).
Undisturbed soil cores from 0-10 cm depth were collected at study
sites. Spores of Glomeromycota were separated from the soil sam-
ples by the wet sieving, decanting and subsequent sugar gradient
centrifugation technique (
SIEVERDING,
1991). In Chile, soil samples
were taken from replicated plots of a nutrient recycling experiment
in an evergreen natural rainforest and a deciduous secondary forest
in the Experimental Station San Pablo de Tregua of the University
Austral de Chile (Valdivia, Chile, 39°30-39°38’S and 72°02-
72°09’W) at an elevation between 550 and 1600 m a.s.l. (
CASTILLO
et al., 2006). Spores were separated as given above.
AM fungal bait cultures
Bait cultures were established in Switzerland directly after soil
sampling as described in
OEHL
et al. (2005b, 2011a) using a steri-
lised substrate (Terragreen (American aluminium oxide, Oil Dry US
special, type III R, >0.125 mm; Lobbe Umwelttechnik Iserlohn,
Germany)
-Loess mixture 3:1; pH-KCl 6.2; organic carbon 0.3 %;
available P (Na-acetate) 2.6 mg kg
-1
; available K (Na-acetate)
350 mg kg
-1
) in pots of different sizes (1 L in 2003-2005;
OEHL
et al., 2011a, 3.5 L in 2009-2010, and 9 L in 2000-2002;
OEHL
et al., 2005b). Sub-samples of the eld samples represented natural
eld inocula and were placed as a thin sandwich layer between
two substrate layers, about 5 cm below the surface. Above the soil
inocula, about 5-7 seeds of each of the four bait plants,
Plantago
lanceolata
L.,
Lolium perenne
L
.
,
Trifolium pratense
L., and in some
experiments also
Hieracium pilosella
L. were sown.
Two weeks-old
Trifolium pratense
plants received
1 mL of a 1:5 with water diluted
12 h old culture of
Rhizobium trifolii
(DSM 30138, from DSMZ-
Deutsche Sammlung von Mikroorganismen und Zellkulturen
GmbH, Braunschweig, Germany), grown in liquid DSMZ 98
medium at 27 C. An automated watering system (Tropf-Blumat,
Weninger GmbH, A-6410 Telfs) was installed and the cultures
were kept in the greenhouse under ambient light and temperature
conditions for 16-32 months. The spore formation was monitored
in the bait cultures in bi- or four-monthly intervals as described in
OEHL
et al. (2009, 2011a). The new fungus reproduced spores only
in two of approximately 650 bait cultures established. All trials to
130
F. Oehl, C. Castillo, D. Schneider, V. Säle,
E. Sieverding
reproduce the new fungus in so-called AMF mono-species cultures
so far failed.
Morphological analyses
The described morphological characteristics of spores and their
subcellular structures are based on observations of specimens
mounted in polyvinyl alcohol-lactic acid-glycerol (PVLG;
KOSKE
and
TESSIER,
1983), in a mixture of PVLG and Melzer’s reagent
(
BRUNDRETT
et al., 1994), a mixture of lactic acid to water at 1:1,
Melzer’s reagent, and in water (
SPAIN,
1990). The terminology
of the spore structure basically is that suggested by
SPAIN
et al.
(2006) for
Ambispora
species, and by
OEHL
et al. (2011b) for all
glomeromycotean taxa. Photographs in Fig. 1-9 were taken with
a digital camera (Olympus model DP70-CU) on a compound
microscope (Zeiss Axioplan). Specimens mounted in PVLG and
the mixture of PVLG and Melzer’s reagent were deposited at
the mycological herbarium of the ETH Zürich (Z+ZT, Zurich,
Switzerland).
Latin diagnosis
Ambispora reticulata
Oehl & Sieverd. sp. nov. (
Fig. 1-9
)
Mycobank MB 800269
Sporae acaulo-ambisporoideae avo-fuscae vel fuscae, 87-131
x 125-150 µm, formatae appendice, tunicis tribus; tunica media
duobus stratis hyalinis reticulum tetragonale at hexagonale formans,
depressionibus 3-7.5(-10) µm in diametro et 0.5-2.5 µm profundis.
Typus hic designatus # 57-5701 (ZT Myc 24171).
Etymology.
Latin,
reticulata
referring to the reticulate ornamentation
of the middle wall.
