Comparative sampling of Neotropical
and Paleotropical elevation gradients reveals the role of climate in
shaping the functional and taxonomic composition of soil-borne fungal
communities in tropical forests
Running title: Tropical montane fungi
József Geml1,2*, A. Elizabeth
Arnold3, Tatiana A.
Semenova-Nelsen1, Eduardo R.
Nouhra4, Luis N. Morgado1,5, Oriol
Grau6,7, Alicia Ibáñez3, Balázs
Hegyi8,9, François Lutzoni10
1Naturalis Biodiversity Center, Darwinweg 2, P.O. Box
9517, 2300 RA Leiden, The Netherlands
2MTA-EKE Lendület Environmental Microbiome Research
Group, Eszterházy Károly University, Leányka u. 6, H-3300 Eger, Hungary.
3School of Plant Sciences and Department of Ecology
and Evolutionary Biology, University of Arizona, Tucson, AZ, U.S.A.
4Instituto Multidisciplinario de Biología Vegetal
(IMBIV), CONICET, FCEFyN, Universidad Nacional de Córdoba, Av. Vélez
Sarsfield 1611, CC 495, 5000 Córdoba, Argentina
5Department of Biosciences, Faculty of Mathematics and
Natural Sciences, University of Oslo, Oslo, Norway
6CREAF, Global Ecology Unit, 08193, Cerdanyola del
Vallès, Catalonia, Spain
7Cirad, UMR EcoFoG (AgroParisTech, CNRS, Inra, Univ.
Antilles, Univ. Guyane), Campus Agronomique, 97310 Kourou, French Guiana
8Innoregion Knowledge Centre, Eszterházy Károly
University, Leányka u. 6, H-3300 Eger, Hungary.
9Doctoral School of Earth Science and Department for
Landscape Protection and Environmental Geography, University of
Debrecen, Egyetem tér 1, H-4002 Debrecen, Hungary.
10Department of Biology, Duke University, Durham, NC,
27708 U.S.A.
*Corresponding author, address:
MTA-EKE Lendület Environmental Microbiome Research Group, Eszterházy
Károly University, Leányka u. 6, H-3300 Eger, Hungary
Phone: (+36) 36 523-456; E-mail: jozsef.geml@gmail.com,
geml.jozsef@uni-eszterhazy.hu
Abstract
Because of their steep gradients in abiotic and biotic factors,
mountains offer an ideal setting to enhance our understanding of
mechanisms that underlie species distributions and community assemblies.
We compared the structure of taxonomically and functionally diverse soil
fungal communities in soils along elevational gradients in the Neo- and
Paleotropics (northern Argentina, Central America, and Borneo). We found
that soil fungal community composition reflects environmental factors at
both regional and pantropical scales, particularly temperature and soil
pH. Elevational turnover is driven by contrasting environmental
preferences among functional groups and replacement of species within
functional guilds. In addition, we found that habitat preference can
already be observed at the level of taxonomic orders, often irrespective
of functional guild, which suggests shared physiological constraints and
environmental optimum for relatively closely related taxa. Strong
biogeographic structure likely reflects dispersal limitation and
resulting differences in local species pools of fungi, as well as their
hosts or substrates. Although the number of species shared among regions
is low, remarkable similarity of functional profiles across regions
suggests functional niche proportions may be driven by similar
mechanisms across moist tropical forests, resulting in relatively
predictable proportions of functional guilds. The pronounced
compositional and functional turnover along elevation gradients driven
mainly by temperature and correlated environmental factors implies that
tropical montane forest fungi will likely be sensitive to climate
change, resulting in variation in composition and functionality over
time.
Key Words: Argentina, Borneo, ITS, DNA metabarcoding, Panama, soil fungi
INTRODUCTION
Montane ecosystems generally are recognized as biodiversity hotspots as
well as areas of high endemism (Lomolino 2001). Despite representing
about one-eighth of the world’s land area outside Antarctica, mountains
harbor about one-third of all terrestrial species (Spehn et al .
2012; Antonelli 2015). Since the early scientific studies of Darwin,
Wallace and von Humboldt on mountain biota, documentation of changes in
species richness and community composition have been central to
ecological and biogeographic studies (Lomolino 2001; McCain and Grytnes
2010). Mountains provide unique opportunities to test various ecological
hypotheses, such as those relevant to climate change, as they are
characterized by gradients of abiotic factors such as temperature and
available moisture (Guo et al. 2013). However, in most organismal
groups we still lack answers to fundamental questions regarding
diversity, distributional patterns, and community composition in montane
systems (Lomolino 2001; Guo et al. 2013; Perrigo et al.2020).
