Conclusions
This is the first study comparing community structure of fungi along
elevation gradients in the Neo- and Paleotropics. Climate, particularly
temperature, appears to be the driving factor shaping the distribution
of fungi along elevational gradients in a variety of ways, e.g., by
affecting microbial processes (e.g., decomposition), vegetation, and
edaphic factors, and by altering species interaction dynamics. Montane
forests are among the most vulnerable terrestrial ecosystems to climate
change and warming will undoubtedly affect fungal communities in these
ecosystems. Given the contrasting habitat preferences of several
taxonomic groups and the possible functional differences among them
within the broad functional guilds, future communities at a given site
may differ considerably from current ones not only in composition, but
also in functionality. Habitat specificity exhibited by many fungi
offers possibilities for monitoring and habitat characterization and we
advocate incorporating fungi in biodiversity assessments and
conservation efforts. With the accumulating spatial data points for
fungal taxa from metabarcoding studies, it will be possible in the near
future to determine the climatic niches and model the suitable habitats
for many fungi.
Acknowledgements
Financial support for the fieldwork was provided by E. Nouhra (SECYT
Universidad Nacional de Córdoba, 26/11; 162/12; 124/13), Naturalis and
Sabah Parks as part of the Kinabalu-Crocker Range expedition, and the
National Science Foundation (NSF) GoLife grant (DEB 1541548) to F.
Lutzoni. Molecular work was financed by a Naturalis Research Initiative
grant to J. Geml and the above NSF GoLife grant to F. Lutzoni. The
authors thank
staff members of all national parks, national reserves, provincial
parks, and provincial reserves sampled in Argentina, Malaysia and Panama
(listed in Table S1), the Panamanian Ministry of Environment in Panama,
and Sabah Biodiversity Center and Sabah Parks in Malaysia for issuing
access and export permits. The authors are grateful for the Fundación
ProYungas in Agentina, the Panamanian Institute for Scientific Research
and High Technology Services (INDICASAT-AIP) in Panama and Sabah Parks
and Universiti Malaysia Sabah (UMS) in Malaysia for providing logistical
support during fieldwork, and for Marcel Eurlings and Elza Duijm
(Naturalis) for conducting the Ion Torrent sequencing. J. Geml
acknowledges support by the MTA-EKE Lendület programme (no. 96049) of
the Támogatott Kutatócsoportok Irodája. The authors declare no conflict
of interest.
[dataset] Geml J; 2020; Soil metagenome; DDBJ/EMBL/GenBank;
KDPX01000000, KDPY01000000, and KDPZ01000000
REFERENCES
Aiba S, Kitayama K (1999) Structure, composition and species diversity
in an altitude-substrate matrix of rain forest tree communities on Mount
Kinabalu, Borneo. Plant Ecology , 140, 139–157.
Antonelli A (2015) Biodiversity: Multiple origins of mountain life.Nature , 524, 300–301.
Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal
endophytes: are tropical leaves biodiversity hotspots? Ecology ,88, 541–549.
Bagchi R, Gallery RE, Gripenberg S, Gurr SJ, Narayan L, Addis CE,
Freckleton RP, Lewis OT (2014) Pathogens and insect herbivores drive
rainforest plant diversity and composition. Nature , 506,85–88.
Bahram M, Põlme S, Kõljalg U, Zarre S, Tedersoo L (2012) Regional and
local patterns of ectomycorrhizal fungal diversity and community
structure along an altitudinal gradient in the Hyrcanian forests of
northern Iran. New Phytologist , 193, 465–473.
Bakker MR, Brunner I, Ashwood F et al . (2019) Belowground
biodiversity relates positively to ecosystem services of European
forests. Frontiers in Forests and Global Change , 2, 6
Barry RG (2008) Mountain Weather and Climate . Cambridge
University Press, Cambridge, UK.
Beaman JH, Anderson C (2004) The plants of Mount Kinabalu. 5.
