Species Richness and Beta Diversity

Patterns of American Marsupials

Felipe O. Cerezer, Nilton C. Cáceres, and Andrés Baselga

Contents
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
Species Richness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
Compositional Dissimilarity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
Species Richness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
Compositional Dissimilarity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
Species Richness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
Compositional Dissimilarity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
Cross-References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15

Abstract
Understanding the causes of spatial variation in biodiversity is a prominent issue
in ecology and biogeography. Here, the species richness and the change in the
species composition (beta diversity) of American marsupials were mapped and
the main predictors underlying these diversity patterns were investigated. Species
distribution maps covering the American continent were obtained from the IUCN

F. O. Cerezer (*)
Programa de Pós-Graduação em Biodiversidade Animal, Departamento de Ecologia e Evolução,
Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Santa Maria, Brazil
e-mail: cerezerfelipe@gmail.com
N. C. Cáceres
Departamento de Ecologia e Evolução, CCNE, Universidade Federal de Santa Maria, Santa Maria,
Brazil
A. Baselga
Depto de Zoología, Facultad de Biología, Univ. de Santiago de Compostela, Santiago de
Compostela, Spain

© Springer Nature Switzerland AG 2022 1

N. C. Cáceres, C. R. Dickman (eds.), American and Australasian Marsupials,
https://doi.org/10.1007/978-3-030-88800-8_13-1
2 F. O. Cerezer et al.

and mapped onto grid cells of 1
by 1
. For each grid cell, species richness and
species composition were quantified and climatic/environmental variables eco-
logically relevant for marsupials (e.g., energy and seasonality) were extracted.
Then, structural equation models were used to analyze the association between
species richness and predictor variables. Models of distance decay of similarity
and variance partitioning were applied to evaluate whether beta diversity (com-
positional dissimilarity) in the northern and southern hemispheres is related to
geographic or climatic distances. We show that energy availability and climatic
seasonality measures are the best predictors of the latitudinal cline in marsupial
species richness. We also recorded a latitudinal asymmetry in beta diversity in
which communities in the southern hemisphere exhibit a distinct species compo-
sition from those of the northern hemisphere and the contribution of geographic
and climatic distances differed between these regions of the Americas.

Keywords
Small mammals · Diversity gradients · Macroecology · Turnover component ·
Distance-decay · Structural equation

Abbreviations
FVS Forest vertical structure
IUCN International Union for Conservation of Nature
NPP Net primary productivity
PCoA Principal coordinate analysis
Pmin Precipitation of driest month
SEM Structural equation models
Tmean Annual mean temperature
Tmin Minimum temperature of coldest month
βjac Jaccard dissimilarity index
βjne Nestedness-resultant dissimilarities
βjtu Spatial turnover
ΔP Precipitation seasonality
ΔT Temperature seasonality

Introduction

Documenting how biological diversity is distributed in space and understanding the

determinants that produce this variation have been the focus of ecologists and
biogeographers for more than two centuries (Brown 2014). The increase in species
diversity toward the tropics (i.e., the Latitudinal Diversity Gradient) is one of the
most striking geographic patterns on Earth. Although there are a plethora of hypoth-
eses that attempt to explain latitudinal diversity gradients (Willig et al. 2003;
Hillebrand 2004), the relative importance of different mechanisms is still the subject
of intense debate (McGill et al. 2019).
Species Richness and Beta Diversity Patterns of American Marsupials 3

