Dynamic trait-niche relationships shape niche partitioning across habitat transformation gradients

Abstract

Multidimensional approaches examining complex trait-niche relationships are crucial to understand community assembly. This is particularly important across habitat transformation gradients because specialists are progressively substituted by generalists and, despite increasing functional homogenization, in both specialist and generalist communities niche partitioning is apparent. Here, in line with the continuum hypothesis, we expected that divergent trait-niche relationships would arise in passerine assemblages across the natural-to-urban transformation gradient. More specifically, we expected that traits linking form to function would be more important in less transformed habitats, while population density and traits linked to dispersal and dominance would predominate in more transformed habitats. Accordingly, we found that beak length and its interaction with tarsus length correlated significantly with isotopic niches in natural and rural habitats, where specialists predominate. Conversely, body size and aggressiveness only showed significant relationships with isotopic niches with increasing habitat transformation, where generalists prevail. Interestingly, we recorded a mix of these processes in rural habitats, which acted as a frontier between these two domains. Our study is thus important in showing that a complex combination of morphological and behavioral traits determine niche characteristics, and that these relationships are dynamic across habitat transformation gradients.

Full text

Dynamic trait-niche relationships shape niche partitioning
across habitat transformation gradients
Emilio Pagani-N
u~
nez
a,x,
*, Dan Liang
b,c,x
, Chao He
d
, Yang Liu
c
, Xu Luo
e
,
Eben Goodale
d
a
Department of Health and Environmental Sciences, Xi’an Jiaotong- Liverpool University, Suzhou 215123, China
b
Princeton School of Public and International Affairs, Princeton University, New Jersey 08540, U.S
c
School of Ecology/School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China
d
Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning
530004, China
e
Key Laboratory for Forest Resources Conservation and Utilization in the Southwest Mountains of China, Ministry of
Education, Southwest Forestry University, Kunming 650224, China
Received 20 July 2021; accepted 4 January 2022
Available online 6 January 2022
Abstract
Multidimensional approaches examining complex trait-niche relationships are crucial to understand community assembly.
This is particularly important across habitat transformation gradients because specialists are progressively substituted by gener-
alists and, despite increasing functional homogenization, in both specialist and generalist communities niche partitioning is
apparent. Here, in line with the continuum hypothesis, we expected that divergent trait-niche relationships would arise in pas-
serine assemblages across the natural-to-urban transformation gradient. More specifically, we expected that traits linking form
to function would be more important in less transformed habitats, while population density and traits linked to dispersal and
dominance would predominate in more transformed habitats. Accordingly, we found that beak length and its interaction with
tarsus length correlated significantly with isotopic niches in natural and rural habitats, where specialists predominate. Con-
versely, body size and aggressiveness only showed significant relationships with isotopic niches with increasing habitat trans-
formation, where generalists prevail. Interestingly, we recorded a mix of these processes in rural habitats, which acted as a
frontier between these two domains. Our study is thus important in showing that a complex combination of morphological and
behavioral traits determine niche characteristics, and that these relationships are dynamic across habitat transformation
gradients.
© 2022 The Authors. Published by Elsevier GmbH on behalf of Gesellschaft für Ökologie. This is an open access article under
the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
Keywords: Competition; Coexistence; Dispersal; Functional traits; Niches
Introduction
Over millions of years, animal species have evolved mor-
phological and behavioral adaptations enabling highly effi-
cient exploitation of certain habitats and food resources,
*Corresponding author. Tel.: +86 0512 8818 9112.
E-mail address: emilio.pnunez@xjtlu.edu.cn (E. Pagani-N
u~
nez).
xThese authors contributed equally to this manuscript.
https://doi.org/10.1016/j.baae.2022.01.002
1439-1791/© 2022 The Authors. Published by Elsevier GmbH on behalf of Gesellschaft für Ökologie. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
Basic and Applied Ecology 59 (2022) 5969 www.elsevier.com/locate/baae

which facilitate species coexistence through competition
avoidance (Tokeshi, 2009). For example, hummingbirds
have refined beak morphologies matching the shape of the
flowers from which they extract nectar (Jordano, 1987). Her-
bivore mammals inhabiting the African savannah have body
morphologies adapted to exploit different strata of the avail-
able plant resources (Kleynhans et al., 2011). African Cich-
lid fishes evolved complex mouth morphologies finely
adapted to specialized foraging strategies (Albertson et al.,
2005). Therefore, there is often a fine match between spe-
cialists’functional traits, i.e. traits linking form to function,
and their niches an n-dimensional space where a species
can exist (Hutchinson, 1957). These relationships are com-
monly referred to as trait-niche relationships. However, our
planet has periodically experienced profound and abrupt
environmental changes, so that becoming excessively spe-
cialized may make species less resilient to environmental
perturbations (Alvarez et al., 2019).