Holotype
Holotype (here designated: Slide Nr. 57-5701; accession number
ZT Myc 24171) and isotypes (ZT Myc 24172) were isolated from
soil samples taken from the rhizosphere of an high mountainous
pasture characterized by
Nardus stricta
, at Cuolms dil Run Alp
(46°42’57’’N; 8°57’54’’E), Surrein-Sumvitg, Surselva, Kanton
Graubünden, Switzerland, at about 1600 m a.s.l. Paratypes isolated
from several locations in the Swiss Alps and central lowlands of
Switzerland (see below) were also deposited at Z+ZT (ZT Myc
24173-24175).
Description
Acaulo-ambisporoid spores
are formed by the fungus, but so
far sporiferous saccules
and glomo-ambisporoid spores were not
detected. The acaulo-ambisporoid spores
are yellow brown to brown,
globose to oval to g-like, 87-131 x125-150 µm in diameter (Fig. 1-
2) consisting of three walls: outer wall (OW), middle wall (MW) and
inner wall (IW; Fig. 3).
Outer spore wall
consists of three layers (OWL1-OWL3) and is
in total 4-9 µm thick (Fig
. 2-3)
. OWL1 is hyaline, unit, 0.5-1.0 µm
thick (Fig. 1), evanescent (Fig. 2) and thus, usually dif cult or not to
observe in mature spores. Second layer (OWL2) is yellow-brown to
brown, laminated, 3-8 µm thick. It sometimes swells up to 10-20 µm
in PVLG (plus Melzer reagent) under pressure applied on the cover
slide (Fig. 4). OWL3 is hyaline, 0.5-1.5 µm thick, often tightly
adherent to OWL2, but can be separated under pressure. Swelling
laminae of OWL2 stain pinkish, and OWL3 stains pinkish purple
to purple in Melzer’s reagent (Fig. 4). With age, OW shows many
ssures, a feature that becomes more obvious when pressure is
applied on the cover slide (Fig. 3).
Middle wall
is hyaline, bi-layered (MWL1-MWL2) and 1.5-
3.5 µm thick (Fig. 5-6). Both layers are tightly adherent to each
other. MWL1 is semi- exible, 0.8-2.5 µm thick and has a reticulate
surface ornamentation (Fig. 6-7). The pits are irregular triagonal to
octagonal (usually tetra- to hexagonal) and are 3-7.5(-10) µm wide
and 0.5-2.5 µm deep (Fig. 6, 7). Pits are surrounded by ridges that are
0.5-1.2 µm wide. Inner MWL2 is unit, smooth and 0.8-2.1 µm thick.
None of the layers reacts to Melzer’s reagent.
Inner wall
is hyaline, with (two to) generally three layers (IWL1-
IWL3) that are 1.2-3.0 µm thick in total (Fig. 8). IWL1 is < 0.5 µm
thick, and often appears to be missing (Fig. 5-6). IWL2 is 1.2-2.5 µm
thick and rigid, and IWL3 is very thin and usually very dif cult to
detect since tightly adherent to IWL2. None of the layers reacts to
Melzer’s reagent, but in old spores IWL3 sometimes becomes yellow
(Fig. 8).
Pedicel
at spore base is formed by the outer wall and the outer layer
of the middle wall (Fig. 2, 9). It is 7-14 µm broad and 4-16 µm long,
respectively, at the spore base. The pedicel OW layers are 3-6 µm
thick at spore base and taper to 1.2-2.2 µm within a few µm distances
from the base. On the spore surface, they may form a wide pore
(=collar), which is 5-13 µm in diameter. The continuation of MWL1
is reticulate to undulate at the pedicel (Fig. 9). MWL1 wall layer
regularly is only 0.5-1.5 µm thick at pedicel.
Distribution.
In all regions of the Swiss Alps and in Southern
Chile, where the fungus was found, spores of
Am. reticulata
were
common, but they were rarely found in numbers > 1 g
-1
soil. In
Switzerland, they were frequently isolated from the rhizosphere
of mountainous to subalpine grasslands at 1000-2100 m a.s.l. up
to the tree line with vegetation characterized by the dominance
of
Nardus stricta
or
Trisetum avescens
, in soils of pH 3.6-5.9.
