Austral Ecology (2021) 46, 603–612

Influence of altitude and climate on species richness and

endemism: A study case with non-volant small mammals
in the Atlantic Forest, Brazil


ATILLA COLOMBO FERREGUETTI,1,2*

MARJORE BEZERRA DE MENEZES,3
1
JULIANE PEREIRA-RIBEIRO, CARLOS FREDERICO DUARTE ROCHA1 AND
1
HELENA GODOY BERGALLO
1
ario Esp
ırito-Santense/FAESA, Rua Anselmo Serrat 199,
Department of Biology, Centro Universit

Ilha de Monte Belo, Vit
oria, ES, 29053-250, Brazil; (Email: Atilla.ferreguetti@gmail.com)
2
Department of Ecology, Rio de Janeiro State University, Rio de Janeiro, RJ, Brazil; and 3Department
of Ecosystem Science and Management, Intercollege Graduate Degree Program in Ecology, Pennsylvania
State University, University Park, Pennsylvania, USA

Abstract Elevational gradients usually help to explain the potential factors underlying global biodiversity, as
changing altitude leads to strong habitat changes in a relatively small area. We tested the influence of the altitude
gradient on the small non-volant mammal’s community along the regional landscape of the Atlantic Forest
located of the Esp
ırito Santo state, Brazil. We trapped non-volant small mammals from January 2017 to October
2018 in 12 locations distributed along an altitude gradient ranging from sea level to 2100 m above sea level
(asl). We ordered the non-volant small mammal species by using a Non-Metric Multidimensional Scaling analy-
sis using the Bray–Curtis metric. To understand how the altitude, vegetation types and climate variables influ-
ence the richness and abundance of species, we fitted generalised linear model. We observed that small mammal
species composition differed according to altitude, with higher richness in locations with intermediate altitude
between 500–1500 m asl. In locations with higher altitude, between 1501–2200 m asl, we recorded a lower spe-
cies richness, but higher endemism. Our results suggest altitude influenced the community of non-volant small
mammals. However, altitude direct influence on other variables is not evaluated in the present study, such as
food availability. In addition, we found a high endemism in higher altitude areas, pointing out the importance of
conserving these mountain areas for the preservation of endemic species. Thus, highlighting the importance of
this study to suggest areas that deserve greater attention in the development of management and conservation
plans.

Key words: altitudinal gradient, marsupials, mid-domain effect, rodents, species richness.

INTRODUCTION 2014). Mountains environments are intrinsically

Documenting spatial patterns in species richness,
composition and abundance together with under-
standing the mechanisms determining these patterns
has long been the focus of ecological and biogeo-
graphic studies. Elevational gradients help to explain
potential factors underlying global biodiversity
(McCain & Grytnes 2010; Antonelli et al. 2018) as
changing altitude leads to strong habitat changes in a
relatively small area (Grabherr et al. 2003; K€ orner
2007; Rahbek et al. 2019a). These changes have
direct impact on species richness and composition of
the community (Rickart 2001; McCain 2004; Novillo
& Ojeda 2014; Benedek & S^ırbu, 2019; Rahbek et al.
2019b) as well as on species occurrence and abun-
dance (Sundqvist et al. 2013; Andrade & Monjeau
*Corresponding author:
Accepted for publication January 2021.
unstable systems, undergoing substantial changes in
response to tectonic, erosional and climatic processes
over geologically short time scales (Badgley et al.
2017; Antonelli et al. 2018; Rahbek et al. 2019b).
Mountains can act like hotbeds of speciation, espe-
cially in the tropics, influenced by geological and cli-
matic dynamics over deep time forming centres of
endemism (Jetz et al. 2004; Rahbek et al. 2019b). For
example, several organisms show a species diversity
peak at intermediate altitudes having comparatively
lower diversity at extreme altitudes (Rahbek 1995;
Siqueira & Rocha 2013). Possible explanations for
mid-elevation peak in species richness include
increased rainfall and relative humidity and the
mostly geometric effect of overlapping ranges of spe-
cies with broad elevation range (Colwell & Lees
2000; Colwell et al. 2004). The latter is called the
mid-domain effect (MDE), and it is supported by a
substantial amount of empirical data from a range of

