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Intra‐specific variation in tree growth responses to neighborhood composition and seasonal drought in a tropical forest

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1. Functional traits are expected to provide insights into the abiotic and biotic drivers of plant demography. However, successfully linking traits to plant demographic performance likely requires the consideration of important contextual and individual‐level information that is often ignored in trait‐based ecology. 2. Here, we modeled 8 years of growth from 1,138 individual trees from 36 tropical rain forest species. We compared models of tree growth parameterized using individual‐level versus species mean trait data. We also compared models that considered regional climatic, local biotic and whole‐plant allocation contexts to those that do not. 3. Our analyses show that growth models parameterized using individual‐level trait information outperformed those that used species mean trait information and that these models often contradicted one another indicating that the common practice of using species mean trait data requires more scrutiny. Additionally, we found that models including climatic, biotic and allocation contexts outperformed those that did not and provide nuanced insights into the drivers of tree growth in a tropical forest. 4. Synthesis. Here, we have shown that the development of models of tree demographic performance upon the basis of traits can be improved through a consideration of individual‐level trait variation as well as phenotypic and climatic contexts. We highlight that our ability to understand the drivers of tree population and community structure and dynamics in current and in future climates will be limited if contextual and individual‐level data remains understudied.
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Investigating the direct and indirect effects of
forest fragmentation on plant functional
Jenny ZambranoID
*, Norbert J. Cordeiro
, Carol Garzon-Lopez
, Lauren Yeager
Claire FortunelID
, Henry J. Ndangalasi
, Noelle G. BeckmanID
1School of Biological Sciences, Washington State University, Pullman, Washington, United States of
America, 2Department of Biology (mc WB 816), Roosevelt University, Chicago, Illinois, United States of
America, 3Science & Education, The Field Museum, Chicago, Illinois, United States of America, 4Grupo de
´a y Fisiologı
´a Vegetal, Departamento de Ciencias biolo
´gicas, Universidad de los Andes, Bogota
Colombia, 5Department of Marine Science, University of Texas at Austin, Port Aransas, Texas, United
States of America, 6Department of Ecology and Evolutionary Biology, University of California, Los Angeles,
California, United States of America, 7AMAP (botAnique et Mode
´lisation de l’Architecture des Plantes et des
´tations), Universite
´de Montpellier, CIRAD, CNRS, INRAE, IRD, Montpellier, France, 8Botany
Department, University of Dar es Salaam, Dar es Salaam, Tanzania, 9Department of Biology & Ecology
Center, Utah State University, Logan, Utah, United States of America
Ongoing habitat loss and fragmentation alter the functional diversity of forests. Generalising
the magnitude of change in functional diversity of fragmented landscapes and its drivers is
challenging because of the multiple scales at which landscape fragmentation takes place.
Here we propose a multi-scale approach to determine whether fragmentation processes at
the local and landscape scales are reducing functional diversity of trees in the East Usam-
bara Mountains, Tanzania. We employ a structural equation modelling approach using five
key plant traits (seed length, dispersal mode, shade tolerance, maximum tree height, and
wood density) to better understand the functional responses of trees to fragmentation at
multiple scales. Our results suggest both direct and indirect effects of forest fragmentation
on tree functional richness, evenness and divergence. A reduction in fragment area appears
to exacerbate the negative effects resulting from an increased amount of edge habitat and
loss of shape complexity, further reducing richness and evenness of traits related to
resource acquisition and favouring tree species with fast growth. As anthropogenic distur-
bances affect forests around the world, we advocate to include the direct and indirect effects
of forest fragmentation processes to gain a better understanding of shifts in functional diver-
sity that can inform future management efforts.
Forest loss and fragmentation result in long-lasting and complex changes in biodiversity that
may go beyond the loss of species to include the alteration of functional diversity of remaining
PLOS ONE | July 2, 2020 1 / 16
Citation: Zambrano J, Cordeiro NJ, Garzon-Lopez
C, Yeager L, Fortunel C, Ndangalasi HJ, et al.
(2020) Investigating the direct and indirect effects
of forest fragmentation on plant functional
diversity. PLoS ONE 15(7): e0235210. https://doi.
Editor: Berthold Heinze, Austrian Federal Research
Centre for Forests BFW, AUSTRIA
Received: December 11, 2019
Accepted: June 10, 2020
Published: July 2, 2020
Peer Review History: PLOS recognizes the
benefits of transparency in the peer review
process; therefore, we enable the publication of
all of the content of peer review and author
responses alongside final, published articles. The
editorial history of this article is available here:
Copyright: ©2020 Zambrano et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: The data supporting
the results are deposited in the The Knowledge
Network for Biocomplexity repository (DOI: 10.
communities. Forest fragmentation threatens the long-term persistence of species [13], as
well as the goods and services provided by those ecosystems [4]. Fragmentation is a hierarchi-
cal process that involves breaking apart the habitat of a focal species into populations isolated
from each other in a matrix of modified habitat [57]. Changes in the spatial configuration of
the landscape alter the abiotic and biotic filters that govern community assembly, selecting
individuals with suites of traits that enable them to survive, grow, reproduce, and colonize
remaining fragments. Species traits relate to physiological, morphological, and phenological
functions [810], and local functional diversity can influence ecosystem functioning [11,12]. If
species’ traits in remaining fragments become more similar over time, a process known as
functional homogenization, this could severely alter a variety of ecosystem functions per-
formed by remaining communities and, by extension, the ecosystem services they provide.
Previous studies provide evidence that forest fragmentation often favours plant species with
traits within a specific range of values [e.g. 13], potentially leading to functional homogeniza-
tion by reducing alpha diversity of functional traits [14]. By taking into account functional
diversity within a community, we can better understand how species respond to fragmentation
processes that alter the abiotic and biotic filters that govern community assembly.
Trait values that allow species to take advantage of recent disturbances are commonly
hypothesised to determine species success in fragmented landscapes [15,16]. Recent studies
have shown that reductions in fragment area and increases in the amount of edge habitat
locally favour tree species with faster growth rates (e.g. pioneers), smaller seeds, shorter leaf life
span and lower wood density [1520]. Additionally, increased spatial isolation and an inhospi-
table matrix habitat are expected to select for abiotically-dispersed tree species and/or small-
seeded, animal-dispersed tree species that have the potential for wide dissemination by attract-
ing many seed-disperser species [16,18,20,21]. However, because of the variable results across
studies and systems, there is limited consensus on the generality of the magnitude of these
shifts and their drivers.
The process of landscape fragmentation can be considered at multiple, interacting scales.
Fragmentation effects via fragment isolation or matrix quality that impact dispersal among
fragments or meta-population dynamics may manifest most strongly at the landscape scale. In
contrast, fragmentation effects via edge effects, fragment shape or size that impact fine-scale
habitat quality and individual persistence may be best detected at the fragment-scale (as with
our study with fragments ranging from 0.011–9.51 km
). Furthermore, these landscape- and
fragment-scale changes typically occur concurrently which may lead to interactions among
various fragmentation effects. For example, dispersal between fragments typically declines
with isolation and an inhospitable matrix habitat may exacerbate the effects of fragment isola-
tion on species diversity [7]. In forest fragments, altered abiotic conditions such as greater des-
iccation through increased wind and light, causing higher temperatures and lower humidity,
are among the main edge effects as the shape of fragments becomes narrower and/or as the
size of fragments decreases [6]. Decreasing fragment size could both directly impact species
persistence by lowering local population sizes and increasing edge effects as the relative
amount of edge habitat is greater in smaller fragments. Teasing apart these co-occurring
changes across spatial scales has posed a major challenge in predicting the net response of
functional diversity to forest fragmentation to date [6,22,23].