Numerous abiotic factors that shape biological communities change more
or less predictably with increasing elevation. Among these, temperature
is the most predictable, with an average decrease of ca. 0.6 °C per 100
m increase in elevation (Barry 2008). Despite the crucial importance of
water for living organisms, changes in precipitation along elevation
gradients are much less predictable in general due to complex
relationships of regional climate and topography (Barry 2008). In mid-
and high latitudes, precipitation tends to increase with elevation,
whereas tropical mountains typically show little variation in rainfall
along an elevation gradient or exhibit a moderate mid-elevation peak
(McCain and Grytnes 2010). Related environmental factors interplay with
temperature and precipitation to determine biological productivity,
including solar radiation, cloud cover, soil type and nutrient content,
as well as habitat surface area due to geometric constraints (Stevens
1992; Rosenzweig 1995). For example, cloud forests, perhaps the most
characteristic vegetation of tropical montane habitats, are
characterized by largely persistent clouds at mid- to high elevations.
Organisms occupy different habitats along elevation gradients according
to their physiological requirements for abiotic factors and their
interaction dynamics with other species. Resulting changes in community
structure with increasing elevation have been a focal point for
ecological and evolutionary research and have contributed to the
understanding of spatial patterns of biodiversity and their underlying
mechanisms.
On a global scale, most studies of species richness along elevation
gradients have focused on vascular plants and animals (e.g., Parriset al. 1992; Wood et al. 1993; Nor 2001; Cardelús et
al. 2006; Ghalambor et al. 2006; Grau et al . 2007;
Grytnes et al. 2008; Liew et al . 2010). Fungi represent
one of the largest groups of living organisms with key roles in the
functioning of ecosystems, and their importance is increasingly
recognized with respect to food safety and human health. Several studies
have been conducted in mountains in temperate regions on the
distribution of specific fungal functional groups: phyllosphere fungi
(Cordier et al. 2012; Coince et al . 2014),
bryophyte-associated fungi (Davey et al. 2013), wood-inhabiting
fungi (Meier et al. 2010), arbuscular mycorrhizal (AM) fungi (Gaiet al. 2012), and ectomycorrhizal (ECM) and other root-associated
fungi (Bahram et al. 2012; Nouhra et al. 2012; Coinceet al. 2014; Miyamoto et al . 2014; Javis et al.2015; Rincón et al. 2015; Bowman and Arnold 2018; Schön et
al . 2018). However, species richness and composition of fungal
communities in tropical mountains remain virtually unknown. This gap in
our knowledge seems particularly concerning because fungi have been
reported as major drivers of the diversity and composition of plant
communities in tropical forests (Bagchi et al. 2014) and because
fungi, through their interactions with plants, contribute to ecosystem
services such as the provision of clean water, food and air (Bakkeret al . 2019). The few studies that have examined fungi in
tropical mountains were reviewed recently by Geml (2017). These include
morphological studies of macrofungi in eastern Mexico (Gómez-Hernándezet al. 2012) and freshwater ascomycetes in the Peruvian Andes
(Shearer et al. 2015), environmental DNA studies of total fungal
communities (Geml et al. 2014) and AM fungi (Geml 2017) in the
Tucuman-Bolivian Yungas, and AM fungi (Merckx et al. 2015) and
ECM fungi (Geml et al. 2017) in Malaysian Borneo. Consequently,
alpha and beta diversity of a wide range of fungal groups in tropical
mountains remain mostly unexplored.
In this study, we compared community composition and richness of diverse
functional groups of fungi in forest soils along elevation gradients in
three tropical mountain areas: Mt. Kinabalu and Crocker Range in Sabah,
Malaysian Borneo; the rainforests of western Panama; and the Andean
Yungas in northwestern Argentina. The aims of this work were to 1)
characterize soil fungal communities in major elevational forest types;
2) compare elevation patterns of richness in taxonomic and functional
groups of fungi among Neotropical and Paleotropical mountains; 3)
evaluate the possible influence of climatic and edaphic factors on
fungal community composition in tropical mountains; and 4) provide the
first characterization of Pantropical core mycobiomes in soils of
lowland and montane forests.
We hypothesized that elevation gradients would structure fungal
communities through changes in temperature and precipitation, reflecting
effects on soil edaphic variables and plant community composition.
