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461
© The Ecological Society of America www.frontiersinecology.org
Is climate change altering
the geographic distribution
of truffles?
Peer-reviewed letter
Truffles (Tuber spp) – the aromatic
fruiting bodies of fungi that grow
underground and symbiotically colo-
nize the roots of hazels, oaks, and
other trees or shrubs – are a luxury
food item, with prices often compa-
rable to those of caviar. The exorbi-
tant prices of truffles reflect a
decreasing worldwide production
(Hall et al. 2003) and an increasing
international demand. By mostly
relying on a rare occurrence of the
Burgundy truffle (Tuber uncinatum
syn T aestivum; Paolocci et al. 2004;
Wedén et al. 2005) (Figure 1a) in
southwest Germany, Büntgen et al.
(Front Ecol Environ 2011; 9[3]:
150–151) speculated that climate
change has expanded the species’
geographic distribution. Here, on the
basis of historical data and an updated
distribution map of the Burgundy
truffle, we offer an alternative view to
Büntgen et al.’s hypothesis.
Historical evidence suggests that
truffles were present throughout
Europe well before late 19th-century
climate change. Since the 17th cen-
tury, truffles have been harvested in
regions of the UK, Slovakia, Poland,
Austria, and Germany (Robinson
1691–1693; Brückmann 1730;
Rittersma 2010, a and b). The sudden
interest in truffles outside of tradi-
tional truffle-consuming countries
like France and Italy resulted from
the emergence of the court society,
which reached its zenith between
1648 and 1789 (Rittersma 2010b).
During the 19th century, Germany
emerged as a truffle-consuming
nation that contributed to the myco-
logical, culinary, and commercial
spectrum of the European truffle tra-
dition of that time (Figure 1b;
Rittersma 2010a). This clearly
demonstrates that truffles’ perception
and appreciation in Germany and
elsewhere in Northern Europe has
been strongly determined by culture.
The natural habitat of the Burgundy
truffle covers Europe (WebFigure 1a,
based on data from Chevalier and
Frochot [1997] and Splivallo et al.
[2012]). Büntgen et al.’s distribution
map, which limited the occurrence of
the Burgundy truffle to a few European
sites, is incomplete, perhaps because
the authors attempted to distinguish
summer Burgundy truffles from winter
Burgundy truffles. If so, this distinction
has no taxonomical relevance because
winter and summer Burgundy truffles
are a single species (Paolocci et al.
2004; Wedén et al. 2005) and have
similar aromas (Splivallo et al. 2012).
The Burgundy truffle’s European-wide
distribution indicates that the species
can adapt to a broad temperature
range. In beetles, upper thermal toler-
ance has been positively linked to the
extent of geographic ranges (Calosi
et al. 2010); similarly, the high toler-
ance of the Burgundy truffle to both
high and low temperatures suggests
that, contrary to the hypothesis of
Büntgen et al., climate change might
have a minimal effect on its geo-
graphic distribution.
In wines, a few growing regions (eg
Bordeaux) traditionally dominated
the market until the emergence of
global competition in the 20th cen-
tury. A similar trend is currently hap-
pening with truffles, the market for
which has been overshadowed in
recent decades by the two most
expensive species: the Piedmont (T
magnatum, ~ €5000 kg–1) and the
Périgord (T melanosporum, ~ €2500
kg–1) truffle. Being three to ten times
cheaper and more widely distributed
than the latter two species, the
Burgundy truffle offers an attractive
and readily available substitute. The
increase in Burgundy truffle demand
throughout Europe can be attributed
in part to the recent creation of
numerous truffle grower/hunter asso-
ciations (eg The German Truffle
Association [www.ahrtrueffel.com],
The Swiss Burgundy Truffle Associa-
tion [www.uncinatum.ch/web], The
Hungarian Truffle Growers Associa-
tion [www.szarvasgombaegyesulet.hu]).
These associations contribute to rais-
ing public awareness of the Burgundy
truffle by conducting educational
efforts, organizing events (eg truffle
tastings), and supporting the estab-
lishment of truffle orchards.
Truffles might have colonized
Europe about 10 000 years ago, after
the last glacial period, as documented
for the Périgord truffle (Murat et al.
2004). This hypothesis has not yet
been tested for the Burgundy truffle.
Geographic and genetic distance were
not correlated when considering all
eight populations in our study (Web-
Figure 1); however, a significant cor-
relation was observed when consider-
ing only the five populations on the
gradient from the South of France
toward the UK. This indicates that
the overall European distribution of
the Burgundy truffle does not result
from isolation caused by distance (ie
not attributable to range expansion);
however, species range expansion
might have happened northward from
southern France toward the UK.