Previous investigations have yielded mixed results, with functional diversity responding
either positively or negatively to forest fragmentation [14,24,25]. This lack of consensus could
be the result of not accounting for the direct and indirect effects of both landscape- and frag-
ment-level effects. While measuring the independent effects of individual landscape properties
is useful to identify mechanisms behind fragmentation-driven biodiversity changes, such
approaches may miss critical indirect effects between fragment-level and landscape-level
A multi-scale approach of functional diversity
PLOS ONE | July 2, 2020 2 / 16
Funding: JZ and NGB were supported by the
National Socio-Environmental Synthesis Center
under the US National Science Foundation (NSF)
Grant DBI-1052875. CF benefited from an
“Investissements d’Avenir” grant managed by
Agence Nationale de la Recherche (CEBA, ref. ANR-
10-LABX-25-01). Support for LY was also provided
from NSF grant #OCE-1661683.
Competing interests: The authors have declared
that no competing interests exist.
fragmentation variables [26], and potentially leads to incorrect inferences and predictions
regarding the impacts of forest fragmentation on communities. Structural Equation Models
(SEM) have been proposed as an alternative tool to jointly study the direct and indirect effects
of habitat amount and configuration because SEMs specify predictor variables that may not
have been measured or that may be difficult to observe directly, and therefore measure the
strength of causal relationships among predictors and provide rigorous estimates of direct and
indirect effects [27].
Here, we use a SEM approach that permits the evaluation of direct and indirect effects of
forest fragmentation on plant functional diversity in the East Usambara Mountains of Tanza-
nia. This approach in particular allows us to tease apart the attributes of forest fragmentation
that operate across different spatial scales and to compare the relative importance of local ver-
sus landscape-scale processes affecting different dimensions of functional diversity (e.g rich-
ness, evenness and divergence). In this study, we censused trees in plots across a fragmented
rainforest in the East Usambara Mountains, an area in Africa known for its high levels of bio-
diversity and endemism [28] that is currently protected under the United Nations Educational,
Scientific and Cultural Organization (UNESCO) Biosphere Reserve status. We hypothesize
1. The variation in functional diversity in response to fragmentation is mediated by both frag-
ment- and landscape-scale factors (Fig 1). We expect that the impacts of fragment size,
shape complexity, and edge effects on functional diversity are indirectly affected by land-
scape-level processes such as fragment isolation and matrix quality. For example, edge
effects tend to be more severe in small and/or narrow or irregularly-shaped fragments,
which would therefore affect functional diversity. Finally, we anticipate a greater negative
effect of isolation on functional diversity for fragments surrounded by an inhospitable
matrix habitat.
Fig 1. Conceptual model illustrating the directional relationships between fragmentation processes occurring at
the landscape and fragment level affecting functional diversity. Functional diversity was defined in terms of
functional richness, evenness and divergence. Functional metrics were fitted in separate models. Arrows indicate the
hypothesized causal relationships, with dashed arrows representing indirect effects and continuous lines representing
direct effects.
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2. The effects of fragmentation are expected to impact functional diversity in several ways:
a) functional richness, evenness and divergence of resource use traits are expected to
decline with reduced fragment area and shape complexity as the amount of forest edge
increases; b) low quality of matrix surrounding the remaining fragments is expected to
exacerbate the environmental stress in edge habitats, further reducing functional richness,
evenness and divergence (Fig 1); c) trait distribution is expected to become more skewed
towards species with trait values associated with fast resource use (e.g. short stature, light-
demanding species with low wood density and small seeds) within edge habitats; and d)
functional richness, evenness and divergence of dispersal traits are expected to decrease
with increasing fragment isolation and decreasing matrix quality. Specifically, we expect
abiotically-dispersed species and small-seeded, animal-dispersed species to dominate in
more isolated fragments surrounded by a less hospitable matrix.
Materials and methods
Study area
The forest of the East Usambara Mountains stretches continuously from about 250 m to 1100
m asl in the southern part of this mountain range to form what is now protected as Amani
Nature Reserve (8380 ha; -5˚04’58.80" S 38˚40’1.20" E). To the north of this reserve is Nilo
Nature Reserve, and eastwards is the Derema corridor and several large fragments of lowland
forest. Rainfall averages at 2000 mm per annum, falling largely from March to May and Octo-
ber to November; however, with the exception of January and February, precipitation is preva-
lent in most other months due to moisture carried across from the adjacent Indian Ocean
[29]. The forest on the submontane plateau, in and around the primary study area of Amani
Nature Reserve, is dominated by a suite of wet rainforest species. These include two emergent
species Newtonia buchananii (Fabaceae) and Maranthes goetzeniana (Chrysobalanaceae),
and several canopy and midstory/understorey species such as Allanblackia stuhlmannii
(Clusiaceae), Cephalosphaera usambarensis (Myristicaceae), Sorindeia madagascariensis (Ana-
cardiaceae), Parinari excelsa (Chrysobalanaceae), Isoberlinia schefflerii (Fabaceae), Greenwayo-
dendron suaveolens (Annonaceae), Anisophyllea obtusifolia (Anisophylleaceae), Leptonychia
usambarensis (Sterculiaceae), Myrianthus holstii (Urticaceae), Macaranga capensis (Euphor-
biaceae), Trilepisium madagascariense (Moraceae) and Strombosia scheffleri (Olacaceae). The
forest also contains Maesopsis eminii (Rhamnaceae), an exotic, invasive gap- and edge-special-
ist tree species [29,30].
Amani Nature Reserve is surrounded by several forest fragments of varying sizes in the sub-
montane plateau (S1 Fig) and is primarily separated by a homogenous matrix of tea planta-
tions. Apart from subsistence cultivation, which has shaped the forested landscape in more
recent decades, much of the extensive forest loss and fragmentation arose from initial human
occupation in the early pre-colonial period [31], but more extensively from the historical
expansion of tea plantations, starting in the late 1800s [32]. Loss of original forest cover is esti-
mated to exceed 50% [33]. Ten forest fragments and a large portion of the continuous forest
were used to sample tree communities in 67 vegetation plots between May and July 2000; all
sites are at 900–1100 m asl (S1 Table). Each vegetation plot was 20 x 20m and the plots were
randomly located at ~25, ~150, ~250 and ~ 400 m from the forest edge towards the interior;
smaller fragments (i.e. <20 ha) did not have plots sampled at >200 m from the forest edge.
All trees 10 cm Diameter at Breast Height (DBH) within each plot were identified to species.
A multi-scale approach of functional diversity
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Functional trait data
We collated five traits (seed length, dispersal mode, shade tolerance, maximum tree height,
and wood density) that correspond to key dimensions of species ecological strategies and have
been previously used to explain competitive ability, growth, and reproduction in the context of
forest fragmentation [14]. Traits for all the tree species were obtained through an exhaustive
search of existing literature as well as online databases (S2 Table). Data on seed length and dis-
persal mode were obtained from Chapman et al. [34] and the African Tree Database (https:// Seed length was
based on the largest average length of the diaspore that is transported by the vector, and not
necessarily the seed kernel size. Seed length reflects a seed number-seedling survival trade-off
with small seeds being produced in large quantities and being better colonizers than larger
seeds at the expense of withstanding lack of resources or different hazards thus reducing seed-
ling survival and establishment [35]. Dispersal mode included zoochory (animal-dispersal),
anemochory (wind-dispersal), and barachory (gravity or explosive dispersal). Dispersal mode
influences the capacity of an individual to colonize newly formed or isolated fragments [36].
Maximum tree height was obtained from the literature [37] and an online database (http:// Maximum tree height is associated with competitive ability for light with tal-
ler trees displaying greater carbon assimilation potential than smaller trees [3840]. Wood
density for each species, or genus (when data for a species was not known), was derived from
the global wood density database [41,42]. Wood density is a critical component for many
essential functions, such as mechanical support and nutrient storage [43] and reflects a trade-
off between radial growth to acquire physical stability at the expense of vertical growth [44,45].
Finally, for shade-tolerance guilds, we followed the classifications of Oue
´draogo and collabora-
tors [46,47], and where necessary, supplemented information from other sources [37,48].