© 2021 Ecological Society of Australia doi:10.1111/aec.13010

604
F E R R E G U E T T I ET AL.
A.
organismal groups (Grytnes & Vetaas 2002; Sanders
2002; Geise et al. 2004; McCain 2004; Cardel
us
et al. 2006; Grytnes et al. 2008; Stanley et al. 2014;
Shuai et al. 2017; Sakane et al. 2019).
The relief of the state of Esp
ırito Santo, as well as
the forest remnants of the Atlantic Forest, together
form an excellent ‘natural laboratory’ for the study of
fauna and flora composition along the altitudinal gra-
dient. The remnants of Atlantic Forest in Esp
ırito
Santo state are located from sea level to 2897 m
above sea level (asl), where it is located the third-
highest elevational point in Brazil, Pico da Bandeira,
in the Capara
o National Park (IPEMA 2005). The
state of Esp
ırito Santo encompasses regions that can
be still considered knowledge gaps, because the
research on mammals is still incipient and / or con-
centrated on studies solely reporting species lists
(Moreira et al. 2008). In addition, both studies con-
ducted in the Atlantic Forest had a local focus (Geise
et al. 2004; Sakane et al. 2019). Therefore, there is a
gap in understanding how altitude influences biodi-
versity on a regional scale involving different forma-
tions of the Atlantic Forest. Non-volant small
mammals (marsupials and rodents) are excellent
models for testing diversity patterns, as in natural
communities they act in different trophic levels and
are seed predators and dispersers (Moura et al.
2008).
Therefore, we aimed to look for correlation
between species composition, richness and abun-
dance with altitude in the Atlantic Forest located in
the Esp
ırito Santo state, Brazil. We aimed to answer
the following questions: (1) Is there a variation in
species richness and abundance along the altitudinal
gradient? (2) Is there any trend of higher rate of
endemism in areas comparatively higher in altitude?
(3) To what extent rainfall and temperature explain
species richness and abundance along the altitudinal
gradient? (4) What is the effect of different vegetation
formations on mammals along the altitudinal gradi-
ent? For these questions, we constructed the follow-
ing outcomes: Species richness should be higher at
intermediate altitudes as indicated by the Mid-
Domain Effect, and the rate of endemism should be
higher at higher altitudes because mountains can be
considerate as forming centres of endemism (Jetz
et al. 2004; Rahbek et al. 2019b).
MATERIAL AND METHODS
Study area
We trapped non-volant small mammals in 12 locations in
Esp
ırito Santo state, Brazil (Fig. 1; Table 1). We dis-
tributed the sampling sites along an altitude gradient rang-
ing from sea level to 2100 m asl. (Fig. 1; Table 1). Esp
ırito
doi:10.1111/aec.13010
Santo state is located within the Atlantic Forest Biome
domains, presenting four main vegetation types: (1) Coastal
Plain Forest, (2) Dense Ombrophilous Forest, (3) Semi-
Deciduous Forest and (4) Altitude Forest/Fields (Lani et al.
2008).
All locations were selected according to similar character-
istics of protection and preservation. Of the 12 locations,
10 are areas protected by law. Two locations, although not
protected, are located in preserved regions of the Atlantic
Forest. Each locality features (i.e. cumulative precipitation,
management category, temperature and vegetation) are
summarised in Table 1.
Data collection
We collected data from January to March 2017, October
2017 to March 2018, and October 2018. We conducted
our sampling in the rainy season to control the seasonality.
We visited each sampling location for three campaigns. In
each of the 12 locations, six sampling sites were defined,
excepting in Capara
o National Park (CNP) where 12 sam-
pling sites were installed because CNP has twice the area
when compared with other locations. All sampling sites
were spaced at least 500 m apart. In each sampling site, we
defined six sampling stations that consisted of a plot of
10 9 10 m with a minimum distance of 50 m between sta-
tions. In each sampling station, we installed five live-traps,
one tomahawk (size: 45 9 21 9 21 cm) in the centre and
four Shermans (size: 25 9 8 9 9 cm) at the corners. The
traps remained open for three consecutive nights in each
campaign and were checked every morning.
We used a bait composed of banana, sardines, ground
peanuts and cornmeal, mixed until it became a homoge-
neous paste. For each captured animal, we recorded: the
date of capture, the point at which it was captured and
identified the species. We marked the individuals with
numbered ear tags to make it possible to recognise if the
individual had been recaptured. After all the information
was collected, the individual was released in the same place
where it was captured. We used field guides, such as: mam-
mals guide (Emmons & Feer 1997) and guide specifics
such as the Rodents Guide of Brazil (Bonvicino et al. 2008)
for species identification. The species that were not possible
to identify only with external characters were classified in
genus and differentiated by morphotypes. This study was
conducted with the research licence Process 76444341 –
Authorization 003A-2017 provided by the ‘Instituto Estad-
ual de Meio Ambiente e Recursos H
ıdricos – IEMA’.
Data analysis
We performed Moran’s I (Dormann et al., 2007) to check
for spatial autocorrelation. Values of Moran’s I range from
1 (indicating perfect dispersion) to +1 (perfect correla-
tion). Moran’s I was computed using a permutation-based
test (99 permutations at 5% significance level using the
‘moran.cp’ function in the ‘spdep’ package in R; Bivand,
2010). We did not find spatial autocorrelation in the resid-
uals (Moran’s I = 0.64).
© 2021 Ecological Society of Australia
 ALTITUDE AND CLIMATE EFFECT ON MAMMALS 605

Fig. 1. (a) Map of 12 sampling locations along Esp
ırito Santo state, southeastern Brazil; and (b) variation in altitude of each
sampling site. CNP – Capara
o National Park; FGSP – Forno Grande State Park; PASP – Pedra Azul State Park; ISP –
unas State Park; PCSP – Paulo C
esar Vinha State Park; SEP – Setiba Environmental Protection Area; GEP – Goiapaba-
Ita

Acßu Environmental Protection Area; MFSP – Mata das Flores State Park; AB – Aguia
Branca Private Reserve of Natural
Heritage; VM – Viana municipality; SLM – Santa Leopoldina municipality; and DBBR – Duas Bocas Biological Reserve.