Spores were rarely found in alpine
Nardus stricta
grasslands and
generally absent in (high) alpine grasslands characterized by
Carex
ferruginea
or
Sesleria caerulea
. They were also less frequently
found in lower mountainous and lowland grasslands. In detail,
Am.
reticulata
was found in Eastern Switzerland at Piz Nadels (Trun
and Surrein-Sumvitg, Surselva, Chantun Grischun) between 1500-
2000 m a.s.l.in
Nardus stricta
grasslands, in Southeastern Switzerland
at Spadla Alp (Sent, Engiadina, Chantun Grischun) at 2300 m a.s.l.
in a
Nardus stricta
grassland, in Central Switzerland in the Gotthard-
Furka region between 1500-1900 m a.s.l. (Hospental and Realp,
Kanton Uri; Airollo, Cantone Ticino) in
Nardus stricta
and
Trisetum
avescens
grasslands, at Axalp (Brienzer See) between 1000-
1800 m a.s.l., and at Grindelwald (Grosse Scheidegg) between 1200-
2000 m a.s.l. (Berner Oberland, Kanton Bern) in
Nardus stricta
and
Trisetum avescens
grasslands, and in Southwestern Switzerland at
1000-1800 m a.s.l. (La Valette, Champex d’en Bas, Bourg-St.-Pierre,
all Canton Valais) in
Trisetum avescens
grasslands. Recently, they
were also detected in the Canton Berne in an extensively managed
conventional crop rotation system in Niederösch (three years of
temporary grassland and one year of potatoes production) and in a
conservation tillage system in Rubigen (7 year crop rotation with
winter wheat, sugar beet, winter wheat, maize, winter barley and one
year of grass/clover). The soil types were a broad range of Eutric
to Dystric Cambisols in the Swiss Alps, and a Luvisol and Calcaric
Cambisol in the lowlands of Berne, that had developed on a broad
range of bedrocks: acidic sandstones, siliceous gneiss and granite
Ambispora reticulata
sp. nov.
131
Fig.
1-
9:
Ambispora reticulata –
all acaulo-ambisporoid morphs. 1-2. Uncrushed spores isolated from eld soils with a pedicel (pcl) formed by the outer and
the middle wall. 3. Crushed spores with outer, middle and inner wall: OW, MW and IW; OW showing multiple ssures which are especially seen
in aged spores. 4. Crushed spore in PVLG & Melzer’s reagent, with slight pinkish staining reaction on layer OWL2 and purple reaction of layer
OWL3. 5-8. Bi-layered MW (MWL1-MWL2) and triple layered IW (IWL1-IWL3). Middle wall has a diagnostic tetragonal to hexagonal reticulate
ornamentation on the outer surface. Rarely depressions have three or more than six sides. 9. Wall of the pedicel (pcl) is a continuation of MWL1
having exible to semi- exible appearance.
rocks, calcareous ‘Bündner Schiefer’ schists, moraine sediments
and carbonatic limestones. The soil pH was always < 6.0 in the
mountainous areas, while it was 6.0 and 7.1 in the two lowland sites.
Available P (Na-acetate, see
OEHL
et al., 2011a) was between 3.2-
15.2 mg kg
-1
in the mountainous to low alpine areas and 17.2 and
42.8 mg kg
-1
in the two lowland soils.
In Chile,
Am. reticulata
was found in an evergreen forest dominated
by
Nothofagus dombeyi
and
Laureliopsis philippiana
tree species
and a deciduous forest dominated by
Nothofagus alpina
at moun-
tainous altitudes between 550-1600 m a.s.l. (
CASTILLO
et al., 2006).
Soil pH was 4.6 and 5.4, and available P was 6.1 and 3.6 mg kg
-1
,
respectively.
Discussion
Ambispora reticulata
can be easily distinguished from all other
glomeromycotean fungi by its spore wall structure since the
reticulate ornamentation on the middle spore wall is hitherto unique
132
F. Oehl, C. Castillo, D. Schneider, V. Säle,
E. Sieverding
and thus, diagnostic. In the genus
Ambispora
there are only two
other fungi with ornamentation on the middle wall. These are
Am.
appendicula
and
Am. jimgerdemannii
that both have an alveolate
middle wall, in which both middle wall layers are ornamented on
their interface (
ROSE
et al., 1979;
SCHENCK
et al., 1984;
SPAIN
et al.,
2006), while in
Am. reticulata
the reticulum is only on the outer
surface of the middle wall.
The outer wall (OW) of aging spores of
Am. reticulata
regularly
shows many ssures. This is a feature that becomes more obvious
when pressure is applied to the cover slide of permanent specimens
in PVLG, and is also known for the acaulo-ambisporoid morph of
most of the other
Ambispora
species. These are
Am. appendicula
,
Am. gerdemannii
,
Am. fennica
,
Am. nicolsonii
, and
Am. brasiliensis
(
SPAIN
et al., 2006;
GOTO
et al., 2008;
OEHL
et al., 2011d), while
this is not observed with
Am. granatensis
which has a shorter-lived,
since substantially thinner OW (
PALENZUELA
et al., 2011).