Plant successional guilds included pioneer (species dependent on gaps or forest edge to estab-
lish), shade-tolerant (species dependent on shade across different ontogenetic levels), and
light-demanding non-pioneer (species that establish in shade but initially require light to max-
imize growth) [46, sensu 49].
Fragmentation metrics
Fragments were mapped using the high-resolution satellite imagery from Google Earth Pro.
After mapping, metrics were calculated for each plot and all forest fragments using the GRASS
GIS software [50,51]. Edge effects were evaluated based on the calculated distance of the center
of the sampled plot to the forest edge. We also calculated fragment area (km
), distance from
the edge of a fragment to the closest edge of the continuous forest (m), matrix quality based on
the surrounding cultivated land, and shape complexity.
For assessing matrix quality, we first characterized the matrix habitat of the study area into
three land cover types: tea plantations (the primary matrix habitat), Eucalyptus woodlots, and
subsistence cultivation of mixed crops such as bananas, beans, maize, cassava, cardamom,
cloves and cinnamon. Tea and eucalyptus plantation represent a more hostile environment
surrounding fragments, while subsistence cultivation is less hostile as it includes a mix of small
forest patches and multi-crop species farms. To calculate matrix quality (MQ), we quantified
the percentage of the forest edge in contact with each of the mentioned land covers as
MQ = 100—(%tea + %eucalyptus). Thus, matrix quality is reduced as the percentage of forest
edge in contact with the hostile matrix habitats comprising of tea or eucalyptus plantation
To describe the shape complexity of the fragment, we calculated a fractal dimension index
[52,53] where lower values correspond to regular shapes and higher ones to convoluted shapes,
A multi-scale approach of functional diversity
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as follows:
FDI ¼2ln P
 �
ln A
where Prepresents the perimeter and Athe fragment area. FDI measures how much a shape
deviates from a circumference thus excluding the effect of area on the edge complexity; if frag-
ments are more complex, the perimeter increases and yields a higher fractal dimension.
Functional diversity. We used functional indices that capture three major components of
functional diversity: functional richness (FRic) or the amount of niche space occupied by the
community [54], evenness (FEve) or regularity of the distribution of species abundances in the
functional space [55] and divergence (FDiv) or variance of species trait distribution in the trait
space [54]. We calculated multivariate FRic, FEve and FDiv using all five functional traits, as
studies have demonstrated that considering a single trait can lead to an oversimplification of
results [e.g. 56]. All indices were calculated within the FD package [57] in R (Version 3.6.1; R
Core Team 2019) and Gower distances were used to calculate functional distance between spe-
cies pairs as it allows for the inclusion of both continuous and categorical traits. We calculated
a weighted FEve index using the abundance of species (defined using number of stems) with
different trait values within a community and an unweighted FEve index independent of spe-
cies abundances. We then compared both weighted and unweighted FEve indices to improve
the interpretation of this index as suggested by Legras and Gaertner [56]. To determine the
functional trait value of a species community and explore how shifts along individual trait axes
underlie the observed FRic, FEve and FDiv patterns, we calculated community-weighted mean
(CWM) values (i.e. mean plot-level species trait values weighted by their relative abundance).
To explore how community shifts along single traits underlie the observed FRic, FEve and
FDiv patterns, we also calculated community-weighted mean (CWM) trait values (i.e. species
trait values weighted by their relative abundance in each plot).
To further examine the potential drivers of functional diversity from the forest edge to inte-
rior of forests, we examined patterns of recruitment between edge and interior plots. It is pos-
sible that edge habitats have a more even distribution in wood density due to a mix of pre-
fragmentation trees with high wood density and new post-fragmentation trees characterized
by mostly low wood density. Thus, to evaluate whether there was a difference in tree size, we
compared size distributions between interior and edge habitats for each guild using a Kolgo-
morov-Smirnov test. Edge plots were defined as all plots within <100 m of the fragment/forest
edge and interior plots included all plots >100 m from the edge following Laurance [58] as
100 m being the threshold for edge effects.
Statistical modelling. We implemented a structural equation modelling approach using
the R package piecewiseSEM [59] to investigate direct and indirect relationships of fragment-
and landscape-scale variables in predicting local functional diversity. The general model inves-
tigated in this study (Fig 1) hypothesizes that variation in functional diversity among plots can
be explained by the interacting direct and indirect effects of processes occurring at the frag-
ment-level and the landscape-level. These include distance of plot to the nearest forest edge,
distance of fragment to continuous forest as a measure of isolation, fragment area, matrix qual-
ity, and shape complexity. We used linear functions for all relationships in the structural equa-
tion models and ran separate models for each functional metric. To derive comparable
estimates, we standardized all quantitative predictors to a mean of zero and standard deviation
of one. In some cases, variables were log-transformed to achieve a normal error distribution.
A multi-scale approach of functional diversity
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To further explore potential shifts in trait distributions underlying variation in FRic FEve and
FDiv, we used general linear models as a post-hoc test to determine changes in CWM traits
values as a result of fragment- and landscape-scale variables. In these models, the responses are
CWM values and the predictors are fragment- and landscape-level variables.
Relationships among fragmentation variables
We found a strong positive relation between matrix quality and fragment isolation
(coef = 0.704, se = 0.11, p <0.001; Fig 2) and found a weak relationship between matrix quality
and distance from plot to forest edge (coef = -0.595, se = 0.189, p = 0.568; Fig 2). The distance
from plot to forest edge increased with fragment area (coef = 0.603, se = 0.156, p <0.001; Fig
2) and tended to decrease as shape complexity of the fragment was reduced (coef = -0.423,
se = 0.167, p = 0.015; Fig 2). Finally, shape complexity was positively associated with fragment
area (coef = 0.541, se = 0.116, p <0.001; Fig 2), with larger fragments characterized by more
complex shapes than small fragments.
Response of functional diversity to fragmentation
We found that direct and indirect effects between fragment-level fragmentation attributes
appeared to be important drivers of local functional diversity within plots, while landscape-
level attributes seemed to be less important in most cases. Functional richness tended to
decrease with reduced shape complexity (coef = -0.936, se = 0.314, p = 0.004; Fig 2A). In addi-
tion, we found evidence that functional evenness tended to increase with fragment isolation
(coef = 0.038, se = 0.017, p = 0.03; Fig 2B). No other significant effects at the landscape or frag-
ment level were captured on functional evenness (Fig 2B). Finally, functional divergence
tended to decrease with distance of a plot from the forest edge (coef = -0.028, se = 0.012,
p = 0.031; Fig 2C), with no other significant effects on functional divergence (Fig 2C).
Fig 2. Structural equation models examining the effects of forest fragmentation on functional diversity in the East
Usambara Mountains, Tanzania. A) functional richness, B) functional evenness and C) functional divergence. Grey
lines represent indirect effects and dark lines representing direct effects. Values associated to lines represent
standardized path coefficients. Significant results (p 0.05) are represented in dark blue.
A multi-scale approach of functional diversity
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Shifts in community weighted mean traits with fragmentation
Values of community-weighted means were significantly associated with fragment isolation
and distance from plot to forest edge (i.e. edge effects). CWM values for dispersal mode was
significantly associated with fragment shape complexity, with anemochory increasing in more
complex fragments (estimate = 0.182, se = 0.073). CWM values for wood density significantly
declined with increasing fragment isolation (estimate = -0.015, se = 0.006). Furthermore,
CWM values for successional guilds were significantly associated with fragment isolation and
edge effects (distance from plot to forest edge). Specifically, CWM values for shade tolerance
significantly declined with increasing fragment isolation (estimate = -0.071, se = 0.025) and
increasing distance from plot to forest edge (estimate -0.388, se = 0.122). Distance from plot to
forest edge was negatively associated with CMV values of light-demanding non-pioneer spe-
cies (estimate = -0.171, se = 0.083), but, in contrast, positively associated with pioneer species
(estimate = 0.097, se = 0.022). We also found distance of plot to forest edge was positively asso-
ciated with maximum height (estimate = 1.305, se = 0.630) and wood density (estimate = 0.022,
se = 0.005). See Table 1 for all results.