Across many animal taxa, the large-scale patterns in species richness have
generally been attributed to spatial variations in climatic conditions (Currie et al.
2004). Due to the ubiquity of the climate-diversity relationship (Hawkins et al.
2003a), different mechanisms have been widely proposed: (i) the “evolutionary
speed hypothesis” suggests that higher temperatures in the tropics may accelerate
metabolic processes (Brown et al. 2004), increasing the rates of molecular evolution
and speciation (Allen et al. 2006); (ii) the “more-individuals hypothesis” predicts
that more productive areas can support more individuals, which would allow the
co-existence of more species with viable populations due to the reduced stochastic
extinctions (Storch et al. 2018); (iii) the “climatic stability hypothesis” states that
seasonality associated with climate may indicate environmental instability, promot-
ing extinction or forcing species to develop broader niches (Evans et al. 2005);
(iv) the “climatic tolerance hypothesis” suggests that colder and drier environments
are physiologically stressful and few species can tolerate these conditions (Evans
et al. 2005). Alternatively, several previous studies have also shown that environ-
mental heterogeneity, such as topographic complexity and forest vertical structure,
are important forces influencing spatial variation in species richness (Gouveia et al.
2014; Rahbek et al. 2019). Therefore, it is reasonable to argue that the above
hypotheses are not mutually exclusive and that they can interact to maintain latitu-
dinal gradients of species richness.
Although most macroecological studies focus exclusively on processes that drive
the number of species in a given area, recent efforts have been directed to investigate
how species composition varies along spatial and environmental gradients (i.e., beta
diversity – differences in species composition; Tuomisto 2010). Approaches that
include differences in species composition between areas can provide additional
information that is difficult to capture using only species richness. Changes in
species composition among sites may be a reflection of community assembly
mechanisms (Nekola and White 1999; Soininen et al. 2007), which are related to:
(i) purely deterministic processes including selection imposed by environmental
heterogeneity (environmental filtering); (ii) purely stochastic processes including
random birth-death events and spatially restricted dispersal; (iii) interaction between
these two processes, resulting in a continuum from purely deterministic to purely
stochastic. Additionally, the relative contribution of deterministic and stochastic
processes has been shown to vary along with space depending on abiotic conditions
and taxonomic groups (Chase and Myers 2011). Thus, patterns of beta diversity and
the importance of space and climate for those patterns can vary across regions
(e.g., hemispheres) due to particular events, such as disturbance, evolutionary
history, climatic, and geographic changes over time (Dunn et al. 2009; Castro-
Insua et al. 2016).
Extant American marsupials radiated mostly in the isolated South American
continent during the Cenozoic and only recently invaded the Central and North
America during the Great American Interchange (Willig and Gannon 1997;
Sánchez-Villagra 2013; Goin et al. 2016). Approximately 130 species of American
marsupials are currently recognized within the orders Didelphimorphia,
Paucituberculata, and Microbiotheria (Astúa et al. 2022). The vast majority of
4 F. O. Cerezer et al.

species are endemic to South America and represented mainly by Didelphidae (Jansa
et al. 2014). With representatives in the three Americas, American marsupials exhibit
a wide geographic distribution, ranging from lowland tropical rainforests to xeric,
arid environments (Gardner 2008). They also show a broad adaptive spectrum to the
environment in which they occur (Charles-Dominique 1983; Bubadué et al. 2019;
Cerezer et al. 2020). However, despite the conspicuous morphological and ecolog-
ical diversity, studies attempting to explain the drivers of species richness and beta
diversity in American marsupials are scarce (e.g., Willig and Gannon 1997; Figuei-
redo and Grelle 2018).
Here spatial patterns of American marsupial species richness were mapped and
the influence of multiple candidate variables related to energy, seasonality, and
environmental heterogeneity were investigated. We also examined the spatial pat-
terns on taxonomic beta diversity (here compositional dissimilarity) and quantified
to what extent the beta diversity is related to geographic (e.g., dispersal limitation)
and climatic (e.g., adaptation) distances between communities in the southern and
northern American hemispheres.

Methods

Species Richness

The species richness of American marsupials (n ¼ 91 species) was calculated based

on the IUCN assessment (www.iucnredlist.org/). Range maps for each species were
projected into cells of 1
by 1
of resolution (~110 km at the Equator) covering all
extent of the Americas. Species richness in each cell was quantified by counting
range maps’ overlaps. A species was considered present in a given cell when the
range map crossed the cell centroid. For subsequent analyzes, only cells that
contained at least one species were considered, totaling 2023 cells.
We select variables widely used in macroecological studies (Currie et al. 2004;
Evans et al. 2005) and which represent surrogates for energy availability, seasonality,
and environmental heterogeneity. The energy input in the environment was mea-
sured through the annual mean temperature (Tmean) because this variable has been
shown as one of the main correlates of species richness (Brown 2014). Additionally,
ecosystem primary production was measured using the Net Primary Productivity
(NPP) index. As variables reflecting the climatic seasonality (i.e., environmental
instability), we used temperature seasonality (ΔT) and precipitation seasonality (ΔP).
Minimum temperature of coldest month (Tmin) and precipitation of driest month
(Pmin) represent an association between cold and dry conditions and were used to
characterize extreme environments conditions. Topographic complexity has been
associated with mammalian species richness (Rahbek et al. 2019) and was calculated
from the difference between maximum and minimum elevation values for each cell.
Finally, as many species of American marsupials are forest dwellers and have
arboreal habits (Voss and Jansa 2009), the forest vertical structure (FVS) was also
quantified through a model of forest canopy height. Except for NPP and FVS, all
Species Richness and Beta Diversity Patterns of American Marsupials 5