Across the last centuries, and accelerating in the last deca-
des, a human-driven sudden change is altering Earth’s envi-
ronmental conditions, which is commonly referred to as the
Anthropocene (Lewis & Maslin, 2015). This process is pro-
ducing strong disturbances in the normal functioning of
Earth’s ecosystems, erasing million-year-old species interac-
tions, and inducing the collapse of complex trophic webs
(Emer et al., 2019;Pringle et al., 2019). More specifically,
environmental changes modifying habitat structure and the
availability of resources are strongly detrimental for special-
ists, so that this group is progressively substituted by gener-
alists across habitat transformation gradients (Ducatez et al.,
2018). Species turnover often results in a simplification of
these communities, meaning that species in communities in
transformed habitats often are less specialized than species
in natural communities, a process commonly labelled func-
tional homogenization (Devictor et al., 2008). Understand-
ing how biodiversity loss associated with environmental
change disrupts ecosystem functioning is thus fundamental
before millions of years of evolutionary history are irrevers-
ibly lost (Sol et al., 2017).
Interestingly, functional homogenization does not neces-
sarily imply that species’realized niches are redundant, i.e.,
that there is increased niche overlap. Communities of spe-
cialists and generalists may show comparable levels of niche
partitioning facilitating species’coexistence (Liang et al.,
2020;Pagani-N
u~
nez et al., 2019). To overcome this para-
dox, and in line with the “continuum hypothesis”
(Gravel et al., 2006), species would need different sets of
traits and dynamic trait-niche relationships to maintain dif-
ferentiated niches across transformation gradients. Trait-
niche relationships linking form to function, i.e. morphologi-
cal traits directly related to niche use (Pigot et al., 2020),
would be relevant where specialists’links to their resources
may be unaltered. In contrast, with increasing habitat trans-
formation and functional homogenization, other traits would
drive niche partitioning. For instance, population density
effects would confer a central, dominant, niche position to
more abundant species (Thompson et al., 2020;Vela Díaz
et al., 2020). Similarly, dispersal capacity would facilitate
species’niche expansion (Bastianelli et al., 2017;
Salisbury et al., 2012). Finally, body size and aggressiveness
would enable species to maintain differentiated niches (Mar-
tin & Bonier, 2018;Ulrich et al., 2018).
Here, we assessed trait-niche relationships across natural-to-
urban transformation gradients in eight highly diverse, subtrop-
ical passerine assemblages. Birds are highly suitable to study
this question due to their high taxonomic and functional diver-
sity and broad variety of responses to environmental change
(Bregman et al., 2014;Sol et al., 2020). To do this, we used
d
13
Candd
15
N stable isotopes to quantify species’realized
niches, namely niche width and overlap (Pagani-N
u~
nez et al.,
2019). Stable isotopes provide continuous metrics of resource
use and integrate both habitat use (d
13
C) and trophic level
(d
15
N) (Boecklen et al., 2011;Pagani-N
u~
nez, Renom, et al.,
2017). We also took comprehensive behavioral and morpho-
logical measurements. In doing so, we overcome implicit limi-
tations imposed when relying on diet categories or single-trait
approaches (Pigotetal.,2020). We formulated several predic-
tions. We expected a contraction of the morphological trait
space, namely functional homogenization, across the habitat
transformation gradient (Callaghan et al., 2019). Moreover, we
expected that divergent trait-niche relationships would arise
across these gradients. In natural habitats, we expected that spe-
cialized morphologies (particularly long beaks and the ratio
between different body traits) would be the main drivers of
niche partitioning, i.e., these traits would show a negative rela-
tionship with niche overlap. For instance, the ratio between
beak and tarsus length is indicative of specialization to forage
on the ground or the canopy, and that between tarsus and wing
length is indicative of specialization to capture insects in flight
or using short leaps (Remsen & Robinson, 1990). Conversely,
in transformed habitats, we expected that high population den-
sities, larger body sizes and high dispersal capacity would be
linked to larger niche width, while high aggressiveness would
be linked to reduced niche overlap. This study contributes to
expanding our knowledge about how environmental change
affects ecosystem functioning by ascertaining how habitat
transformation modifies trait-niche relationships in highly
diverse animal communities.