Patterns of recruitment between edge and interior plots
We found significant differences in size distributions between the edges and the interior habi-
tats for light-demanding non-pioneer species (D = 0.25, p = 0.03), with many small sized indi-
viduals found at the edges of the forest (Fig 3). We found a similar pattern for pioneer species
(Fig 3), although this difference was not statistically significant (D = 0.18, p = 0.23). For shade-
tolerant species, larger individuals were found at the interior of the forest (Fig 3), but, similar
to pioneer species, this difference was not statistically significant (D = 0.07, p = 0.65).
Delineating the different processes that occur during landscape fragmentation and evaluating
how they affect functional diversity is challenging. This is because landscape fragmentation
leads to a series of changes in forest dynamics that occur at multiple spatial scales. Using a
SEM approach with data from the rainforest of East Usambara Mountains, Tanzania, we detect
several direct and indirect effects of forest fragmentation for different facets of functional
diversity. We use this example to illustrate the great potential for significant advancements
towards a more in depth understanding of the ecological consequences of forest fragmenta-
tion. At the landscape level, we find an indirect effect of matrix quality on functional evenness
via its effect on increased fragment isolation. At the fragment-level, we find an indirect effect
of fragment area on functional richness and functional divergence via its effects on shape com-
plexity and edge effects (i.e. distance from plot center to forest edge), respectively. In this
study, loss of shape complexity leads to significant changes in functional richness for traits
related to dispersal mode. For resource use traits, we find that functional richness and diver-
gence decline with decreasing shape complexity and distance from plot to forest edge, respec-
tively, while functional evenness increased with isolation. Our results also suggested a negative
relationship between fragment shape complexity and distance from plot center to forest edge,
in line with previous work [7,60,61]. A reduction in fragment shape complexity might exacer-
bate edge effects on functional diversity, effects that might not be revealed when analysed
using simple regression [7].
The relative importance of landscape and fragment-level factors vary considerably between
traits, but fragment-level factors were generally more important than landscape characteristics
in explaining variation in functional richness and divergence. By favouring tree species with
fast growth, edge effects and shape complexity seem to be key drivers of changes in the
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PLOS ONE | July 2, 2020 8 / 16
competitive hierarchies of tree communities in the fragmented forests of the East Usambaras.
The lesser importance of landscape-scale variables in the current study, only observed for func-
tional evenness, may be driven in part by our focus on plot-scale functional diversity. While
the plot-scale data are informative in assessing variation in diversity at small spatial scales, they
might not capture changes in diversity at large scales (e.g., at landscape scales or patterns in
beta-diversity). Future work examining patterns in functional diversity aggregated at larger
scales and across landscapes will extend the work presented here and better inform models of
the main factors driving tree communities in fragmented forests.
Functional diversity of resource use traits in response to fragmentation
A decrease in area of suitable habitat is expected to lead to the loss of species and a correspond-
ing narrowing of trait value, resulting in lower alpha functional richness [62]. We found evi-
dence of a decline in functional richness and divergence for traits related to resource use (e.g.
wood density and regeneration strategy) due to reduced shape complexity and distance to
edge respectively, both mediated by fragment area. Our results suggest the presence of strong
post-fragmentation edge effects, leading to an increase in pioneer species while shade tolerant
species are negatively impacted. In addition to area-based effects, fragmentation creates more
Table 1. Effects of isolation, shape complexity and distance to edge on community weighted means for plant functional traits in the East Usambara Mountains,
Trait Metric Estimate SE t p-value
Anemochory Isolation -0.064 0.078 -0.812 0.424
Zoochory -0.005 0.013 -0.410 0.683
Barochory 0.073 0.133 0.551 0.586
Height -0.406 0.653 -0.621 0.537
Light-demanding Non-Pioneer 0.111 0.083 1.344 0.185
Pioneer 0.179 0.121 1.482 0.145
Shade-Tolerant -0.071 0.025 -2.903 0.005
Seed length -0.458 0.671 -0.068 0.946
Wood density -0.015 0.006 0.006 0.012
Anemochory Shape complexity 0.182 0.073 2.476 0.020
Zoochory 0.007 0.013 0.528 0.600
Barochory 0.059 0.113 0.526 0.603
Height -0.009 0.655 -0.014 0.989
Light-demanding Non-Pioneer 0.119 0.081 1.473 0.147
Pioneer 0.038 0.122 0.309 0.759
Shade-Tolerant 0.013 0.026 0.505 0.616
Seed length -0.478 0.668 -0.716 0.477
Wood density 0.001 0.006 0.210 0.834
Anemochory Distance to edge -0.006 0.104 -0.059 0.953
Zoochory -0.015 0.013 -1.161 0.251
Barochory 0.104 0.106 0.980 0.334
Height 1.305 0.630 2.071 0.044
Light-demanding Non-Pioneer -0.171 0.083 -2.070 0.044
Shade-Tolerant -0.388 0.122 -3.176 0.003
Pioneer 0.097 0.022 4.326 <0.001
Seed length 1.127 0.652 1.727 0.09
Wood density 0.022 0.005 4.249 <0.001
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edge habitat typified by elevated radiation, temperature and wind turbulence, and lower soil
fertility and air moisture [63,64]. However, CWM trait values suggested that even if we found
evidence of functional divergence decreasing with distance from plot to forest edge, species at
the edges were more functionally diverse. This is likely the result of strong post-fragmentation
edge effects leading to an increase of small stature, light-demanding species characterized by
low wood density, combined with the older and taller, shade-tolerant and high wood-density
species persisting from pre-fragmentation communities.
The studied area has experienced a long history of land use with varying levels of anthropo-
genic disturbance, resulting in significant forest loss and fragmentation [33]. In this highly
fragmented landscape, edge effects on microclimate variables (air temperature, vapor pressure
deficits and light intensity) are stronger within 60 to 94 m from the edge, as compared to the
forest interior [65], explaining the observed changes in the competitive hierarchies of tree
communities in the fragmented forest of the East Usambara Mountains. Functional divergence
for resource use traits decreased with increasing distance of the plot from the forest edge, espe-
cially in large fragments as smaller fragments (<20 ha) generally included far fewer interior
plots (>200 m from the forest edge). The edge effects found here are in line with other studies
[17,18,6668], where species associated with slow growth rates are outcompeted in forest
edges by light-demanding or pioneer species with fast growth. Old-growth species are particu-
larly vulnerable to the detrimental effects of wind turbulence, desiccation, and liana
Fig 3. Size distribution of each of the three successional guilds at edge versus interior vegetation plots in the East Usambara Mountains,
A multi-scale approach of functional diversity
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dominance that characterise the edge of forest fragments [15], including those in the East
Usambaras [65].
Functional diversity of dispersal traits in response to fragmentation
Fragments with more elongated shapes have higher proportion of total edge than interior habi-
tat [60]. Reduced fragment shape complexity often results in low habitat heterogeneity, thus,
communities in fragments with narrow and elongated shapes may exhibit reduced species
richness and abundance [7]. Our results suggest that when fragments reach a certain reduced
size, loss of shape complexity leads to significant changes in functional richness for traits
related to dispersal mode. Increased complexity of fragment shape may limit impact of wind
action to toppling large trees, which may explain why anemochorous species, like the emergent
Newtonia buchananni (Fabaceae), remain in large and more complex East Usambara frag-
ments. Small and less complex shaped fragments tend to be more vulnerable to edge-related
wind damage increasing rates of windthrow and forest structural damage due to the higher
ratio of perimeter to edge compared to larger and more complex shaped fragments [60].