We ordered the composition and abundance data of the RESULTS

non-volant small mammal species in each sampling site
using a Non-Metric Multidimensional Scaling analysis
(NMDS) using the Bray–Curtis metric to calculate the dis-
similarity in the species composition and frequency of
records per species between sites. The analyses were per-
formed in R software version 3.4.4 using the ‘metaMDS’
function in the Vegan package version 2.5–4 for community
analysis (Oksanen et al. 2013). This analysis aimed to verify
the existence of altitudinal pattern in the ordering of the
community.
We fitted generalised linear model (GLM; Poisson error
distribution) to understand how the altitude and climate
variables influence the richness and abundance of species.
We used as predictors the accumulated rainfall in the stud-
ied period (rainfall), mean air temperature (temperature),
vegetation cover and altitude. Cumulative rainfall data (in
mm) and temperature (°C) for each sampling locality were
obtained using local meteorological stations. Correlations
between all covariates were relatively low (Pearson correla-
tion coefficients < 0.5; Appendix S1). We considered as
plausible all models at DAIC < 2 from the best-fitted model
(Burnham & Anderson 2002). We calculated model sup-
port using Akaike weights (wAIC, ranging from 0 to 1, with
larger numbers indicating greater support; Burnham &
Anderson 2002). All analyses were performed in R 3.4 (R
Core Team 2017). Species were classified as endemic to
Atlantic Forest according to Paglia et al. (2012) and
according to the degree of threat in the Brazilian list (ICM-
Bio 2018) and the global list of threatened species (IUCN
2020).
We recorded 45 species of non-volant small mam-
mals in the 12 studied localities, 13 species belonging
to the order Didelphimorphia and 32 species to the
order Rodentia (Appendix S2). Of the 45 species
recorded, 22 species (52.5%) are endemic to the
Atlantic Forest, three species are classified as Vulner-
able and two species are classified as Near Threat-
ened in the Brazilian species red list (ICMBio 2018),
and no species are threatened in the global red list
(IUCN 2020).
Twelve species were captured exclusively at CNP,
the locality with highest altitude of Esp
ırito Santo
state (Appendix S2). These species are: Akodonsp.2,
A. sp.3, Brucepattersonius griserufescens, Calomys callo-
sus, Delomys altimontanus, Juliomyssp.1, Oxymycterus
caparaoe, Oxymycterus hispidus, Rhagomys rufescens,
Trinomys gratiosus, Marmosops paulensis, and Monodel-
phis scalops.
The composition of the non-volant small mammal
community differed between the sampled localities in
the Atlantic Forest of Esp
ırito Santo state, grouping
the sampling sites with higher similarity according to
the altitude gradient (Fig. 2). We observed that spe-
cies composition differed consistently according to
altitude, with higher richness in locations with inter-
mediate altitude between 500–1500 m asl (33

© 2021 Ecological Society of Australia doi:10.1111/aec.13010

606
F E R R E G U E T T I ET AL.
A.

Table 1. Features of each study location in the Esp
ırito Santo state, southeastern Brazil

Minimum Maximum Average Cumulative

Management Vegetation Altitude temperature temperature temperature rainfall
Locality category type Range (m) (°C) (°C) (°C) (mm)

Duas Bocas Protected area Dense 250–620 20 30 26 810

Biological (biological Ombrophilous
Reserve reserve) Forest
Ita

unas State Park Protected area Coastal Plain 0–12 22 35 27 352
(state park) Forest
Paulo C
esar Vinha Protected area Coastal Plain 0–14 21 34 27 730
State Park (state park) Forest
Setiba Protected area Coastal Plain 0–22 22 34 27 363
Environmental (sustainable Forest
Protection Area use area)
Goiapaba-Acßu Protected area Dense 180–470 19 29 26 369
Environmental (sustainable Ombrophilous
Protection Area use area) Forest
Capara
o National Protected area Altitude 950–1890 11 26 22 1250
Park (national Forest/fields
park)
Forno Grande Protected area Altitude 890–1250 15 27 25 850
State Park (state park) Forest/fields
Pedra Azul State Protected area Dense 910–1300 14 26 23 795
Park (state park) Ombrophilous
Forest


Aguia Branca Protected area Dense 850–1220 17 27 24 810
Private Reserve (sustainable Ombrophilous
of Natural use area) Forest
Heritage
Mata das Flores Protected area Semi-Deciduous 120–480 21 31 27 401
State Park (state park) Forest
Viana municipality Non-protected Dense 140–620 20 29 27 710
area Ombrophilous
Forest
Santa Leopoldina Non-protected Dense 110–340 21 31 27 590
municipality area Ombrophilous
Forest

recorded species; Fig. 3). In locations with higher

Fig. 2. Non-Metric Multidimensional Scaling (NMDS)
based on Bray–Curtis distances between localities sampled in
the richness and abundance of non-volant small mammals in
the Atlantic Forest of Esp
ırito Santo state, Brazil. Red: high-
est altitude sampling sites; Green: intermediate altitude sam-
pling sites; and Blue: lowest altitude sampling sites.
altitude, between 1501–2200 m asl, we recorded a
lower species richness (26 species; Fig. 3).
We captured a total of 22 endemic species, and
about 37% of endemic species (eight species) cap-
tured exclusively in the higher altitude area, more
precisely in the CNP (Fig. 3). The remaining 14
endemic species were captured in all altitudinal
ranges (Appendix S2). No endemic species were cap-
tured exclusively in altitudinal ranges between 0–
1500 m asl (Fig. 3).
We found support that two variables (i.e. altitude
and accumulated precipitation ‘rainfall’) best pre-
dicted species richness in the sampled localities, with
a wAIC of 0.45 for the model with only altitude, and
with a wAIC of 0.31 for the model with both vari-
ables (Table 2). For species abundance, we also
found support that same variables (i.e. altitude and
accumulated rainfall) best predicted species response
with a wAIC of 0.33 for the model with both vari-
ables and with a wAIC of 0.31 for the model with