Materials and methods
Study area and field procedures
We collected data from eight passerine assemblages dur-
ing 2016 and 2017 using 70 m of mist nets at fixed sites in a
broad area across Yunnan Province (Southwest China) and
Guangxi Zhuang Autonomous Region (South China)
(Fig. 1). This is a subtropical region according to the
K€
oppen climate classification (Zheng, 2000), harboring rich
biodiversity yet also experiencing intense habitat transfor-
mation (Dai et al., 2018;Pan et al., 2019). We categorized
60 E. Pagani-N
u~
nez et al. / Basic and Applied Ecology 59 (2022) 5969

them into natural (3 sites), rural (3 sites), or urban (2 sites)
(Fig. 1). Natural sites were primary or secondary forests
with little human activity. Rural sites were areas where agri-
culture and silviculture predominated. Urban sites were
urban parks. We captured a total of 1068 individuals from
137 species. Species diversity was generally high, with rare-
fied richness ranging from 13.90 (natural site) to 31.00 (rural
site). Average rarefied richness was 20.26 for natural sites,
26.69 for rural sites, and 22.58 for urban sites. Thus, all the
sites harbored relatively high diversity (Mann-Whitney U
Tests of differences in rarefied richness between pairs of
habitat types all had P-values >0.40). Sampling duration
and elevation had negligible effects on niche characteristics
and were not included in our analyses (Pagani-N
u~
nez et al.,
2019).
We captured birds in suitable places with abundant vege-
tation cover. In five sites in Guangxi (2 urban, 1 rural and 2
natural), we followed a constant effort protocol by visiting
each location at least once per month, except during July
and August 2016 when temperatures were extremely high
(>40°C). In these sites, we left the nets open for six hours
after dawn during two consecutive days in each visit. In
three remote sites in Yunnan (2 rural and 1 natural), we fol-
lowed an intensive approach, working during several conse-
cutive days and leaving the nets from dawn to dusk. We
checked mist nets every hour, and every 30 minutes when
temperature exceeded 30°C. We banded individual birds
with numbered plastic rings and released them near the pla-
ces at which they were captured, once morphological and
behavioral measurements were taken. We excluded recap-
tured individuals from our analyses.
Behavioral and morphological measurements
We carefully extracted the captured birds and put them
into separate cloth bags for at least 5 minutes before taking
any measurements. We measured behavioral traits first
because handling may result in considerable behavioral
changes (Senar et al., 2017). To characterize aggressiveness,
we measured breath and pecking rates, and the number of
distress calls (Koolhaas et al., 1999). These traits are optimal
proxies of proactivity and aggressiveness (Carere &
van Oers, 2004). We first took breath rate, holding the bird
over our open hand and counting the number of breaths for
30s (Liang et al., 2018;Senar et al., 2017). We then quanti-
fied pecking rate as the number of pecks or bites to the han-
dler, holding a finger vertically in front of the bird for 15 s
(Senar et al., 2017), and recording the number of distress
calls emitted during the same period. Most species in our
sample showed no or little sexual dimorphism, and little dif-
ferences in breath rate (Liang et al., 2018), so we assumed
negligible sex effects on behavioral traits.
Then, we recorded body mass to the nearest 0.1 g using an
electronic balance, and wing (of both primary and secondary
feathers), tail, tarsus and beak length to the nearest mm
using a digital ruler. We computed the Hand-Wing-Index
(HWI), as the Kipp’s distance corrected for wing size (i.e.,
the difference between primary and secondary length), com-
monly used as a proxy of dispersal capacity (Paradis et al.,
1998;Sheard et al., 2020). We also computed population
density as the number of individuals captured per meter of
net and hour (N/m*h). We required at least 5 individuals per
species in each population to compute niche characteristics
Fig. 1. Map of our study areas. From left to right, geographical map of the People’s Republic of China highlighting our study areas, depiction
of our two study regions: Yunnan Province and Guangxi Zhuang Autonomous Region, depiction of our eight study locations, and three pic-
tures illustrating habitat differences across the transformation gradient. Pictures of study sites taken by the authors.