Dicotyledon families Magnoliaceae to Winteraceae. Royal Botanic
Gardens, Kew.
Beaman JH, Beaman RS (1990) Diversity and distribution patterns in the
flora of Mount Kinabalu. In: Baas P, Kalkman P, Geesink R (eds.)The plant diversity of Malesia . Kulwar Academic Publishers,
Dordrecht, pp. 147–160.
Blake JG, Rougés M (1997) Variation in capture rates of understory birds
in El Rey National Park, Northwestern Argentina. Ornitología
Neotropical , 8, 185–193.
Bowman EA, Arnold AE. 2018. Distributions of ectomycorrhizal and foliar
endophytic fungal communities associated with Pinus ponderosaalong a spatially constrained elevation gradient. American Journal
of Botany , 105, 687–699.
Branco S, Gladieux P, Ellison C et al. (2015) Genetic isolation
between two recently diverged populations of a symbiotic fungus.Molecular Ecology , 24, 2747–2758
Brown AD, Grau HR, Malizia LR, Grau A (2001) Argentina. In: Kappelle M,
Brown AD, eds. Bosques nublados del neotrópico . INBio, Cambridge,
623–659.
Brown AD, Pacheco S, Lomáscolo T, Malizia LR (2005) Ecoregión Yungas:
situación ambiental en los bosques andinos yungueños. In: Brown AD,
Martinez Ortiz U, Acerbi M, Corcuera J, eds., Situación ambiental
Argentina , Fundación Vida Silvestre Argentina, Argentina, 53–72.
Cabrera A (1976) Regiones fitogeográficas de la República Argentina.Enciclopedia de Agricultura, Jardinería y Fruticultura ,2, 1–85.
Cardelús CL, Colwell RK, Watkins JE (2006) Vascular epiphyte
distribution patterns: explaining the mid-elevation richness peak.Journal of Ecology , 94, 144–156.
Clemmensen KE, Bahr A, Ovaskainen O et al. (2013) Roots and
associated fungi drive long-term carbon sequestration in boreal forest.Science , 339, 1615–1618.
Coince A, Cordier T, Lengellé J et al . (2014) Leaf and
root-associated fungal assemblages do not follow similar elevational
diversity patterns. PLOS ONE , 9, e100668
Condit R, Pérez R, Daguerre N (2011) Trees of Panama and Costa
Rica . Princeton University Press, Princeton, NJ, U.S.A.
Cordier T, Robin C, Capdeville X et al. (2012) The composition of
phyllosphere fungal assemblages of European beech (Fagus
sylvatica ) varies significantly along an elevation gradient. New
Phytologist , 196, 510–519.
Coughlan AP, Dalpé Y, Lapoint L, Piché Y (2000) Soil pH-induced changes
in root colonization, diversity, and reproduction of symbiotic
arbuscular mycorrhizal fungi from healthy and declining maple forests.Canadian Journal of Forest Research , 30, 1543–1554.
Davey ML, Heegaard E, Halvorsen K et al . (2013)
Amplicon-pyrosequencing-based detection of compositional shifts in
bryophyte-associated fungal communities along an elevation gradient.Molecular Ecology , 22, 368–383.
De Cáceres M, Legendre P, Wiser SK, Brotons L. 2012. Using species
combinations in indicator analyses. Methods in Ecology and
Evolution , 3, 973-982.
Dufrêne M, Legendre P (1997) Species assemblages and indicator species:
the need for a flexible assymetrical approach. Ecological
Monographs , 67, 345–366.
Edgar RC (2010) Search and clustering orders of magnitude faster than
BLAST. Bioinformatics , 26, 2460–2461.
Fernandez CW, Kennedy PG (2016) Revisiting the ‘Gadgil effect’: do
interguild fungal interactions control carbon cycling in forest soils?New Phytologist , 209, 1382–1394.
Gadgil RI, Gadgil PD (1971) Mycorrhiza and litter decomposition.Nature , 233, 133.