doi:10.1111/aec.13010 © 2021 Ecological Society of Australia

 ALTITUDE AND CLIMATE EFFECT ON MAMMALS
Fig. 3. Ordination of non-volant small mammals in relation to the altitude gradient of the Atlantic Forest sampled localities
in the Esp
ırito Santo state, Brazil.
only altitude (Table 2). We found no support that
temperature and vegetation type would be good pre-
dictor variables for species richness and abundance.
Species richness and abundance were higher at inter-
mediate altitudes (Fig. 4a and b) and increased with
higher accumulated precipitation values (Fig. 4b and
d).
DISCUSSION
Our study found evidence of a mid-domain effect in
non-volant mammals. We recorded a higher species
richness (i.e. 33 species of non-volant small mam-
mals) at locations with intermediate altitude ranging
from 500 to 1500 m asl. The recorded richness cor-
responds to about 80% of non-volant small mammals
presently known to occur in Esp
ırito Santo state
(Moreira et al. 2008) and about 34% of the known
species to the Atlantic Forest Biome (Paglia et al.
2012). This high species richness at intermediate alti-
tudes may be related to the mid-domain effect.
McCain (2004) described a mid-domain effect
© 2021 Ecological Society of Australia
607
related to small mammals, where species richness
culminates in locations at intermediate elevations
associated with optimal natural conditions (Lomolino
2001). The mid-domain effect means the increase of
richness with altitude up to a point (Wake et al.
1992; Grytnes et al. 2006). This effect is more fre-
quently demonstrated to occur along the tropical ele-
vation gradient of Central and South America
(S
anchez-Cordero 2001; McCain 2004; Andrade &
Monjeau 2014; Novillo & Ojeda 2014), although it
has also been confirmed in the gradient of several
Southeast and East Asia mountains (Nor 2001; Li
et al. 2003). Some authors corroborate the idea that
there was limitation in the dispersion of ancestors
that were in the medium elevations, occurring spe-
cialisation and tolerance to a certain climate, thus
providing a richness peak at medium altitudes (Smith
et al. 2007; Wiens et al. 2007). Graham et al. (2014)
argued that the variation in species richness and
diversity along an altitudinal gradient is strongly
linked to the natural history and environmental char-
acteristics of each chain of mountains. In Brazil, a
similar trend was recorded in other areas of the
doi:10.1111/aec.13010
608
F E R R E G U E T T I ET AL.
A.

Table 2. Generalised linear models (GLM; binomial mammals (Stanley et al. 2014; Sabuni et al. 2018). In
error distribution and logit link function) that best fact, high altitude areas are important landforms for
explained richness and abundance of non-volant small both biodiversity and the evolution of endemism
mammals selected by AIC in the 12 locations of the Atlan-
(Krukeberg & Rabinovitz 1985; Jim
enez-Mejias et al.
tic Forest, Esp
ırito Santo, Brazil, from January 2017 to
October 2018 2015; Rahbek et al. 2019B), and consequently also
for conservation (e.g. Rosenzweig 1995; Moritz et al.
Model AIC DAIC wAIC 2000; Tang et al. 2006; Fjeldsa et al. 2012). More-
over, some species may have a physiological limit that
Richness reflects their restriction to certain environments,
Altitude 156.26 0 0.45
where climate is determinant for reproduction rate,
Precipitation + Altitude 158.12 1.86 0.31
NULL 160.23 3.97 0.09 therefore interfering with the population structure
Precipitation 160.42 4.16 0.08 (Brown 2001; Hawkins et al. 2003).
Altitude + Temperature 161.52 5.26 0.04 The accumulated precipitation of the period in the
Precipitation + Altitude 164.63 8.37 0.02 different sampling sites positively affected both, spe-
+ Temperature cies richness and abundance. Climate conditions
Precipitation + Temperature 165.36 9.1 0.01 limit the number of species that can survive at differ-
Abundance
Precipitation + Altitude 169.15 0 0.33
ent locations and elevations, while the physiological
Precipitation 170.25 1.1 0.31 limits of species affect their occurrence (McCain &
Altitude 170.58 1.43 0.18 Grytnes 2010). Current meteorological conditions
NULL 172.56 3.41 0.09 may also have significantly positive influence on small
Precipitation + Altitude 175.23 6.08 0.04 mammals (Stokes et al. 2001). Moreover, the rela-
+ Temperature tionship with precipitation could be related to the
Precipitation + Temperature 178.69 9.54 0.03
availability of food resources, which is higher in rainy
Altitude + Temperature 180.05 10.9 0.02
periods (Graipel et al. 2006; Santos-Filho et al.
Variables: precipitation = accumulated precipitation 2006). Moreover, in the rainy season, due to com-
(rainfall), temperature = mean temperature, Altitude = alti- paratively higher food availability, the reproductive
tude in each sampling site (m), vegetation cover. period of most non-volant small mammal species
tends to concentrate (Bergallo & Magnusson 1999,
Atlantic Forest with small mammals, where a higher 2002; Graipel et al. 2006). In fact, several studies
species richness occurred at intermediate altitudes have tested altitude as a driver of species diversity,
(Geise et al. 2004; Sakane et al. 2019). This pattern pointing to other variables, such as temperature and
in the Atlantic Forest and other tropical locations is precipitation (i.e. climate), which together act for the
because higher altitude locations present extreme MDE (Colwell & Lees 2000; Colwell et al. 2004).
environmental features. On the other hand, we did not find a relationship of
High altitudes, while having lower species diversity, temperature with the richness and abundance of
present high levels of endemism with eight endemic non-volant small mammals. This result may be
species, about 37% of all endemic species recorded related to the low seasonality of air temperature
in the present study. The remaining endemic species recorded in the studied locations. In addition to the
were distributed similarly in altitudinal gradient. The climate variables tested, other factors may be acting
vegetation and climate at higher altitude sampling in the community of non-volant small mammals,
sites are distinct when we compare all our sampled such as topography (terrain relief), historical factors
locations. However, vegetation type is not a good (occurrence of species across evolutionary time-
predictor in our study for richness, the distinct vege- scales), heterogeneity and habitat complexity (vertical
tation can still be responsible for the higher ende- strata within habitat) and the influence of other biotic
mism. We believe that for small mammals the soil factors (Kelt et al. 1994; Lomolino 2001; Rahbek &
and other microhabitat variables present in the vege- Graves 2001; Jetz & Rahbek 2002; McCain & Gryt-
tation type found at high altitudes may be better pre- nes 2010; Mena & Medellin 2017).
dictors. In fact, the Serra do Capara
o area above Our results suggest altitude as a structuring element
1500 m altitude have particular characteristics as in the community of non-volant small mammals. The
lithological basement soils (Simonelli & Fraga 2007); altitude had a significant influence on the richness and
therefore, it is considered by some authors as a for- abundance of non-volant small mammals. However,
mation restricted to the CNP (Garbin et al. 2017), altitude can influence on other factors not evaluated in
which could favour endemism. The uniqueness of the present study, such as food availability, which
mountain environmental conditions encourages the therefore may affect the fauna. In addition, we found a
existence of different types of refugia and survival of high endemism exclusively in more extreme altitudes,
relict endemic species (Jen
ık & Stursa 2003; Jetz pointing out the importance of conserving these
et al. 2004; Rahbek et al. 2019B), including small mountain areas for the preservation of these species.
doi:10.1111/aec.13010 © 2021 Ecological Society of Australia
 ALTITUDE AND CLIMATE EFFECT ON MAMMALS 609