E. Pagani-N
u~
nez et al. / Basic and Applied Ecology 59 (2022) 5969 61

(see below), so we only used data from such species. We
computed the average values for each trait using the individ-
uals of a given species in each site (for each population).
The first author collected field data and trained together with
Dan Liang and Chao He for months to guarantee that in
some instances in which the first author could not be in the
field the collected data was comparable.
Quantifying niche characteristics
For stable isotopic analyses, we cut the tip of the claws as
the isotopic ratio of tip claws represents the diet information
over weeks to months depending on the size of the claw
(Bearhop et al., 2003). We measured carbon (d
13
C) and
nitrogen (d
15
N) stable isotopes of claws from all individuals
in each community. Samples were cleaned with a NaOH
(0.25 M) solution, air-dried for at least 12 hours, and
weighed (0.35 mg) into tin capsules. The abundances of
13
C/
12
C,
15
N/
14
N were determined at the Guangxi Univer-
sity Stable Isotopic Laboratory using an elemental analyzer
with an isotope ratio mass spectrometer via a continuous
flow interface. Stable isotope ratios were converted using
the equation: dX(%) = [(Rsample/Rstandard) 1] £1000,
where X is
13
Cor
15
N and R is the corresponding ratio
13
C/
12
Cor
15
N/
14
N, and then referenced against the interna-
tional standards: Pee Dee belemnite for
13
C, and atmo-
spheric nitrogen for
15
N. The precisions of measurements
were 0.15% for d
13
C and 0.25% for d
15
N, respectively.
We quantified niche width and overlap of species with at
least five individuals in at least one assemblage (Pagani-
N
u~
nez et al., 2019). This procedure reduced our dataset to 608
individuals of 29 species, of which nine species were present
in at least two assemblages (2 to 4 assemblages), yielding a
total of 42 populations in our dataset. We computed niche
width as the standard ellipse areas corrected by sample size
(SEAc) of the isotopic space of each population using SIBER
v2.1.4 (Jackson et al., 2011). SEAc are geometric representa-
tions of a population’s niche space, so that populations with
individuals showing higher variability in stable isotopes would
produce a larger ellipse area and vice versa. We computed
niche overlap as the average overlap of a species with all the
other species in each assemblage (i.e., of each population in
each assemblage). Niche overlap was quantified using nicheR-
over v 1.0, which relies on a Bayesian resampling approach
understood as the probability of an individual of a given spe-
cies/population to be recorded in the niche space of a second
species/population (Swanson et al., 2015).
Statistical analyses
We performed all analyses in R v3.6.1 (R Core
Team, 2021). Morphological and behavioral traits are likely
correlated with each other and co-vary across axes such as
body size (Pigot et al., 2020). Hence, we computed two
principal component analysis (PCA) with scale transforma-
tion, one for morphological traits (body mass and wing, tail,
tarsus, and beak length) and another for behavioral traits
(pecking and breath rate, and number of distress calls), sum-
marizing their relationships. We decided not to control for
phylogenetic relatedness at this stage because we did so in
all further analyses. We only considered variable scores
over 0.50 and component eigenvalues higher than 1. We set
the number of dimensions to reach 100% of explained vari-
ance. We obtained two main components from the PCA on
morphological traits (“body size”) and one from the PCA on
behavioral traits (“aggressiveness”) fulfilling these criteria
and aligned with our predictions, which were used as predic-
tors in our models (Supplementary Material S1). We also
obtained a potentially interesting component from the PCA
on morphological traits (beak vs tarsus length, which we
labelled “body morphology”), yet with an eigenvalue
slightly lower than 1 (Supplementary Material S1). For
instance, species with long tarsi and short beaks would be
particularly well adapted to forage on a broad diversity of
prey on the ground, while species with short tarsi and long
beaks would be adapted to exploit prey found within trees’
bark (Remsen & Robinson, 1990). Therefore, we included
this component in our analyses but also ran models using
beak and tarsus length. In summary, we considered six vari-
ables characterizing species morphology and behavior
(body size, body morphology, aggressiveness, beak and tar-
sus length, and the HWI), and population density.