Unfortunately, generalizing on the overall effects of fragment shape complexity on functional
diversity is limited because it remains understudied compared to other fragmentation pro-
cesses. It is important to highlight that our evidence of fragmentation effects on functional
diversity comes from data of mature trees that represent the historical legacies of pre-fragmen-
tation communities. Hence, without data on seedlings and saplings, it is difficult to ascertain
whether the abundance of wind dispersed species is associated with reduced animal seed dis-
persers and therefore dispersal limitation which are negatively impacted by forest fragmenta-
tion in this study area [24,74,75]. Evidence from research in this study area has shown that
several important frugivores are absent from or occur in lower abundance in forest fragments
as compared to the continuous forest, threatening their persistence, as well as trees dependent
on many these vectors [6971].
Furthermore, we failed to uncover a relationship between traits related to dispersal (i.e.
seed length, dispersal mode) and fragment isolation or matrix quality. Instead, our results sug-
gest a less even distribution for traits related to resource use (e.g. wood density) as fragments
became more isolated. Wood density is a strong indicator of successional dynamics with light
wood often associated to early successional species (e.g. pioneer, light demanding species) that
exhibit high fecundity and long-distance dispersal allowing them to colonize recently dis-
turbed sites [41,72]. Therefore, light-wood species may be able to reach more isolated frag-
ments perhaps due to better colonization abilities than hard-wood species. Fragmentation
leads to increasing degree of isolation between fragments, hereby increasing the minimum dis-
persal distance for species from the regional pool to colonize fragments. However, it is impor-
tant to highlight a potential correlation between dispersal and resource acquisition traits.
Specifically, seed mass tends to define the mode of dispersal and is also related to the succes-
sional habit that determines resource acquisition strategies [40,73]. Light-demanding, early
successional species often produce numerous small seeds and thus are considered better colo-
nizers than shade-tolerant, late successional species [35], with potential to increase in abun-
dance over time and negatively impacting the future establishment of late-successional trees.
The effects of isolation and matrix quality may require exploring functional diversity at a
larger scale, beyond the local scale investigated in this study. Fragmentation leads to a high
degree of isolation between the remaining fragments increasing the minimum dispersal dis-
tance for species from the regional pool to colonize fragments [61,7476]. As species become
more dispersal limited with decreasing fragment connectivity, we expect that fragments would
become more similar in species composition, decreasing alpha functional richness and
A multi-scale approach of functional diversity
PLOS ONE | July 2, 2020 11 / 16
increasing evenness. Moreover, a more diverse matrix may promote habitat heterogeneity
between fragments increasing the range of total available niches at the landscape scale [7779],
potentially increasing functional richness and evenness. However, with most studies con-
ducted at a local scale, the effects of isolation and matrix type on functional diversity remains
fairly unexplored.
By analysing trait variation due to processes occurring at the landscape scale and integrating
this information with well-known fragment-scale processes using a structural equation
approach, we were able to provide a more in-depth understanding of the different components
of fragmentation and their impact on functional diversity. Specifically, the effects of fragment
variables on functional diversity of trees were largely mediated by the indirect effect of frag-
ment area on the amount of edge habitat and shape complexity. Our results demonstrate the
power of this approach in detecting the effects of processes occurring at different spatial scales
that may have been missed if only the direct impacts of landscape fragmentation would have
been considered. This approach could greatly facilitate future empirical work in forest frag-
mentation and help advocate for management and restorations strategies that aim to achieve
long-term persistence of remaining forests. Given that many fragmented forest systems will
experience environmental conditions outside the range to which they are adapted, it is impor-
tant to improve efforts to predict biodiversity responses to current human pressure to imple-
ment effective management and conservation strategies.
Supporting information
S1 Fig. Map of study area in the East Usambara Mountains of Tanzania. Map of the study
area in the East Usambara Mountains of Tanzania. The protected area, Amani Nature Reserve,
includes the continuous forest (dark green) and the largest forest fragment (largest fragment
in light green). The landcover classification (i.e. tea plantation, Eucalyptus plantation, forest
and subsistence farming) was based on a Landsat-8 images from 2016 (courtesy of the U.S.
Geological Survey) and performed using the random forest classification extension (r.learn.
lm) in GRASS GIS.
S1 Table. Main fragment and continuous forest characteristics of study sites in the East
Usambara Mountains, Tanzania.
S2 Table. Functional traits of tree species sampled in vegetation plots in the East Usambara
Mountains, Tanzania.
Norbert Cordeiro and Henry Ndangalasi acknowledge the following for permits and assis-
tance: Tanzania Commission for Science and Technology, East Usambara Conservation Area
Management Programme, Amani Nature Reserve, East Usambara Tea Company, Tanga
Regional Forest Office, Amani Parish and numerous individuals cited in Cordeiro et al.
(2009). We are thankful to Sabine Kasel, Lionel Hertzog and an anonymous reviewer for valu-
able suggestions that greatly improved this manuscript.
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Author Contributions
Conceptualization: Jenny Zambrano, Noelle G. Beckman.
Formal analysis: Jenny Zambrano, Carol Garzon-Lopez, Lauren Yeager, Claire Fortunel,
Noelle G. Beckman.
Investigation: Norbert J. Cordeiro, Henry J. Ndangalasi.
Methodology: Jenny Zambrano, Carol Garzon-Lopez, Lauren Yeager.
Writing – original draft: Jenny Zambrano.
Writing – review & editing: Norbert J. Cordeiro, Carol Garzon-Lopez, Lauren Yeager, Claire
Fortunel, Noelle G. Beckman.
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A multi-scale approach of functional diversity
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... Such interactive effects between traits and environments on individual performance (performance landscapes) have drawn increasing attention and have been empirically tested in recent studies. For instance, trait × environment interactions have been reported to affect plant survival , growth Yang et al. 2021), seedling establishment (Zirbel and Brudvig 2020) and multiple performance metrics (Blonder et al. 2018;Y. Li et al. 2021). ...
... Despite the evidence of trait × environment interactions, models including such interactions explained surprisingly small proportions of variation in plant performance Yang et al. 2021), even if higher-order interactions between multiple traits and environments were included (Y. Li et al. 2021;Worthy et al. 2020). ...
... Therefore, it is not surprising that empirical evidence has been reported that models of tree growth using individual-level traits (ITV considered) outperformed those using species mean traits (ITV ignored) (X. Liu et al. 2016;Yang et al. 2021). However, opposing evidence was also found that plant performances were not better predicted and trait × environment interactions were not more likely detected using individual-level traits than using species mean traits (Lourens Poorter et al. 2018;Y. ...
Full-text available
A foundational assumption of trait‐based ecology is that individual performances should be predicted by its functional traits. However, the trait–performance relationships reported in literature were typically weak, probably due to the ignorance of interactions between traits and environments, intraspecific trait variability and hard traits (directly linked to physiological processes of interest). We conducted an experiment of planting 900 seedlings of six tree species separately (one seedling per pot) along experimentally manipulated light and water gradients, monitored their survival and growth, and measured their morphological, photosynthetic and hydraulic traits. Most trait–performance relationships depended on the environments, either marginally changing (weak trait × environment interaction) or even reversing (strong trait × environment interaction) along light or water gradients in our experiment. Such trait × environment interactions were more likely to be detected in growth models using individual‐level traits than models using species mean traits, but seedling growth was not better modelled with individual‐level traits than species mean traits. Additionally, none of the hard traits (photosynthetic and hydraulic traits) were better predictors than soft traits (morphological traits) modeling seedling growth and survival along light and water gradients. Our study highlights the necessities of considering trait × environment interactions when predicting response of plants to changing environments. The benefits of using individual‐level traits or hard traits to predict plant performance might be reduced or even cancelled if their measurement errors are not well controlled.
... This article is protected by copyright. All rights reserved Trait-growth relationships have been used to reveal plant growth strategies and predict the demographic trajectories of species (Adler et al. 2013;Yang et al. 2021). However, the predictive power of traits has been sometimes weak which raises a question about the significance of traits (Paine et al. 2015). ...
... A 15 m radius was chosen following the previous work (Yang et al. 2021 (1) ...