Fig. 4. Relationships between the richness and (a) altitude (m), (b) abundance and altitude (m), (c) richness and accumu-
lated rainfall of studied period (mm), and (d) abundance and accumulated rainfall of studied period (mm) in the localities
studied of the Atlantic Forest, Esp
ırito Santo state, Brazil.

Thus, highlighting the importance of this study to sug-
gest areas that deserve greater attention in the develop-
ment of management and conservation plans. Finally,
we suggest that other studies with the same focus eval-
uate other variables not considered in this study. We
believe that studies like this one, that characterise the
community of non-volant small mammals, could con-
tribute for management and conservation plans. Gra-
dient analysis of species and their distribution not only
provide input to ecology and environment, but also
guide their conservation and management pro-
grammes.
ACKNOWLEDGEMENTS
authors benefitted from grants provided to HGB
(process 307781/2014-3) and to CFDR (302974/
2015-6 and 424473/2016-0) from CNPq and through
‘Cientistas do Nosso Estado’ programme from
FAPERJ to CFDR (processes Nos. E-26/
202.920.2015 and E-26/202.803/2018) and to HGB
(process E-26/201.267.2014). HGB and CFDR
thank Proci^encia/UERJ. This study was conducted
with the research licence Process 76444341 – Autho-
rization 003A-2017 provided by the ‘Instituto Estad-
ual de Meio Ambiente e Recursos H
ıdricos –
IEMA’. This study was financed in part by the Coor-
denacß~ao de Aperfeicßoamento de Pessoal de N
ıvel
Superior – Brasil (CAPES) – Finance Code 001.

This study includes part of the results of the ‘Pro-
grama de Pesquisas em Biodiversidade da Mata
Atl^antica (PPBio Mata Atl^antica Network)’ of Min-
ist
erio de Ci^encia, Tecnologia, Inovacß~ao e Comu-
nicacß~ao (MCTIC) and was supported by Conselho
Nacional de Desenvolvimento Cient
ıfico e Tec-
nol
ogico (CNPq) (Process No. 457458/2012-7). The
© 2021 Ecological Society of Australia
AUTHOR CONTRIBUTION