All further analyses accounted for species’phylogenetic
relatedness. We computed a phylogenetic tree by download-
ing 10000 Markov chain Monte Carlo (MCMC) backbone
phylogenies of the 29 target species and generated the Maxi-
mum Clade Credibility (MCC) tree using the function “max-
CladeCred”in the package phangorn v2.5.5 (Schliep, 2011).
To include all populations of nine species with more than
one population, we modified the MCC tree by manually add-
ing small branches (10
10
) between conspecific populations
(Pagani-N
u~
nez et al., 2019).
Firstly, we determined whether there were differences in
morphological and behavioral traits across habitat types to
understand how habitat transformation shaped the trait
space. To do this, we constructed Phylogenetic Generalized
Least Squares (PGLS) models for each dependent variable
(body size, body morphology, aggressiveness, beak length,
tarsus length, and the HWI) using the package caper v1.0.1
(Omer, 2018). We included habitat type (natural, rural, or
urban) as categorical factor. We computed the phylogenetic
signal lambda (λ) for each model. The body size model did
not converge, so that we used instead a phylogenetically
controlled Markov chain Monte Carlo generalized linear
mixed model (MCMCglmm) for that variable using the
package MCMCglmm v2.30 (Hadfield, 2010). We set the
model to run 75000 iterations, with a thinning interval of 40
and a burn-in of 7500.
Secondly, we determined which traits were more impor-
tant in explaining variability in niche characteristics. We
62 E. Pagani-N
u~
nez et al. / Basic and Applied Ecology 59 (2022) 5969

constructed two PGLS models including niche width and
overlap as dependent variables and body size, body mor-
phology, aggressiveness, HWI, and population density, as
predictors. We ran two additional models using beak and tar-
sus length, instead of the component body morphology. We
improved model performance by applying a model selection
and averaging approach using the package MuMIn v1.43.17
(Burnham & Anderson, 2002). We ranked the subset models
based on their Akaike's Information Criterion corrected for
small sample sizes (AICc) and averaged the coefficients of
the selected models (DAICc <2) (Burnham & Ander-
son, 2002).
Finally, we tested our prediction that divergent trait-niche
relationships would arise across the habitat transformation
gradient using a PGLS approach. Our dependent variables
were niche width and overlap. We ran a model for the varia-
bles selected in the previous section: population density, the
HWI and aggressiveness for niche width, and body size,
body morphology, aggressiveness, beak length, tarsus length
and the HWI for niche overlap. In each model, we analyzed
the interaction between each of these predictors and habitat
type (natural, rural, or urban). We constructed thus a total
number of 9 models.
The absolute values of correlation coefficients (|r|)
between the continuous predictors (the three components,
beak and tarsus length, the HWI and population density)
were less than 0.7, suggesting no significant collinearity
between them (Dormann et al., 2013). As habitat type had
three levels (natural, rural, and urban), we dummy-coded
these levels and repeated the analyses using a different level
as a reference to perform comparisons between each pair of
habitat types. All continuous variables, except for the PCA
components, were scaled (mean of 0 and SD of 1) in all
analyses to improve homoscedasticity and model perfor-
mance.
Results
Differences in morphological and behavioral traits
across habitat types
The morphological trait space became narrower across the
transformation gradient (Fig. 2A). Accordingly, the compo-
nent body morphology showed higher values in natural than
in urban habitats (Natural vs Urban: b§SE = -0.78 §0.30,
z= -2.63, P= 0.01) (Supplementary Material S2; Fig. 2B),
meaning that birds in natural habitats had on average longer
beaks and shorter tarsi than those in urban habitats. There
were no other significant differences between habitat types
in body morphology. We also examined directly differences
in beak and tarsus length between habitat types. We found
that populations in natural habitats had longer beaks than in
rural habitats (Natural vs Rural: b§SE = -3.97 §1.85,
z= -2.14, P= 0.04) (Supplementary Material S2; Fig. 2C),
while urban populations showed no differences with popula-
tions in rural and natural habitats. We recorded no signifi-
cant differences in tarsus length, body size, HWI or
aggressiveness (Fig. 2D) between habitat types (Supplemen-
tary Material S3).