... The result showed that neighborhood crowding did not interact with initial DBH size of trees to significantly limit the relative growth rate of individuals in all census data, which is consistent with the result of our mixed effect models. This finding is in contrast to the idea that large trees might dominate small neighborhood individuals through competition thereby reducing neighborhood density and/or limit individuals' growth, as they may have large canopy, crown and deep root systems (Yang et al. 2021). Overall, our result showed the absence of neighborhood crowding effect on trees growth over time. ...
Full-text available
Questions Linking tree growth dynamics to functional traits and neighborhood conditions that are measured at a single time point gives limited insights into the direction of forest structural and functional change. We used trait and neighborhood data collected at different time points for each individual tree of 15 Ficus species to test how trait (temporal trait plasticity) and neighborhood crowding change over time, and to test how their temporal change affects individual growth rate. We asked the following questions: (i) how do traits, neighborhood crowding, and growth of individual trees change over time; (ii) are functional traits and neighborhood crowding temporally consistent in their association with growth rate of individuals; and (iii) do temporal trait plasticity and changes in neighborhood crowding better predict the relative growth rate of individuals compared to using only a single snapshot of traits and neighborhood crowding? Location Xishuangbanna Tropical Seasonal Rainforest, southwest China. Methods We collected traits (specific leaf area [SLA], leaf area (LA), leaf dry matter content [LDMC], leaf chlorophyll, leaf thickness, and leaf succulence) at two time points (2010 and 2017) for 472 individuals of 15 Ficus species. We used linear mixed-effect models to test the effect of temporal trait plasticity and neighborhood crowding on the relative growth rate of individuals. Results We found that the temporal change in trait values predicts the growth rate of individuals better compared to static trait values in the initial and final censuses. We found significant temporal changes in individual traits suggesting a shift in ecological strategies from being acquisitive to conservative. A difference in neighborhood crowding between the two census years was also observed, indicating that the neighborhood effect on growth might also change over time. Conclusions Our results in general highlight the need to consider the temporal dimension of traits and biotic interactions, as our results suggest that growth–trait relationships may vary between time points, allowing us to understand the demographic response of species to temporal environmental change through functional traits.
... Specifically, neighboring individuals may either enhance or depress the growth of target trees by changing resource allocation, local habitats or introducing pathogens (Maestre et al., 2009;Trinder et al., 2013;Trogisch et al., 2021). For example, tree growth was demonstrated to increase with neighborhood species richness through niche complementarity (Fichtner et al., 2018), whilst competition with neighbors suppresses individual growth and even their survival in the tropics (Uriarte et al., 2004;Lasky et al., 2014;Yang et al., 2021). ...
... Consistent with previous studies in tropical forests, including that on the BCI (Uriarte et al., 2004;Stoll and Newbery, 2005;Lasky et al., 2014;Fortunel et al., 2016;Rozendaal et al., 2020;Yang et al., 2021), we found a significant relationship between tree growth and neighborhood interaction. We explored the variations of the neighbor competition effect with the neighborhood radii, time, and environmental variables. ...
The intensity of interactions among tree individuals in forests is regulated by distance and time. However, few studies have considered the variability of neighborhood competition with varying spatial and temporal scales simultaneously. Based on census data of a 50-ha plot on Barro Colorado Island (BCI) during 1981–2015, we analyzed the variation in the relationship between the neighborhood interaction, represented as the neighborhood competition index (NCI), and the tree growth rate of 41,965 individuals from 211 species along a gradient of the neighborhood radius and over time. The results showed that the neighborhood interaction negatively impacted tree growth, especially for smaller trees, across spatial and temporal scales. The strength of the NCI–growth relationship was scale- and time-dependent. This relationship intensified initially with the increasing neighborhood radius and then plateaued at an average of about 20 m from the target trees, indicating the strong influence from neighbors could be detected at a distance up to 50 m or even 100 m. The intensifying tendency of the NCI–growth relationship over time probably results from the warming trend in recent years or the continuous radial growth of the BCI forest. We emphasize the importance of individual interactions in dynamic forest growth, and that an appropriate radius and forest age should be considered for the neighborhood analysis.
... Most neighborhood crowding studies so far used specieslevel traits (Uriarte et al. 2010;Lasky et al. 2013;Fortunel et al. 2016), but there is a growing interest in evaluating the role of individual-level traits (Yang et al. 2021). At the CBS plot, we found that individual-level traits were stronger predictors of tree growth than species-level traits, consistent with recent findings in subtropical and tropical forests (Liu et al. 2016;Yang et al. 2021). ...
... Most neighborhood crowding studies so far used specieslevel traits (Uriarte et al. 2010;Lasky et al. 2013;Fortunel et al. 2016), but there is a growing interest in evaluating the role of individual-level traits (Yang et al. 2021). At the CBS plot, we found that individual-level traits were stronger predictors of tree growth than species-level traits, consistent with recent findings in subtropical and tropical forests (Liu et al. 2016;Yang et al. 2021). In particular, trees with higher photosynthesis rate (LChl) and light capture surface (LA) grow faster, as they are better at capturing light (Givnish 1987;Poorter and Bongers 2006). ...
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Forest dynamics are shaped by both abiotic and biotic factors. Trees associating with different types of mycorrhizal fungi differ in nutrient use and dominate in contrasting environments, but it remains unclear whether they exhibit differential growth responses to local abiotic and biotic gradients where they co-occur. We used 9-year tree census data in a 25-ha old-growth temperate forest in Northeast China to examine differences in tree growth response to soil nutrients and neighborhood crowding between tree species associating with arbuscular mycorrhizal (AM), ectomycorrhizal (EM), and dual-mycorrhizal (AEM) fungi. In addition, we tested the role of individual-level vs species-level leaf traits in capturing differences in tree growth response to soil nutrients and neighborhood crowding across mycorrhizal types. Across 25 species, soil nutrients decreased AM tree growth, while neighborhood crowding reduced both AM and EM tree growth, and neither soil nor neighbors impacted AEM tree growth. Across mycorrhizal types, individual-level traits were stronger predictors of tree growth than species-level traits. However, most traits poorly mediated tree growth response to soil nutrients and neighborhood crowding. Our findings indicate that mycorrhizal types strongly shape differences in tree growth response to local soil and crowding gradients, and suggest that including plant-mycorrhizae associations in future work offers great potential to improve our understanding of forest dynamics.
... In the last few years, there has been increasing interest in understanding the ecological roles of intraspecific variation regarding responses to environmental change, especially human-induced alterations to ecosystems and their effects on the loss of biodiversity [8,[34][35][36][37]. However, there is still a lack of knowledge on the possible mechanisms underlying intraspecific variation and how to infer the potential ecological impacts of this variation. ...
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Spanish fir (Abies pinsapo Boiss.) is an endemic, endangered tree that has been scarcely investigated at the molecular level. In this work, the transcriptome of Spanish fir was assembled, providing a large catalog of expressed genes (22,769), within which a high proportion were full-length transcripts (12,545). This resource is valuable for functional genomics studies and genome annotation in this relict conifer species. Two intraspecific variations of A. pinsapo can be found within its largest population at the Sierra de las Nieves National Park: one with standard green needles and another with bluish-green needles. To elucidate the causes of both phenotypes, we studied different physiological and molecular markers and transcriptome profiles in the needles. “Green” trees showed higher electron transport efficiency and enhanced levels of chlorophyll, protein, and total nitrogen in the needles. In contrast, needles from “bluish” trees exhibited higher contents of carotenoids and cellulose. These results agreed with the differential transcriptomic profiles, suggesting an imbalance in the nitrogen status of “bluish” trees. Additionally, gene expression analyses suggested that these differences could be associated with different epigenomic profiles. Taken together, the reported data provide new transcriptome resources and a better understanding of the natural variation in this tree species, which can help improve guidelines for its conservation and the implementation of adaptive management strategies under climatic change.
... The sixth IPCC assessment report (AR6) further affirms that global warming-caused by man-made influences-has caused an increase in the frequency of extreme events and subtropical. The region has a typical monsoon climate, with obvious alternations between dry (November to April) and rainy seasons (May to October) [40]. The annual average temperature is 21.5 • C [41]; the average annual total precipitation is about 1557 mm [41], and about 87% [41] of the precipitation occurs in the rainy season. ...