Atilla Colombo Ferreguetti: Conceptualization
(equal); Data curation (equal); Formal analysis
(equal); Funding acquisition (equal); Investigation
(equal); Methodology (equal); Project administration
(lead); Supervision (equal); Writing-original draft
doi:10.1111/aec.13010
610
F E R R E G U E T T I ET AL.
A.
(equal); Writing-review & editing (equal). Marjore
Bezerra de Menezes: Conceptualization (equal);
Data curation (equal); Investigation (equal); Method-
ology (equal); Writing-original draft (equal); Writing-
review & editing (equal). Juliane Pereira Ribeiro:
Conceptualization (equal); Methodology (equal);
Writing-review & editing (equal). Carlos Frederico
Duarte Rocha: Conceptualization (equal); Funding
acquisition (lead); Methodology (equal); Resources
(lead); Supervision (equal); Writing-review & editing
(equal). Helena Godoy Bergallo: Conceptualization
(equal); Formal analysis (equal); Funding acquisition
(lead); Investigation (equal); Methodology (equal);
Resources (lead); Supervision (equal); Writing-review
& editing (equal).
CONFLICT OF INTEREST DISCLOSURE
There is no conflict of interest to report.
DATA AVAILABILITY STATEMENT
Data will be available on request.
REFERENCES
Andrade A. & Monjeau A. (2014) Patterns in community
assemblage and species richness of small mammals across
an altitudinal gradient in semi-arid Patagonia, Argentina.
J. Arid Environ. 106, 18–26.
Antonelli A., Kissling W. D., Flantua S. G. et al. (2018)
Geological and climatic influences on mountain
biodiversity. Nat. Geosci. 11(10), 718–25.
Badgley C., Smiley T. M., Terry R. et al. (2017) Biodiversity
and topographic complexity: modern and geohistorical
perspectives. Trends Ecol. Evol. 32(3), 211–26.
Benedek A. M. & S^ırbu I. (2019) Dynamics of small mammal
communities along an elevational gradient. Can. J. Zool.
97, 312–8.
Bergallo H. G. & Magnusson W. (1999) Effects of climate and
food availability on four rodent species in southeastern
Brazil. J. Mammal. 80(2), 472–86.
Bergallo H. G. & Magnusson W. E. (2002) Effects of weather
and food availability on the condition and growth of two
species of rodents in Southeastern Brazil. Mammalia 66(1),
17–32.
Bivand R. (2010). Package ‘spdep’. CRAN.
Bonvicino C. R., Oliveira J. A. & D’Andrea P. S. (2008) Guide
to Rodents in Brazil, with Genre Keys Based on External
Characters. OPAS/OMS Brasil, Rio de Janeiro.
Brown J. H. (2001) Mammals on mountainsides: elevational
patterns of diversity. Glob. Ecol. Biogeogr. 10(1), 101–9.
Burnham K. P. & Anderson D. R. (2002) Model Selection and
Multimodel Inference. A Practical Information–Theoretic
Approach. Springer-Verlag, New York (USA) (488 pp.).
Cardel
us C. L., Colwell R. K. & Watkins J. E. Jr (2006)
Vascular epiphyte distribution patterns: explaining the
mid-elevation richness peak. J. Ecol. 94(1), 144–56.
doi:10.1111/aec.13010
Colwell R. K. & Lees D. C. (2000) The mid-domain effect:
geometric constraints on the geography of species richness.
Trends Ecol. Evol. 15(2), 70–6.
Colwell R. K., Mao C. X. & Chang J. (2004) Interpolating,
extrapolating, and comparing incidence-based species
accumulation curves. Ecology 85(10), 2717–27.
Dormann C. F., McPherson J. M., Araujo M. B. et al. (2007)
Methods to account for spatial autocorrelation in the
analysis of species distributional data: a review. Ecography
30, 609–28.
Emmons L. H. & Feer F. (1997) Neotropical Rainforest
Mammals: A Field Guide. University of Chicago Press,
Chicago.
Fjeldsa J., Bowie R. C. & Rahbek C. (2012) The role of
mountain ranges in the diversification of birds. Annu. Rev.
Ecol. Evol. Syst. 43, 249–65.
Garbin M. L., Saiter F. Z., Carrijo T. T. & Peixoto A. L.
(2017) Breve hist
orico e classificacß~ao da vegetacß~ao
capixaba. Rodrigu
esia 68(5), 1883–94.
Geise L., Pereira L. G., Bossi D. E. P. & Bergallo H. G.
(2004) Pattern of elevational distribution and richness of
non volant mammals in Itatiaia National Park and its
surroundings, in southeastern Brazil. Brazilian Journal of
Biology 64(3B), 599–612.
Grabherr G., Nagy L. & Thompson D. B. A. (2003) An
outline of Europe’s alpine areas. In: Alpine biodiversity in
Europe, 1st edn (eds L. Nagy, G. Grabherr, C. H. K€ orner
& D. B. A. Thompson) pp. 3–12.Springer, Berlin. https://
doi.org/10.1007/978-3-642-18967-8_1.
Graham C. H., Carnaval A. C., Cadena C. D. et al. (2014)
The origin and maintenance of montane diversity:
integrating evolutionary and ecological processes.
Ecography 37(8), 711–9.
Graipel M. E., Cherem J. J., Monteiro-Filho E. L. & Glock L.
(2006) Din^amica populacional de marsupiais e roedores no
Parque Municipal da Lagoa do Peri, Ilha de Santa Catarina,
sul do Brasil. Mastozoolog
ıa Neotropical 13(1), 31–49.
Grytnes J. A., Beaman J. H., Romdal T. S. & Rahbek C.
(2008) The mid-domain effect matters: simulation analyses
of range-size distribution data from Mount Kinabalu,
Borneo. J. Biogeogr. 35(11), 2138–47.
Grytnes J. A., Heegaard E. & Ihlen P. G. (2006) Species
richness of vascular plants, bryophytes, and lichens along
an altitudinal gradient in western Norway. Acta Oecologica
29(3), 241–6.
Grytnes J. A. & Vetaas O. R. (2002) Species richness and
altitude: a comparison between null models and
interpolated plant species richness along the Himalayan
altitudinal gradient, Nepal. Am. Naturalist 159(3), 294–
304.
Hawkins B. A., Porter E. E. & Felizola Diniz-Filho J. A.
(2003) Productivity and history as predictors of the
latitudinal diversity gradient of terrestrial birds. Ecology 84
(6), 1608–23.
ICMBio – Instituto Chico Mendes de Conservacß~ao da
Biodiversidade. (2018). Livro Vermelho da Fauna Brasileira
Ameacßada de Extincßa ~o. http://www.icmbio.gov.br/portal/ima
ges/stories/comunicacao/publicacoes/publicacoes-diversas/
dcom_sumario_executivo_livro_vermelho_ed_2016.pdf
(accessed 26 March 2019).
IPEMA-Instituto de Pesquisas da Mata Atl^antica. (2005).
Conservacßa~o da Mata Atl^ antica no Esp
ırito Santo: cobertura
florestal e unidades de conservacßa~o. (Programa Centros para a
Conservacßa~o da Biodiversidade – Conservacßa ~o Internacional