Relative importance of niche and neutral traits for
niche characteristics
None of the morphological and behavioral traits, nor pop-
ulation density, showed significant effects on niche width
when pooled together in a single model, either using the
component body morphology, or beak and tarsus length
directly (Supplementary Material S4). However, the compo-
nent body morphology correlated negatively with niche
overlap (Table 1A), meaning that birds with longer beaks
and shorter tarsi had lower overlap. Other morphological
and behavioral traits, and population density, showed no
effects on niche overlap. The model using beak and tarsus
length instead of the component body morphology depicted
slightly different results. Beak length and the HWI corre-
lated negatively with niche overlap (Table 1B), meaning
that birds with longer beaks and more pointed wings had
lower overlap. The other variables showed no significant
effects on niche overlap.
Habitat transformation effects on trait-niche
relationships
The HWI and population density showed no significant
relationships with niche width within any of the habitat
types (Supplementary Material S5). The component aggres-
siveness showed a negative relationship with niche width in
urban habitats (Table 2A; Fig. 3A), meaning that birds dis-
playing more aggressive behaviors (higher pecking rates,
more distress calls, and lower breath rate) had narrower
niches, while this relationship was not significant in rural or
natural habitats.
We recorded significant negative relationships between
niche overlap and the component body morphology in both
natural and rural habitats, yet not in urban habitats
(Table 2B; Fig. 3B). Beak length also showed significant
negative relationships with niche overlap in both natural and
rural habitats, meaning that birds with longer beaks had
lower overlap, yet not in urban habitats (Table 2B; Fig. 3C).
Tarsus length showed no significant relationships with niche
overlap within any of the habitat types (Supplementary
Material S5). The component body size showed no signifi-
cant relationships with niche overlap in any habitat type, yet
the negative relationship in rural habitats showed high effect
size and a marginally significant P-value (0.05) (Table 2B).
The component aggressiveness and the HWI showed no
E. Pagani-N
u~
nez et al. / Basic and Applied Ecology 59 (2022) 5969 63

Fig. 2. (A) Relationships between the principal component analysis components body morphology (beak vs tarsus length) and body size for
44 populations of 29 passerine species in 8 locations across habitat transformation gradients (natural, rural, or urban). Ellipses show 95% nor-
mal-probability areas superimposed over the data points. Species’Latin names are depicted besides each data point. Additionally, histograms
showing data distribution across habitat types (natural, rural, or urban) for (B) the principal component analysis component body morphology
(beak vs tarsus length), (C) scaled beak length, and (D) the principal component analysis component aggressiveness (pecking rates and dis-
tress calls vs breath rate). Vertical dashed lines represent mean values.
Table 1. A) Results of the phylogenetic generalized least squares regression (PGLS) using niche overlap as dependent variable, and the prin-
cipal component analysis components body size, body morphology (beak vs tarsus length), aggressiveness (pecking rates and distress calls
vs breath rate), the Hand-Wing Index (HWI), and population density (N/m/h) as continuous predictors. B) We ran an additional model
directly using beak and tarsus length (mm) instead of the component body morphology. We used model selection and averaging based on
Akaike Information Criteria scores (DAICc <2) and computed conditional averages (only selected models). Number of models in which a
variable was included and its importance (sum of model weights over models including the variable) is provided. All the variables, except for
PCA components, were scaled to improve homoscedasticity and model performance. Significant effects are marked with bold.
bSE z P N models Importance
A
Intercept <0.01 0.13 <0.01 1.00
Aggressiveness -0.19 0.12 1.6 0.11 3 0.52
Body morphology -0.67 0.15 4.49 <0.01 6 1.00
Body size -0.14 0.1 1.39 0.17 3 0.42
HWI -0.28 0.2 1.42 0.16 3 0.42
B
Intercept <0.01 0.12 <0.01 1.00
Beak length -0.72 0.15 4.87 <0.01 3 1.00
HWI -0.46 0.17 2.68 0.01 3 1.00
Aggressiveness -0.14 0.12 1.1 0.27 1 0.29
Tarsus length 0.13 0.18 0.72 0.47 1 0.20
64 E. Pagani-N
u~
nez et al. / Basic and Applied Ecology 59 (2022) 5969

significant relationships with niche overlap in any habitat
type (Supplementary Material S5).