Remarkably, spores of
Am. reticulata
were never found with
sporiferous saccules attached, although in addition of eld sampled
spores, also bait cultured spores were analyzed. The reason of not
detecting sporiferous saccules in these bait cultures might be that the
intervals between single sampling periods were four months in these
pots instead of two months. In the shorter intervals we usually found
sporiferous saccules attached with e.g.
Acaulospora nivalis
,
Ac.
alpina
,
Am. fennica
,
Am. appendicula
,
Otospora bareae
(e.g.
OEHL
et al., 2006, 2009, 2012;
PALENZUELA
et al., 2008). Hence, the
mode of spore formation of
Am. reticulata
still has to be discovered.
Also the glomoid morph of
Am. reticulata
, if existent, still has to be
identi ed. In the genus
Ambispora
, glomoid morphs are known only
for some species but not for all (
SPAIN
et al., 2006;
WALKER
et al.,
2007).
In Switzerland, the new species was frequently found in mountainous
to subalpine regions between 1000 and 2100 m a.s.l., whereas it
was regularly absent in higher alpine areas and only sporadically
found in lowland areas. In the Chilean Andes,
Am. reticulata
was
hitherto revealed solely from mountainous areas between 550 and
1600 m a.s.l. indicating that the preferential occurrence of this
fungus may be in medium altitudes within such colder climates.
Distinct altitude respective climatic preferences in the Swiss Alps
and in Sierra Nevada (Spain) were recently described also for other
Ambispora
species, as well as for several other glomeromycotean
fungi like
Acaulospora alpina
,
Ac. nivalis
,
Ac. punctata
,
Glomus
badium
,
Pacispora robigina
and
Tricispora nevadensis
(
OEHL
and
SIEVERDING,
2004;
SPAIN
et al., 2006;
OEHL
et al., 2005a, 2006,
2011e, f, 2012;
PALENZUELA
et al., 2010). By studying different
ecosystems on global scales, we will gradually get a clearer picture
about the biogeography of the Glomeromycota, that are counted
among the most important soil micro-organisms, since they deliver
a series of ecosystem services like soil aggregation, soil erosion
protection, plant growth promotion, plant health and pathogen sup-
pression, and seedling survival at sites as for example stressed by
RILLIG
and
MUMMEY
(2006),
SMITH
and
READ
(2008) and
VAN DER
HEIJDEN
and
HORTON
(2009).
Acknowledgements
This study has been supported by the Swiss National Science
Foundation within the Programme NFP48 ‘Landscapes and habitats
of the Alps’ and SNSF Project 315230_130764/1. Financial support
was also received from FONDECYT Chile which made visits of
Southern Chile possible for the last author, and recently also for
F. Oehl (FONDECYT Project 11090014). The rst author also
thanks the family Giuanna Albin-Pelican (hostel in Surrein,
Surselva) for great hospitality during several collections at the
type location between 2003 and 2007. We are also grateful to Urs
Zihlmann (Agroscope ART) and our collaborators Claudia Maurer,
Andres Chervet and Wolfgang Sturny at the Bodenschutzfachstelle
of the Kanton Bern for the excellent support at the lowland sampling
sites.
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Address of the authors:
Fritz Oehl, Agroscope Reckenholz-Tänikon Research Station ART, Eco-
logical Farming Systems, Reckenholzstrasse 191, CH-8046 Zürich, Switzer-
land, E-mail:
fritz.oehl@art.admin.ch.
Claudia Castillo, Universidad Católica de Temuco, Facultad de Recursos
Naturales, Escuela de Agronomía, Casilla 15-D, Temuco, Chile.
David Schneider, Zurich-Basel Plant Science Center, Institute of Botany,
University of Basel, Hebelstrasse 1, CH-4056 Basel, Switzerland.
Verena Säle, Agroscope Reckenholz-Tänikon Research Station ART, Ecolo-
gical Farming Systems, Reckenholzstrasse 191, CH-8046 Zürich, Switzer-
land.
Ewald Sieverding, Institute of Plant Production and Agroecology in the
Tropics and Subtropics, University of Hohenheim, Garbenstrasse 13, D-
70593 Stuttgart, Germany.