do Brasil) IPEMA. IPEMA, Vit
oria, Esp
ırito Santo.
© 2021 Ecological Society of Australia
 ALTITUDE AND CLIMATE EFFECT ON MAMMALS
IUCN (International Union for Conservation of Nature).
(2020). The IUCN red list of threatened species. Version 2020-
3. IUCN, Gland, Switzerland. Available from http://www.
iucnredlist.org (accessed October 2020).
Jen
ık J. & Stursa J. (2003) Vegetation of the Giant Mountains,
Central Europe. Ecological Studies 1(167), 47–52.
Jetz W. & Rahbek C. (2002) Geographic range size and
determinants of avian species richness. Science 297(5586),
1548–51.
Jetz W., Rahbek C. & Colwell R. K. (2004) The coincidence of
rarity and richness and the potential signature of history in
centres of endemism. Ecol. Lett. 7(12), 1180–91.
Jim
enez-Mej
ıas P., Fern
andez-Mazuecos M., Amat M. E. &
Vargas P. (2015) Narrow endemics in European
mountains: high genetic diversity within the monospecific
genus Pseudomisopates (Plantaginaceae) despite isolation
since the late Pleistocene. J. Biogeogr. 42(8), 1455–68.
Kelt D. A., Meserve P. L. & Lang B. K. (1994) Quantitative
habitat associations of small mammals in a temperate
rainforest in southern Chile: empirical patterns and the
importance of ecological scale. J. Mammal. 75(4), 890–
904.
K€orner C. (2007) The use of ‘altitude’ in ecological research.
Trends Ecol. Evol. 22(11), 569–74.
Kruckeberg A. R. & Rabinowitz D. (1985) Biological aspects of
endemism in higher plants. Annu. Rev. Ecol. Syst. 16(1),
447–79.
Lani J. L., Resende M., de Rezende S. B. & Feitoza L. R.
(2008) Atlas de ecossistemas do Esp
ırito Santo. SEMA/
Vicßosa: UFV, Vit
oria, 504 p.
Li J. S., Song Y. L. & Zeng Z. G. (2003) Elevational gradients
of small mammal diversity on the northern slopes of Mt.
Qilian, China. Glob. Ecol. Biogeogr. 12(6), 449–60.
Lomolino M. V. (2001) Elevation gradients of species-density:
historical and prospective views. Glob. Ecol. Biogeogr. 10
(1), 3–13.
McCain C. M. (2004) The mid-domain effect applied to
elevational gradients: species richness of small mammals in
Costa Rica. J. Biogeogr. 31(1), 19–31.
McCain C. M. & Grytnes J. (2010) Elevational gradients in
species richness. In: John Wiley and Sons (eds)
Encyclopedia of life sciences. Chichester, UK. https://doi.org/
10.1002/9780470015902.a0022548.
Mena J. L. & Medellin R. A. (2017) Complejidad de h
abitat y
diversidad de mam
ıferos peque~ nos en un gradiente
altitudinal en el sur de M
exico. Mastozoologia Neotrop. 24
(1), 121–35.
Moreira D., Coutinho B. R. & Mendes S. L. (2008) O status
do conhecimento sobre a fauna de mam
ıferos do Esp
ırito
Santo baseado em registros de museus e literatura
cient
ıfica. Biota. Neotrop. 8(2), 163–73.
Moritz C., Patton J. L., Schneider C. J. & Smith T. B. (2000)
Diversification of rainforest faunas: an integrated molecular
approach. Annu. Rev. Ecol. Syst. 31(1), 533–63.
Moura M. C., Grelle C. E. V. & Bergallo H. G. (2008) How
does sampling protocol affect the richness and abundance
of small mammals recorded in tropical forest? An example
from the Atlantic Forest, Brazil. Neotropical Biol. Conserv. 3
(2), 51–8.
Nor S. M. (2001) Elevational diversity patterns of small
mammals on Mount Kinabalu, Sabah, Malaysia. Glob.
Ecol. Biogeogr. 10(1), 41–62.
Novillo A. & Ojeda R. A. (2014) Elevation patterns in rodent
diversity in the dry Andes: disentangling the role of
environmental factors. J. Mammal. 95(1), 99–107.
© 2021 Ecological Society of Australia
611
Oksanen J., Blanchet F. G. & Kindt R. et al. (2013) The vegan
package. Community ecology package. https://cran.ism.ac.jp/
web/packages/vegan/vegan.pdf. 30 October 2018.
Paglia A. P., da Fonseca G. A. B. & Rylands A. B. et al.
(2012) Annotated Checklist of Brazilian Mammals. In:
Occasional Papers in Conservation Biology (ed P. Adriano),
2nd edn. Conservation International, Arlington.
R Core Team (2017) R: A Language and Environment for
Statistical Computing. Vienna, Austria: R Foundation for
Statistical Computing, Vienna.
Rahbek C. (1995) The elevational gradient of species richness:
a uniform pattern? Ecography 18(2), 200–5.
Rahbek C., Borregaard M. K., Antonelli A. et al. (2019b)
Building mountain biodiversity: Geological and
evolutionary processes. Science 365(6458), 1114–9.
Rahbek C., Borregaard M. K., Colwell R. K. et al. (2019a)
Humboldt’s enigma: What causes global patterns of
mountain biodiversity? Science 365(6458), 1108–13.
Rahbek C. & Graves G. R. (2001) Multiscale assessment of
patterns of avian species richness. Proc. Natl Acad. Sci. 98
(8), 4534–9.
Rickart E. A. (2001) Elevational diversity gradients,
biogeography and the structure of montane mammal
communities in the intermountain region of North
America. Glob. Ecol. Biogeogr. 10(1), 77–100.
Rosenzweig M. L. (1995) Species Diversity in Space and Time.
Cambridge University Press, Cambridge, UK.
Sabuni C., Aghov
a T., Bryjov
a A., Sumbera R. & Bryja J.
(2018) Biogeographic implications of small mammals from
Northern Highlands in Tanzania with first data from the
volcanic Mount Kitumbeine. Mammalia 82(4), 360–72.
Sakane K. K., Percequillo A. R. & Setz E. Z. F. (2019)
Community of small mammals along an elevational gradient
in Biological Reserve of Serra do Japi, municipality of
Jundia
ı-SP, Brazil. Austral Ecol. 44(7), 1236–44.
S
anchez-Cordero V. (2001) Elevation gradients of diversity for
rodents and bats in Oaxaca, Mexico. Glob. Ecol. Biogeogr.
10(1), 63–76.
Sanders N. J. (2002) Elevational gradients in ant species
richness: area, geometry, and Rapoport’s rule. Ecography
25(1), 25–32.
Santos-Filho M., da Silva D. J. & Sanaiotti T. M. (2006)
Efficiency of four trap types in sampling small mammals in
forest fragments, Mato Grosso, Brazil. Mastozoolog
ıa
Neotrop. 13(2), 217–25.
Shuai L. Y., Ren C. L., Yan W. B., Song Y. L. & Zeng Z. G.
(2017) Different elevational patterns of rodent species
richness between the southern and northern slopes of a
mountain. Sci. Rep. 7(1), 8743.
Simonelli M. & Fraga C. N. (2007) Esp
ecies da flora ameacßadas
de extincßa~o no estado do Esp
ırito Santo, 146 p. Ipema,
Vit