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Figure 1. (a) Characteristic morphology of the Burgundy truffle, Tuber uncinatum.
The inside tissue (or gleba, left) bears mature spores and is light brown with characteristic
white veins, whereas the outer layer (or peridium, right) is melanized and black. (b) 19th-
century illustration of women carrying baskets filled with truffles in Baden, in
southwestern Germany (from Dumaine J-M. 2010. Trüffeln, die heimischen Exoten).
(a) (b)
© Aarau/München: AT Verlag
462
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Considering that truffles were har-
vested throughout Europe during
the 17th century, the Burgundy
truffle might have, similarly to the
Périgord truffle (Murat et al. 2004),
recolonized Europe from some
southern refugia, possibly following
the last ice age. The observed corre-
lation is not necessarily evidence of
a climate-driven range expansion,
however, given that other factors
(eg competition with other fungi,
shift in host-plant range) might
lead to such a finding. Clearly, more
specimens and a more comprehen-
sive approach, accounting for all
variables (eg climate, soil, associ-
ated species), will be needed to
identify the possible driving forces
behind the Burgundy truffle’s cur-
rent distribution.
Here, our analysis suggests that cli-
mate change that started in the late
19th century has had little effect on
the present distribution of the
Burgundy truffle. Büntgen et al.’s
conclusions might nevertheless
apply to other truffle species with
narrower ranges and higher commer-
cial values (eg Périgord or Piedmont
truffles). If climate does limit the dis-
tribution of the latter two species,
even the slight warming in northern
Europe envisioned by Büntgen et al.
might induce northern expansion. In
addition to temperature, other fac-
tors – including precipitation, soil
properties (Chevalier et al. 2001),
and mating type (Rubini et al. 2011)
– determine whether truffles produce
fruiting bodies. Successful truffle cul-
tivation will consequently succeed
only if truffle orchard management
shifts from current empirical prac-
tices to practices based on scientific
evidence. Increasing temperatures
alone will not be sufficient for suc-
cessful truffle cultivation in more
northern parts of Europe.
Richard Splivallo1*, Rengenier
Rittersma2, Nayuf Valdez1, Gérard
Chevalier3, Virginie Molinier4,
Daniel Wipf4, and Petr Karlovsky1
1Molecular Phytopathology and
Mycotoxin Research, University of
Goettingen, Goettingen, Germany
*(ricsi17@hotmail.com);
2Beltheim-Heyweiler, Germany;
3Résidence Cristelle, Cournon
d’Auvergnes, France; 4UMR 1347
Agroécologie AgroSup/INRA/uB, Pôle
IPM CNRS ERL 6300, Dijon, France
Brückmann FE. 1730. Epistolae itinerar-
ium XX: de tuberibus terrae.
Wolfenbüttel, Germany.
Calosi P, Bilton DT, Spicer JI, et al. 2010.
What determines a species’ geo-
graphical range? Thermal biology
and latitudinal range size relation-
ships in European diving beetles
(Coleoptera: Dytiscidae). J Anim Ecol
79: 194–204.
Chevalier G and Frochot H. 1997. La
truffe de Bourgogne: Tuber uncinatum
Chatin. Levallois-Perret, France: Edi-
tions Pétrarque.
Chevalier G, Gregori G, Frochot H, and
Zambonelli A. 2001. The cultivation of
the Burgundy truffle. In: Bencivenga M
and Granetti B (Eds). Proceedings of the
Second International Conference on
Edible Mycorrhizal Mushrooms. 3–6 Jul
2001. Spoleto, Italy: Comunità Montana
dei Monti Martani e del Serano.
Hall IR, Yun W, and Amicucci A. 2003.
Cultivation of edible ectomycorrhizal
mushrooms. Trends Biotechnol 21:
433–38.
Murat C, Díez J, Luis P, et al. 2004.
Polymorphism at the ribosomal DNA
ITS and its relation to postglacial re-
colonization routes of the Perigord
truffle Tuber melanosporum. New Phytol
164: 401–11.
Paolocci F, Rubini A, Riccioni C, et al.
2004. Tuber aestivum and Tuber uncina-
tum: two morphotypes or two species?
FEMS Microbiol Lett 235: 109–15.
Rittersma RC. 2010a. Die verspätete
Trüffelnation. Zu Geschichte, Gegen-
wart und Zukunft der Trüffel in
Deutschland. In: Dumaine JM and
Wojtko N (Eds). Trüffeln: die heimis-
chen Exoten. Aarau/München, Ger-
many: AT Verlag.