Discussion
Multidimensional trait approaches examining dynamic
interactions between functional traits and multiple dimen-
sions of niche use, and considering species’evolution, are
fundamental to ascertain community assembly rules and
niche structure dynamics (Cadotte et al., 2013;Kraft et al.,
2008). In this study, we found support to our hypothesis that
specialized morphologies directly linked to resource use
(beak length and the ratio between beak and tarsus length)
would decrease in importance in predicting niche character-
istics with increasing habitat transformation (Fig. 3). Other
traits such as aggressiveness and body size determined niche
width and overlap in transformed habitats, suggesting a pro-
found change in how these communities are structured. This
change was probably elicited by a contraction of the mor-
phological trait space and species’need to exploit broader
niches to guarantee population viability, across this gradient.
Nevertheless, some of these results were unexpected.
Aggressiveness was linked to smaller niche widths rather
than to lower niche overlap in urban habitats, and larger
body sizes were linked to lower niche overlap rather than
larger niche widths in rural habitats. All in all, these findings
are important in suggesting that a combination of morpho-
logical and behavioral traits rather than single traits
(Pigot et al., 2020)determine niche characteristics, and
that these relationships are dynamic across habitat transfor-
mation gradients (Gravel et al., 2006).
Trait-niche relationships and niche partitioning in
transformed habitats
Morphology and behavior determine species’function
and position in communities and ecosystems (Ferry-
Graham et al., 2002). Across the last decades, many studies
have regarded specialized morphologies as the main driver
of niche partitioning in assemblages of closely related spe-
cies. For instance, bats and fishes partition their niches
according to highly evolved morphologies and refined forag-
ing techniques that enable the exploitation of particular prey
types (Aguirre et al., 2002). Similarly, birds are relatively
specialized animals and strict omnivory is rather uncommon
(Burin et al., 2016). Surprisingly, previous studies have
shown a relatively weak match between form and function
i.e. between morphological traits and niche position in
birds (Pigot et al., 2020;Ricklefs, 2012), inverse relation-
ships between microhabitat use and morphological speciali-
zation in tropical fishes (Brandl et al., 2015), and divergent
mechanisms allowing coexistence between old and young
avian lineages (Laiolo et al., 2017). We found that morpho-
logical traits determined niche overlap in natural and rural
habitats, while increased aggressiveness was only linked to
narrower niche widths in urban habitats. Therefore, our
results illustrate highly dynamic trait-niche relationships by
exploring the association among its multiple dimensions and
in the context of habitat transformation. Our study is thus in
line with a growing body of literature suggesting that a com-
bination of niche and neutral processes drive community
structure and assembly rules (Burson et al., 2019;
Simmons et al., 2020).
Biotic homogenization and species’
complementarity
Generalist species can be considered functionally equiva-
lent and thus are often regarded as redundant, a pattern par-
ticularly evident in transformed habitats (Devictor et al.,
2008;McKinney, 2006). However, functionally similar
Table 2. A) Results of phylogenetic generalized least squares
regression (PGLS) using niche width as dependent variable, and
the interaction between habitat type (natural, rural, or urban) and
the PCA component aggressiveness (pecking rates and distress
calls vs breath rate) as continuous predictors. B) We ran additional
models using niche overlap as dependent variable, and the interac-
tion between habitat type (natural, rural, or urban) and body mor-
phology, beak length (mm) and the PCA component body size as
continuous predictors. All the variables (except for PCA compo-
nents) were scaled to improve homoscedasticity and model perfor-
mance. Significant effects are marked with bold.