oria.
Siqueira C. C. & Rocha C. F. D. (2013) Altitudinal gradients:
concepts and implications on the biology, the distribution
and conservation of Anurans. Oecologia Australis 17(2),
282–302.
Smith S. A., De Oca A. N. M., Reeder T. W. & Wiens J. J.
(2007) A phylogenetic perspective on elevational species
richness patterns in Middle American treefrogs: why so
few species in lowland tropical rainforests? Evol.: Int. J.
Organic Evol. 61(5), 1188–207.
Stanley W. T., Rogers M. A., Kihaule P. M. & Munissi M. J.
(2014) Elevational distribution and ecology of small
mammals on Africa’s highest mountain. PLoS One 9(11),
e109904.
doi:10.1111/aec.13010
612
F E R R E G U E T T I ET AL.
A.
Stokes M. K., Slade N. A. & Blair S. M. (2001) Influences of
weather and moonlight on activity patterns of small
mammals: a biogeographical perspective. Can. J. Zool. 79
(6), 966–72.
Sundqvist M. K., Sanders N. J. & Wardle D. A. (2013)
Community and ecosystem responses to elevational
gradients: processes, mechanisms, and insights for global
change. Annu. Rev. Ecol. Evol. Syst. 44, 261–80.
Tang Z., Wang Z., Zheng C. & Fang J. (2006) Biodiversity in
China’s mountains. Front. Ecol. Environ. 4(7), 347–52.
Wake D. B., Papenfuss T. J. & Lynch J. F. (1992) Distribution
of salamanders along elevational transects in Mexico and
Guatemala. Tulane Studies in Zoology and Botany,
Supplementary Publication 1, 303–19.
Wiens J. J., Parra-Olea G., Garc
ıa-Par
ıs M. & Wake D. B.
(2007) Phylogenetic history underlies elevational
biodiversity patterns in tropical salamanders. Proc. Royal
Soc. B: Biol. Sci. 274(1612), 919–28.
doi:10.1111/aec.13010
SUPPORTING INFORMATION
Additional supporting information may/can be found
online in the supporting information tab for this arti-
cle.
Appendix S1. Pearson correlation matrix of the
covariates used in the generalized linear models
(GLM; binomial error distribution and logit link
function) in the 12 locations of the Atlantic Forest,
Esp
ırito Santo, Brazil, from January 2017 to October
2018.
Appendix S2. Non-volant small mammals species
recorded in the 12 locations studied with their
respective altitude range (in m) for the Atlantic For-
est in the Esp
ırito Santo state, Brazil.
© 2021 Ecological Society of Australia