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Droughts that occur in tropical forests (TF) are expected to significantly impact the gross primary production (GPP) and the capacity of carbon sinks. Therefore, it is crucial to evaluate and analyze the sensitivities of TF-GPP to the characteristics of drought events for understanding global climate change. In this study, the standardized precipitation index (SPI) was used to define the drought intensity. Then, the spatially explicit individual-based dynamic global vegetation model (SEIB-DGVM) was utilized to simulate the dynamic process of GPP corresponding to multi-gradient drought scenarios—rain and dry seasons × 12 level durations × 4 level intensities. The results showed that drought events in the dry season have a significantly greater impact on TF-GPP than drought events in the rainy season, especially short-duration drought events. Furthermore, the impact of drought events in the rainy season is mainly manifested in long-duration droughts. Due to abundant rainfall in the rainy season, only extreme drought events caused a significant reduction in GPP, while the lack of water in the dry season caused significant impacts due to light drought. Effective precipitation and soil moisture stock in the rainy season are the most important support for the tropical forest dry season to resist extreme drought events in the study area. Further water deficit may render the tropical forest ecosystem more sensitive to drought events.
... Our study explicitly focussed on interspecific trait coordination and their relevance for species' differential fitness and abundance responses, and ecological filtering. If and to what extent trait expression of individuals in the natural habitat may weaken or strengthen such interspecific relations remains an important aspect for further studies (Yang et al., 2021). However, intraspecific variation is unlikely to override the observed (or missing) interspecific relations, since it is usually lower than interspecific variation (Kazakou et al., 2014;Siefert et al., 2015). ...
... As remnant habitats become smaller and more fragmented, considerable variation in local population dynamics and seed dispersal may occur among remnant patches, due to environmental heterogeneity and context dependency of local population dynamics and seed dispersal (Baden et al., 2021;Clobert et al., 2012). Accordingly, recent studies emphasize the significance of intraspecific variation in seed dispersal Snell et al., 2019) and local population dynamics (Yang et al., 2021) for predicting how plants respond to environmental change. Understanding this intraspecific variation is crucial in fragmented landscapes, because fragmentation could directly affect dispersal traits Dener et al., 2021) and local population dynamics (Hobbs & Yates, 2003;Ibáñez et al., 2014;Opdam et al., 1993). ...
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Aim Habitat loss and fragmentation impose high extinction risk upon endangered plant species globally. For many endangered plant species, as the remnant habitats become smaller and more fragmented, it is vital to estimate the population spread rate of small patches in order to effectively manage and preserve them for potential future range expansion. However, population spread rate has rarely been quantified at the patch level to inform conservation strategies and management decisions. To close this gap, we quantify the patch-specific seed dispersal and local population dynamics of Minuartia smejkalii, which is a critically endangered plant species endemic in the Czech Republic and is of urgent conservation concern. Location Želivka and Hrnčíře, Czechia. Methods We conducted demographic analyses using population projection matrices with long-term demographic data and used an analytic mechanistic dispersal model to simulate seed dispersal. We then used information on local population dynamics and seed dispersal to estimate the population spread rate and compared the relative contributions of seed dispersal and population growth rate to the population spread rate. Results We found that although both seed dispersal and population growth rate in M. smejkalii were critically limited, the population spread rate depended more strongly on the maximal dispersal distance than on the population growth rate. Main conclusions We recommend conservationists to largely increase the dispersal distance of M. smejkalii. Generally, efforts made to increase seed dispersal ability could largely raise efficiency and effectiveness of conservation actions for critically endangered plant species.
... Leaf traits and wood density will change with ontogenetic stages (Jiang et al. 2018a, Liu et al. 2020, and the intraspecific variation in these traits likely influences our ability to know the relationships between demographic rates and traits (Jiang et al. 2018a). Therefore, our study provided a relatively conservative result and using individual-level trait information could capture the trait and environment interaction effect on plant demographic rates better (Worthy et al. 2020;Yang et al. 2020). However, our study provided the first step for predicting forest community dynamics using functional traits under environmental contexts. ...
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Aims Functional traits are usually used to predict plant demographic rates without considering environmental contexts. However, previous studies have consistently found that traits have low explanatory power for plant demographic rates. We hypothesized that accounting for environmental contexts instead of focusing on traits alone could improve our understanding of how traits influence plant demographic rates. Methods We used generalized linear mixed-effect models to analyse the effects of functional traits (related to leaf, stem, seed, and whole plant), environmental gradients (soil nutrients, water, and elevation), and their interactions on the survival dynamics of 14133 saplings and 3289 adults in a 9-ha old-growth temperate forest plot. Important Findings We found that environmental variables, neighbour crowding, and traits alone (i.e., main effects) influenced plant survival. However, the effects of the latter two variables varied between saplings and adults. The trait-environment interactions influenced plant survival, such that resource conservative traits increased plant survival under harsh conditions but decreased survival under mild conditions. The elevational gradient was the most important environmental factor driving these effects in our plot. Our results support the hypothesis that functional traits influence plant survival depending on environmental contexts in local communities. These results also imply that one species with limited trait variation cannot occupy all environments, which can promote species diversity.
Trait-based approaches have emerged as promising strategies for understanding plant adaptation mechanisms to the changing environment. At present, there are a large number of studies on the relationship between plant leaf functional traits and environment, but these studies mostly use the average value of traits instead of species, ignoring the intraspecific changes of traits. Pinus densiflora Sieb. et Zucc. is not only an urban greening tree species, but also an important afforestation tree species, which plays an important role in China's terrestrial ecosystem. In this study, the leaf nitrogen content (LN), the leaf phosphorus content (LP), nitrogen phosphorus ratio (N/P), leaf area (LA) and specific leaf area (SLA) of 16 sites (160 records) distributed in Chinese P. densiflora were measured. (1) The results showed that LN increased with the increase of mean annual precipitation (MAP) and decreased with the increase of soil organic matter (SOM). LP and SLA decreased with the increase of mean annual temperature (MAT) and increased with the increase of AN (soil available phosphorus) and AP (soil available phosphorus). N/P increased with the increase of MAT and MAP, and decreased with the increase of AN and AP. LA increased with the increase of MAT and MAP. (2) Relative importance analysis showed that MAP was the most important driver of LN and LA. The main driving factors of LP is MAT, the main driving factors of N/P is SOM, and the main influencing factors of SLA is AP. Overall, climate was the main driving factor for the variation of leaf functional traits. The variation law of leaf functional traits along environmental gradient strongly supported the temperature-plant physiological hypothesis. It enriches the understanding of leaf functional traits distribution pattern and its driving mechanism under environmental change.
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Habitat loss and fragmentation result in significant landscape changes that ultimately affect plant diversity and add uncertainty to how natural areas will respond to future global change. This uncertainty is important given that the loss of biodiversity often includes losing key ecosystem functions. Few studies have explored the effects of landscape changes on plant functional diversity and evidence so far has shown far more pervasive effects than previously reported by species richness and composition studies. Here we present a review on the impact of habitat loss and fragmentation on (1) individual functional traits—related to persistence, dispersal and establishment—and (2) functional diversity. We also discuss current knowledge gaps and propose ways forward. From the literature review we found that studies have largely focused on dispersal traits, strongly impacted by habitat loss and fragmentation, while traits related to persistence were the least studied. Furthermore, most studies did not distinguish habitat loss from spatial fragmentation and were conducted at the plot or fragment-level, which taken together limits the ability to generalize the scale-dependency of landscape changes on plant functional diversity. For future work, we recommend (1) clearly distinguishing the effects of habitat loss from those of fragmentation, and (2) recognizing the scale-dependency of predicted responses when functional diversity varies in time and space. We conclude that a clear understanding of the effects of habitat loss and fragmentation on functional diversity will improve predictions of the resiliency and resistance of plant communities to varying scales of disturbance.