Rittersma RC. 2010b. Only the sky is the
limit of the soil. Manifestations of truf-
fle mania in Northern Europe in the
18th century. In: Bencivenga M and
Granetti B (Eds). Proceedings of the
Second International Conference on
Edible Mycorrhizal Mushrooms. 3–6
Jul 2001. Spoleto, Italy: Comunità
Montana dei Monti Martani e del
Serano.
Robinson T. 1691–1693. An account of
the Tubera Terrae, or truffles found at
Rushton in Northamptonshire. Philos
T Roy Soc London 7: 824–26.
Rubini A, Belfiori B, Riccioni C, et al.
2011. Tuber melanosporum: mating type
distribution in a natural plantation and
dynamics of strains of different mating
types on the roots of nursery-inocu-
lated host plants. New Phytol 189:
723–35.
Splivallo R, Valdez N, Kirchhoff N, et al.
2012. Intraspecific genotypic variabil-
ity determines concentrations of key
truffle volatiles. New Phytol 194:
823–35.
Wedén C, Danell E, and Tibell L. 2005.
Species recognition in the truffle genus
Tuber – the synonyms Tuber aestivum
and Tuber uncinatum. Environ Microbiol
7: 1535–46.
doi:10.1890/12.WB.020
Illuminating the mysterious
world of truffles
On the basis of discovering ~2 kg of
truffles (belonging to several Tuber
spp, including a >410-g mature Bur-
gundy truffle [T aestivum syn uncina-
tum]) at >70 sites in southwest
Germany, we postulated in our origi-
nal letter that ongoing climate change
was one possible factor contributing to
species-specific range shifts, as well as
to variation in fruiting body produc-
tion and maturation, in truffles.
A warming-induced extension of
the growing period – together with
redistributed precipitation regimes –
was hypothesized to likely affect the
optimum rather than the entire distri-
bution of individual truffle species.
The detection of not only T aestivum
but also T brumale, T excavatum, T
fulgens, T macrosporum, T mesenter-
icum, and T rufum in the same region
and at the same time, together with
substantial temperature anomalies,
suggested that climatic effects were
involved. Associated environmental
changes may have impacted condi-
tions at local to regional scales but did
not necessarily shift the geographic
scope of entire ecosystems. Our
“hypogeous evidence”, in line with
European-wide myco-phenological
observations (Kauserud et al. 2012),
supports a reported long-term decline
in Périgord black truffle (T melanospo-
rum) harvests across its natural and
cultivated Mediterranean habitats
(Hall et al. 2003; Mello et al. 2006). A
possible reason for this southern
European truffle yield decrease is a loss
in soil moisture.
Nevertheless, we agree with Spli-
© The Ecological Society of America www.frontiersinecology.org
R Splivallo et al. – Supplementary information
WebFigure 1. Geographic distribution and population genetics of Tuber uncinatum. (a)
Countries in which the Burgundy truffle naturally occurs are marked with black circles
(based on reports by Chevalier and Frochot [1997] and Splivallo et al. [2012]). Colored
circles represent the locations of the populations (the number of samples are indicated
inside the circles) used for the genetics study presented here. Background map is available
on Wikimedia Commons (Ssolbergj). Genetic fingerprints were generated by amplified
fragment length polymorphism (AFLP) for the samples depicted by colored circles (as
described in Splivallo et al. [2012]). (b) Dendrogram (unweighted pair group method
with arithmetic mean) based on AFLP data for 14 Burgundy truffle samples collected
from six countries. Black triangles indicate nodes >80% (2000 bootstraps). The Mantel
test did not reveal a significant correlation (P= 0.413, r= 0.028, 10 000 permutations)
between genetic distances (using Jaccard’s distances = 1 – Jaccard’s similarity coefficient)
and geographic distances (log kilometers) among the eight populations depicted in color on
the map. Results of the Mantel test, however, were significant when considering the five
populations on a north–south gradient from southern France toward the UK (P= 0.008,
r= 0.645, 10 000 permutations; http://ibdws.sdsu.edu/; Jensen et al. 2005).
nWebReferences
Chevalier G and Frochot H. 1997. Latruffe de Bourgogne: Tuber
uncinatum Chatin. Levallois-Perret, France: Editions
Pétrarque.
Jensen JL, Bohonak AJ, and Kelley ST. 2005. Isolation by dis-
tance, web service. BMC Genet 6: 13.
Splivallo R, Valdez N, Kirchhoff N, et al. 2012. Intraspecific
genotypic variability determines concentrations of key truf-
fle volatiles. New Phytol 194: 823–35.