Gai JP, Tian H, Yang FY, Christie P, Li XL, Klironomos JN (2012)
Arbuscular mycorrhizal fungal diversity along a Tibetan elevation
gradient. Pedobiologia , 55, 145–151.
Geml J (2011) Coalescent analyses reveal contrasting patterns of
inter-continental gene flow in arctic-alpine and boreal-temperate fungi.
In: Fontaneto D, ed., Biogeography of microscopic organisms – Is
everything small everywhere? Cambridge University Press, 177–190.
Geml J (2017) Altitudinal gradients in mycorrhizal symbioses – the
current state of knowledge on how richness and community structure
change with elevation. In: Tedersoo L, ed., Ecological Studies:
Biogeography of Mycorrhizal Symbioses , Springer, 107–123.
Geml J (2019) Soil fungal communities reflect aspect-driven
environmental structuring and vegetation types in a Pannonian forest
landscape. Fungal Ecology , 39, 63–79.
Geml J, Pastor N, Fernandez L et al. (2014) Large-scale fungal
diversity assessment in the Andean Yungas forests reveals strong
community turnover among forest types along an altitudinal gradient.Molecular Ecology , 23 , 2452–2472.
Geml J, Morgado LN, Semenova-Nelsen TA, Schilthuizen M (2017) Changes in
richness and community composition of ectomycorrhizal fungi among
altitudinal vegetation types on Mount Kinabalu in Borneo. New
Phytologist , 215, 454–468.
Ghalambor CK, Huey RB, Martin PR, G. Wang (2006) Are mountain passes
higher in the tropics? Janzen’s Hypothesis Revisited. Integrative
and Comparative Biology , 46, 5–17.
Glassman SI, Wang IJ, Bruns TD (2017) Environmental filtering by pH and
soil nutrients drives community assembly in fungi at fine spatial
scales. Molecular Ecology , 26, 6969–6973.
Gómez-Hernández M, Williams-Linera G, Guevara R, Lodge DJ (2012)
Patterns of macromycete community assemblage along an altitudinal
gradient: options for fungal gradient and metacommunity analyses.Biodiversity and Conservation , 21, 2247–2268.
Gotelli NJ (1998) A Primer of Ecology . 2nd edition. Sinauer
Associates, Inc., Sunderland, MA.
Grau O, Grytnes JA, Birks HUB (2007) A comparison of elevational species
richness patterns of bryophytes with other plant groups in Nepal,
Central Himalaya. Journal of Biogeography , 34,1907–1915.
Grytnes JA, Beaman JH, Romdal TS, Rahbek C (2008) The mid-domain effect
matters: simulation analyses of range-size distribution data from Mount
Kinabalu, Borneo. Journal of Biogeography , 35,2138–2147.
Guo Q, Kelt DA, Sun Z et al. (2013) Global variation in
elevational diversity. Scientific Reports , 3, 300
Ihrmark K, Bödeker ITM, Cruz-Martinez K et al. (2012) New primers
to amplify the fungal ITS2 region – evaluation by 454-sequencing of
artificial and natural communities. FEMS Microbiology Ecology ,82, 666–677.
Javis SG, Woodward S, Taylor AFS (2015) Strong altitudinal partitioning
in the distributions of ectomycorrhizal fungi along a short (300 m)
elevation gradient. New Phytologist , 206, 1145–1155.
Kappelle M (2016) The Montane Cloud Forests of the Cordillera de
Talamanca. In: Kappelle M, ed., Costa Rican ecosystems . The
University of Chicago Press. Chicago, U.S.A., 451–491.
Kitayama K (1992) An altitudinal transect study of the vegetation on
Mount Kinabalu, Borneo. Vegetatio 102 : 149–171.
Kõljalg U, Nilsson RH, Abarenkov K et al. (2013) Towards a
unified paradigm for sequence-based identification of fungi.Molecular Ecology , 22, 5271–5277.
Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of
soil properties on the structure of bacterial and fungal communities
across land-use types. Soil Biology and Biochemistry ,40, 2407–2415.