bSE z P
A - Niche width
(λ= 0.86, R
2
= 0.06)
Intercept 0.94 0.46 2.04 0.05
Aggressiveness*natural 0.10 0.13 0.73 0.47
Aggressiveness*rural -0.32 0.26 -1.20 0.24
Aggressiveness*urban -0.50 0.23 -2.20 0.03
B - Niche overlap
(λ= 0.00, R
2
= 0.33)
Intercept -0.10 0.15 -0.64 0.53
Body morphology*natural -0.53 0.18 -2.97 0.01
Body morphology*rural -1.17 0.38 -3.06 <0.01
Body morphology*urban -1.10 0.57 -1.92 0.06
(λ= 0.00, R
2
= 0.23)
Intercept 0.04 0.15 0.29 0.77
Beak length*natural -0.62 0.20 -3.12 <0.01
Beak length*rural -0.56 0.26 -2.13 0.04
Beak length*urban -0.05 0.31 -0.15 0.88
(λ= 0.00, R
2
= 0.05)
Intercept -0.07 0.15 -0.44 0.66
Body size*natural -0.10 0.13 -0.80 0.43
Body size*rural -0.39 0.19 -2.05 0.05
Body size*urban 0.06 0.12 0.55 0.59
E. Pagani-N
u~
nez et al. / Basic and Applied Ecology 59 (2022) 5969 65

species likely have the need to partition available niches to a
certain extent. Our findings support that niches are parti-
tioned based on traits such as aggressiveness and body size
in transformed habitats supports the view that this notion of
redundancy can drive to misconceptions (Petchey et al.,
2007). Interestingly, human disturbance and available
human food resources have been linked to increased overlap
in carnivore communities (Manlick & Pauli, 2020), yet pre-
vious studies have also suggested that alternative mecha-
nisms, such as temporal and spatial segregation in response
to human disturbance, could facilitate species coexistence
(Di Bitetti et al., 2010;Schuette et al., 2013). In transformed
habitats in our subtropical study system, food resources are
relatively high. In addition to the comparatively small body
size of birds and thus the capacity to sustain diverse
assemblages across small spatial scales (e.g., through verti-
cal stratification) (Pagani-N
u~
nez, He, et al., 2017), this
would facilitate niche partitioning. Still, body size and
aggressiveness shaped species’niches, suggesting that com-
petitive interactions play a key role in structuring these
assemblages.
Conclusion
We recorded dynamic and heterogeneous trait-niche rela-
tionships across multiple dimensions of niche characteristics
and axes of variation of morphological and behavioral traits.
The relationships between traits and niches and the diver-
gence in the traits explaining niche characteristics were
Fig. 3. Relationships between trait and niches characteristics for 44 populations of 29 passerine species in 8 locations across habitat transfor-
mation gradients (natural, rural, or urban). (A) Relationship between principal component analysis component aggressiveness (pecking rates
and distress calls vs breath rate) and niche width (Standard Ellipse Areas corrected by sample size) (aggressiveness vs niche width in urban:
z= -2.20, P= 0.03), (B) relationship between the principal component analysis components body morphology (beak vs tarsus length) and
niche overlap (body morphology vs niche overlap in natural: z= -2.97, P= 0.01; body morphology vs niche overlap in rural: z= -3.06, P<
0.01), and (C) relationship between scaled beak length and niche overlap (beak length vs niche overlap in natural: z= -3.12, P<0.01; beak
length vs niche overlap in rural: z= -2.13, P= 0.04). Regression lines are shown where these relationships were significant.
66 E. Pagani-N
u~
nez et al. / Basic and Applied Ecology 59 (2022) 5969

strong, so that they likely represent generalizable tendencies
and might apply to other vertebrate taxa. Habitat transforma-
tion is a pervasive force eroding complex species interac-
tions (Emer et al., 2019;Pringle et al., 2019). Consequently,
species traits have variable importance in predicting niche
characteristics in species’assemblages across the natural-to-
urban gradient, hinting at complex responses to global
change. Integrating individual to community level niche
dynamics is fundamental to disentangle the inherent com-
plexity of biodiversity patterns and community assembly
rules in a rapidly changing world.
Declaration of Competing interest
The authors declare that they have no known competing
financial interests or personal relationships that could have
appeared to influence the work reported in this paper.
Acknowledgements
We are grateful to Craig A. Barnett, Demeng Jiang,
Ruchuan He, Indika Peabotuwage, Ge Gao, Wande Li,
Guansheng Wang, Qiang Yang and Binqiang Li for their
help in the field. We are also grateful to the Forestry Bureau
of Guangxi Zhuang Autonomous Region, to the managers
of Damingshan National Reserve, Gaoligongshan National
Reserve, Longshan Regional Reserve, Medicinal Botanical
Garden of Guangxi, and Gaofeng National Forest Park for
providing required permissions. This study was funded by
The Special Talent Recruitment Program of Guangxi Uni-
versity (GXU) to EG, the Postdoctoral Research Fund of
GXU to EPN, the Fundamental Research Funds for the Cen-
tral Universities (161gpy34) to YL, and the National Natural
Science Foundation of China (31660612) to XL.
Supplementary materials
Supplementary material associated with this article can be
found in the online version at doi:10.1016/j.
baae.2022.01.002.
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