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Survival rates of large trees determine forest biomass dynamics. Survival rates of small trees have been linked to mechanisms that maintain biodiversity across tropical forests. How species survival rates change with size offers insight into the links between biodiversity and ecosystem function across tropical forests. We tested patterns of size-dependent tree survival across the tropics using data from 1,781 species and over 2 million individuals to assess whether tropical forests can be characterized by size-dependent life-history survival strategies. We found that species were classifiable into four 'survival modes' that explain life-history variation that shapes carbon cycling and the relative abundance within forests. Frequently collected functional traits, such as wood density, leaf mass per area and seed mass, were not generally predictive of the survival modes of species. Mean annual temperature and cumulative water deficit predicted the proportion of biomass of survival modes, indicating important links between evolutionary strategies, climate and carbon cycling. The application of survival modes in demographic simulations predicted biomass change across forest sites. Our results reveal globally identifiable size-dependent survival strategies that differ across diverse systems in a consistent way. The abundance of survival modes and interaction with climate ultimately determine forest structure, carbon storage in biomass and future forest trajectories.
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This review summarizes current understanding of five key plant traits: seed mass, plant height, wood density, leaf mass per unit area and leaf size, emphasizing ways in which our understanding of large-scale patterns in plant traits have improved over the last two decades. Notable advances include: (1) large-seeded species have greater seed dispersal distances than do small-seeded species, (2) leaf mass per unit area is not strongly or consistently related to plant traits outside the leaf economics spectrum, or to broad gradients in environmental conditions, and (3) fleshy fruit could not have first evolved for seed dispersal, as the first fleshy fruit appeared millions of years before the first potential seed dispersers. While quantifying large-scale patterns in plant traits has yielded many important discoveries, it is clear that the next major leap in understanding will not come from simply including ever more variables in our analyses. I suggest that we build upon Harper's “Darwinian approach to plant ecology” and apply evolutionary ideas to large-scale trait ecology. For example, quantifying trait impacts on lifetime fitness rather than on particular stages of plant regeneration can allow us to understand the coordination between seemingly disparate traits. I use this approach to bring seed mass and plant height together as integrated parts of a species’ life-history spectrum. I then point out problems associated with the implicit assumption that selection acts on species’ mean trait values and show how considering the way selection acts can improve our understanding of the effects of climate on plant traits. A goal for the future is to quantify the full suite of biotic and abiotic factors that shape plant strategy in complex, real-world situations. Synthesis. Enormous data availability and ever more powerful computational and statistical tools have given ecologists unprecedented power to quantify large-scale patterns in plant ecology. However, there is a limit to how far big data alone can take us. The time is ripe for a new generation of hypotheses and ecological theory built on strong evolutionary foundations. Let the creativity begin!. © 2017 The Author. Journal of Ecology
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Occasional periods of drought are typical of most tropical forests, but climate change is increasing drought frequency and intensity in many areas across the globe, threatening the structure and function of these ecosystems. The effects of intermittent drought on tropical tree communities remain poorly understood and the potential impacts of intensified drought under future climatic conditions are even less well known. The response of forests to altered precipitation will be determined by the tolerances of different species to reduced water availability and the interactions among plants that alleviate or exacerbate the effects of drought. Here, we report the response of experimental monocultures and mixtures of tropical trees to simulated drought, which reveals a fundamental shift in the nature of interactions among species. Weaker competition for water in diverse communities allowed seedlings to maintain growth under drought while more intense competition among conspecifics inhibited growth under the same conditions. These results show that reduced competition for water among species in mixtures mediates community resistance to drought. The delayed onset of competition for water among species in more diverse neighbourhoods during drought has potential implications for the coexistence of species in tropical forests and the resilience of these systems to climate change.Reduced competition for water among species in mixed tropical plant communities mediates community resistance to drought: weaker competition permits growth maintenance in drought, whereas stronger competition inhibits it.
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Stomata play a significant role in the Earth's water and carbon cycles, by regulating gaseous exchanges between the plant and the atmosphere. Under drought conditions, stomatal control of transpiration has long been thought to be closely coordinated with the decrease in hydraulic capacity (hydraulic failure due to xylem embolism). We tested this hypothesis by coupling a meta-analysis of functional traits related to the stomatal response to drought and embolism resistance with simulations from a soil–plant hydraulic model. We report here a previously unreported phenomenon: the existence of an absolute limit by which stomata closure must occur to avoid rapid death in drought conditions. The water potential causing stomatal closure and the xylem pressure at the onset of embolism formation were equal for only a small number of species, and the difference between these two traits (i.e. safety margins) increased continuously with increasing embolism resistance. Our findings demonstrate the need to revise current views about the functional coordination between stomata and hydraulic traits and provide a mechanistic framework for modeling plant mortality under drought conditions.
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Tree neighbourhood modelling has significantly contributed to our understanding of the mechanisms structuring communities. Investigations into the impact of neighbouring crowding on tree performance have generally been conducted at local scales, missing important regional-scale context such as the suitability of the climate for each species. Favourable climates may enhance tree performance, but this may come at the cost of increased neighbourhood crowding and competition negatively impacting survival and growth. Through the synthesis of continental-scale forest inventory and trait datasets from the northeast USA and Puerto Rico we present an analytical approach that elucidates the important interactions between local competitive and regional climatic contexts. Our results show strong asymmetries in competitive interactions and significant niche differences that are dependent on habitat suitability. The strong interaction between local neighbourhood and regional climate highlights the need for models that consider the interaction between these two processes that have been previously ignored. © 2017 The Author(s) Published by the Royal Society. All rights reserved.
Foundational to trait-based community ecology is the expectation that functional traits determine demographic outcomes. However, trait-demographic rate relationships are frequently weak, particularly in tree communities. The foundation of trait-based tree community ecology may, therefore, appear to be unstable. Here we argue that there are three core reasons why trait-demographic relationships are generally weak in tree communities. Specifically, important contextual information is frequently ignored, there is too much focus on species relative to individuals, and there are dimensions of tree function that are critical for determining tree demographic rates that are not captured by easily measured functional traits. Rather than being evidence that trait-based community ecology is fundamentally flawed, these issues elucidate a pathway towards a more robust research program.
Predicting the fate of tropical forests under a changing climate requires understanding species responses to climatic variability and extremes. Seedlings may be particularly vulnerable to climatic stress given low stored resources and undeveloped roots; they also portend the potential effects of climate change on future forest composition. Here we use data for ca. 50,000 tropical seedlings representing 25 woody species to assess (a) the effects of interannual variation in rainfall and solar radiation between 2007 and 2016 on seedling survival over 9 years in a subtropical forest; and (b) how spatial heterogeneity in three environmental factors–soil moisture, understory light, and conspecific neighborhood density– modulate these responses.
Understanding how climate affects tree growth is essential for assessing climate change impacts on forests but can be confounded by effects of competition, which strongly influences tree responses to climate. We characterized the joint influences of tree size, competition, and climate on diameter growth using hierarchical Bayesian methods applied to permanent sample plot data from the montane forests of Mount Rainier National Park, Washington State, USA, which are mostly comprised of Abies amabilis Douglas ex Forbes, Tsuga heterophylla (Raf.) Sarg., Pseudotsuga menziesii (Mirb.) Franco, and Thuja plicata Donn ex D. Don. Individual growth was sensitive to climate under low but not high competition, likely because tree ability to increase growth under more favorable climates (generally greater energy availability) was constrained by competition, with important variation among species. Thus, climate change will likely increase individual growth most in uncrowded stands with lower competition. However, crowded stands have more and (or) larger trees, conferring greater capacity for aggregate absolute growth increases. Due to these contrasting effects, our models predicted that climate change will lead to greater stand-scale growth increases in stands with medium compared with low crowding but similar increases in stands with medium and high crowding. Thus, competition will mediate the impacts of climate change on individual-and stand-scale growth in important but complex ways.