Lavilla EO, Manzano AS (1995) La batracofauna de las selvas de montaña
del noroeste argentine. In: Brown AD, Grau HR, eds. Investigación,
conservación y desarollo en las selvas subtropicales de montaña .
Laboratorio de Investigaciones Ecológicas de las Yungas, UNT, Tucumán,
157–162.
Liew TS, Schilthuizen M, Lakim MB (2010) The determinants of land snail
diversity along a tropical elevational gradient: insularity, geometry
and niches. Journal of Biogeography , 37, 1071–1078.
Lomolino MV (2001) Elevation gradients of species-density: historical
and prospective views. Global Ecology and Biogeography ,10, 3–13.
Malizia L, Pacheco S, Blundo C, Brown AD (2012) Caracterización
altitudinal, uso y conservación de las Yungas subtropicales de
Argentina. Ecosistemas , 21, 53–73.
McCain CM (2009) Global analysis of bird elevational diversity.Global Ecology and Biogeography , 19, 346–360.
McCain CM, Grytnes JA (2010) Elevational Gradients in Species Richness.
In: Encyclopedia of Life Sciences (ELS) . John Wiley & Sons, Ltd:
Chichester. doi: 10.1002/9780470015902.a0022548
Meier CL, Rapp J, Bowers RM, Silman M, Fierer N (2010) Fungal growth on
a common wood substrate across a tropical elevation gradient:
Temperature sensitivity, community composition, and potential for
above-ground decomposition. Soil Biology and Biochemistry ,42, 1083–1090
Merckx VSFT, Hendriks KP, Beentjes KK, Mennes CB, Becking LE,
Peijnenburg KTCA, Afendy A, Arumugam N, de Boer H, Biun A, et al.(2015) Evolution of endemism on a young tropical mountain.Nature , 524, 347–350.
Miyamoto Y, Nakano T, Hattori M, Nara K (2014) The mid-domain effect in
ectomycorrhizal fungi: range overlap along an elevation gradient on
Mount Fuji, Japan. ISME Journal , 8, 1739–1746.
Mueller GM, Halling RE, Carranza J, Mata M, Schmit JP (2006)
Saprotrophic and ectomycorrhizal macrofungi of Costa Rican oak forests.Ecological Studies , 185, 55–68.
Nevarez L, Vasseur V, Le Madec L et al. (2009) Physiological
traits of Penicillium glabrum strain LCP 08.5568, a filamentous
fungus isolated from bottled aromatised mineral water.International Journal of Food Microbiology , 130,166–171.
Nguyen NH, Song Z, Bates SC et al. (2015) FUNGuild: An open
annotation tool for parsing fungal community datasets by ecological
guild. Fungal Ecology , 20, 241–248.
Nor SMD (2001) Elevational diversity patterns of small mammals on Mount
Kinabalu, Sabah, Malaysia. Global Ecology and Biogeography ,10, 41–62.
Nouhra E, Urcelay C, Longo S, Fontenla S (2012) Differential hypogeous
sporocarp production from Nothofagus dombeyi and N.
pumilio forests in southern Argentina. Mycologia , 104,45–52.
Nouhra E, Soteras F, Pastor N, Geml J (2018) Richness, community
composition and functional groups of Agaricomycetes along a vegetation
and elevational gradient in the Andean Yungas of Argentina.Biodiversity and Conservation , 8, 1849–1871.
Ojeda RA, Mares MA (1989) A biogeographic analysis of the mammals
of Salta Province, Argentina: Patterns of species assemblage in the
Neotropics . Texas Tech University Press, Lubbock, Texas, U.S.A.
Oksanen J, Blanchet FG, Kindt R et al . 2015. Vegan:
Community Ecology Package . Version 2.3-2. http://cran.r-project.org.
http://vegan.rforge.r-project.org/.
Parris BS, Beaman RS, Beaman JH (1992) The plants of Mount
Kinabalu. 1. Ferns and fern allies. Royal Botanic Gardens, Kew.
Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring
ectomycorrhizal fungal dispersal: macroecological patterns driven by
microscopic propagules. Molecular Ecology , 16,4122–4136.
Perrigo A, Hoorn C, Antonelli A (2020) Why mountains matter for
biodiversity. Journal of Biogeography , 47, 315–325.
Porter WM, Robson AD, Abbott LK (1987) Field survey of the distribution
of Vesicular-arbuscular mycorrhizal fungi in relation to soil pH.Journal of Applied Ecology , 24, 659–662.
Prada CM, Morris A, Andersen KM (2017) Soils and rainfall drive
landscape‐scale changes in the diversity and functional composition of
tree communities in premontane tropical forest. Journal of
Vegetation Science , 28, 859–870.
Prado DE (2000) Seasonally dry forests of tropical South America: from
forgotten ecosystems to a new phytogeographic unit. Edinburgh
Journal of Botany , 57, 437–461.
Rahbek C (2005) The role of spatial scale and the perception of
large-scale species-richness patterns. Ecology Letters ,8, 224–239.
Rincón A, Santamaría-Pérez B, Rabasa SG, Coince A, Marçais B, Buée M
(2015) Compartmentalized and contrasted response of ectomycorrhizal and
soil fungal communities of Scots pine forests along elevation gradients
in France and Spain. Environmental Microbiology , 17,3009–3024
Rosenzweig ML (1995) Species diversity in space and time .
Cambridge University Press, Cambridge.
Rousk J, Bååth E, Brookes PC et al. (2010) Soil bacterial and
fungal communities across a pH gradient in an arable soil. The
ISME Journal , 4, 1340–1351.
Schön ME, Nieselt K, Garnica S (2018) Belowground fungal community
diversity and composition associated with Norway spruce along an
altitudinal gradient. PLOS ONE , 13, e0208493.
Semenova TA, Morgado LN, Welker JM, Walker MD, Smets E, Geml J (2015)
Long-term experimental warming alters community composition of
ascomycetes in Alaskan moist and dry arctic tundra. Molecular
Ecology , 24, 424–437.
Shearer CA, Zelski SE, Raja HA, Schmit JP, Miller AN, Janovec JP (2015)
Distributional patterns of freshwater ascomycetes communities along an
Andes to Amazon elevational gradient in Peru. Biodiversity and
Conservation , 24, 1877–1897.
Spehn EM, Rudmann-Maurer K, Körner C (2012) Mountain biodiversity.Plant Ecology and Diversity , 4, 301–302.
Stevens GC (1992) The elevational gradient in elevational range: an
extension of Rapoport’s latitudinal rule to altitude. American
Naturalist , 140, 893–911.
Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijensundera R, Ruiz
LV, Vasco-Palacios AM, Thu QP, Suija A, et al. (2014) Global
diversity and geography of soil fungi. Science , 346,1256688.
Větrovský T, Kohout P, Kopecký M, et al. (2019) A meta-analysis
of global fungal distribution reveals climate-driven patterns.Nature Communications , 10, 1–9.
Wheeler KA, Hurdman BF, Pitt JI (1991) Influence of pH on the growth of
some toxigenic species of Aspergillus , Penicillium andFusarium . International Journal of Food Microbiology ,12, 141–150.
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct
sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis
MA, Gelfand DH, Sninsky JJ, White TJ, eds. PCR Protocols: A Guide
to Methods and Applications . Academic Press, Inc., New York, 315–322.
Wicaksono CY, Aguirre Gutierrez J, Nouhra ER, Pastor N, Raes N, Pacheco
S, Geml J (2017) Contracting montane cloud forests: a case study of the
Andean alder (Alnus acuminata ) and associated fungi in the
Yungas. Biotropica , 49, 141–152.
Wood JJ, Beaman RS, Beaman JH (1993) The plants of Mount Kinabalu.
2. Orchids. Royal Botanic Gardens, Kew, London, U.K.