Fungal richness and distribution on a global scale is strongly
influenced by mean annual temperature (MAT), mean annual precipitation
(MAP), soil pH, and, in the case of ECM fungi, by diversity and
abundance of host plants (Tedersoo et al . 2014; Větrovskýet al. 2019). Therefore, we expected MAT, MAP, and soil pH to be
the strongest drivers of fungal community structure along the sampled
elevation gradients irrespective of geographic region (Hypothesis 1). We
also hypothesized that elevational patterns of community structure would
differ among functional groups, reflecting different environmental
optima corresponding to distinct life strategies and resulting in
differences in inferred functionality among elevation zones (Hypothesis
2). For example, we expected fungi not associated with plants to be less
affected by vegetation type than those intimately associated with
plants, such as ECM, plant pathogens, root-associated fungi, and to some
extent wood decomposers, resulting in greater differences in richness
and community composition for plant-associated fungi among elevational
forest types (Hypothesis 2a). In addition, we expected higher species
richness of plant pathogens, wood decomposers and generalist saprotrophs
at lower elevations due to higher host- and substrate richness at low to
mid-elevations (Rahbek 2005, McCain and Grytnes 2010, Nouhra et
al. 2018) and more energy available for decomposition (Hypothesis 2b).
Finally, we expected fungal species pools to be different among the
three biogeographic regions due to distinct biogeographic histories,
with substantially more overlap between the two Neotropical regions due
to land connection and consequent similarities in flora and fauna
(Hypothesis 3).
Materials and Methods
We analyzed data from three datasets. Two of these are novel: Borneo and
Panama, except for a small subset of the data representing ECM fungi
from Borneo published by Geml et al. (2017). These were combined
with the Yungas dataset from northwestern Argentina originally published
by Geml et al . (2014), which is re-analyzed here.
In Argentina, the Yungas comprise tropical and subtropical humid montane
forests developed on the eastern slopes of the Andes as a result of
orographic rains. The flora and fauna of the Yungas have been relatively
well studied and are very diverse and rich in endemics (e.g., Ojeda and
Mares 1989; Lavilla and Manzano 1995; Blake and Rougés 1997; Brownet al. 2001). Together with adjacent, seasonally dry piedmont
forests, the Yungas constitute the southern limit of the Amazonian
biogeographic domain (Cabrera 1976; Prado 2000). The forests in this
region are classified into three major elevational types: piedmont
forest (400–700 masl), montane forest (700–1500 masl), and montane
cloud forest (1500–3000 masl) (Brown et al. 2001; Brown et
al. 2005), here considered as lowland, low montane and upper montane
forests, respectively, for comparative purposes.
In Borneo, the Crocker Range is the highest mountain range in Sabah
(Malaysia) with an average height of ca. 1800 masl. With an elevation of
4095 masl, Mt. Kinabalu is the tallest mountain between the Himalayas
and New Guinea. Mount Kinabalu has one of the most species-rich biotas
of the world, and includes more than 5000 vascular plant species (Beaman
and Anderson 2004). The vegetation of Mt. Kinabalu can be divided into
four discrete zones: lowland dipterocarp forests (< 1200
masl), montane forests (1200–2700 masl), ultramafic rock forests
(2700–3000 masl), and granite boulder forests of the summit zone
(3000–4095 masl) (Beaman and Beaman 1990; Kitayama 1992). Of these,
only dipterocarp forests and montane forests occur in other parts of the
Crocker Range. For this paper, ultramafic rock forest samples were
excluded because the vegetation is not typical for the elevation zone:
it is made up of a relatively small number of plant species capable of
surviving serpentine soils that are poor in nutrients and rich in heavy
metals. For comparisons with the other regions, the dipterocarp,
montane, and granite boulder forests were labelled as lowland, lower
montane and upper montane forests, respectively.
Panama and neighboring countries in Central and South America represent
a biodiversity hotspot that is one of the richest in the world. With
respect to trees alone, at least 2300 species are known to occur in
Panama (Condit et al . 2011). The Caribbean side of the isthmus
and the central mountains receive more than 3000 mm precipitation per
year. The Pacific side tends to be somewhat drier, but there is greater
regional variation in rainfall, resulting in a mosaic of wet
(>3000 mm per year), moist (1500-3000 mm per year), and dry
(<1500 mm per year) forests. The major forest types sampled in
this study were classified as lowland wet and moist forests (0–800
masl), lower montane forest (800–1500 masl), and upper montane forests
(1500–3000 masl) (Condit et al . 2011).