variables were extracted for each cell from WorldClim (resolution of 2.5
arc-minutes; Hijmans et al. 2005). NPP was obtained from moderate resolution
imaging spectroradiometer (MODIS) at 1-km pixel resolution (Running et al.
2011). FVS was extracted from the Geoscience Laser Altimeter System at a 1-km
spatial resolution (Simard et al. 2011).
To analyze the direct effects of energy, seasonality, and heterogeneity measures
on species richness, structural equation models (SEM) were used. This approach is a
powerful analytical tool for testing causal relationships in multi-variable datasets and
has already been applied to an array of ecological studies (Fan et al. 2016). Using
SEM, it can be hypothesized that some variables may be influencing species richness
through indirect associations with other variables. For example, the Tmean was
predicted to affect species richness both directly and indirectly through NPP. Sim-
ilarly, NPP was hypothesized to affect species richness directly and indirectly
through FVS. In addition to the direct effects on species richness, indirect paths of
Tmin and Pmin were adjusted for ΔT and ΔP, respectively. The relationships between
variables were quantified using standardized regression coefficients (β), which allow
assessing the relative contribution of each effect. The total effects of a predictor
variable on species richness are equal to the sum of direct and indirect effects
(estimated simply by multiplying the standardized paths involved).

Compositional Dissimilarity

Based on species presence-absence matrix in 1
by 1
cells, taxonomic beta diversity

between pairs of cells was measured following the approach proposed by Baselga
(2010). According to this method, total beta diversity may be associated with both
spatial turnover (species replacement) and nestedness (species loss) components
(Baselga 2010). The total beta diversity was partitioned, which was calculated
here with the Jaccard dissimilarity index (βjac), into two additive components
accounting for species spatial turnover (βjtu) and nestedness-resultant dissimilarities
(βjne). A comprehensive review of methods and equations can be found in Baselga
(2010, 2012). Here, only the spatial turnover component (βjtu) was used to represent
the beta diversity of American marsupials because this component explained the
largest fraction of the total beta diversity (average βjac ¼ 0.858; average βjtu ¼ 0.799;
average βjne ¼ 0.059 – pairwise averages were used here only to show the contri-
bution of the turnover and nestedness components). Similarly, some studies also
showed that the relative importance of spatial turnover increases on broader spatial
scales (Soininen et al. 2018). Since a unique turnover value is quantified for each
combination of cell pairs, a principal coordinate analysis (PCoA) was conducted,
generating ordination scores for each cell. Thus, cells with similar values in the first
axis of PCoA show greater similarity in the turnover, meaning that species compo-
sition is more similar than cells with different values in the PCoA axis. PCoA was
only used to illustrate the compositional dissimilarity across the Americas.
Because of the biogeographic history of the Americas, the taxonomic beta
diversity was also calculated along with cells in the northern (latitude ranging
6 F. O. Cerezer et al.

from 0.5
to 47.5
) and southern (latitude ranging from 0.5
to 48.5
) hemi-
spheres to investigate whether the contribution of geographic and climatic distances
differs between hemispheres. First, a geodesic distance matrix between each pair of
cells was calculated to assess how the turnover component of Jaccard dissimilarity
changes with spatial distance. Second, to evaluate the role of climate in structuring
marsupial communities, a climatic distance matrix was created using Euclidean
distances from 19 variables of the WorldClim (resolution of 2.5 arc-minutes;
Hijmans et al. 2005). These variables were previously standardized at mean ¼
0 and standard deviation ¼ 1.
To investigate the unique and joint contribution of geographic and climatic
distance on the turnover component between southern and northern hemispheres,
we used models of distance decay of similarity and variance partitioning. The
distance decay in the similarity of species composition between hemispheres was
explored fitting negative exponential models through the decay.model function of
the “betapart” package (Baselga et al. 2018). Additionally, the unique and joint
contribution of space and climate were partitioned through negative exponential
models fitted. More specifically, the unique contribution of space was computed
using the r2 explained by the complete model (space and climate together) minus the
r2 explained only by the climate. To compute the unique contribution of climate, the
r2 explained by the complete model (space and climate together) minus the r2
explained only by the space was used.
All analyses were conducted in the R software (R Core Team 2019). Species
richness was calculated using the “raster” (Hijmans 2018) and “sp” (Bivand et al.
2013) packages. Taxonomic beta diversity was calculated using the “betapart”
package (Baselga et al. 2018). Structural equation models (SEM) were implemented
through “lavaan” (Rosseel 2012) package.

Results

Species Richness

American marsupials exhibited a latitudinal gradient in species richness (Fig. 1a),

with the highest species richness occurring near the equator and decreasing toward
more extreme latitudes (Fig. 1b). Species richness peaked along the north and the
central Andes and in portions of the Atlantic forest (Fig. 1a).
The structural equation model (SEM) including the direct and indirect effects of
energy, seasonality, and environmental heterogeneity explained 68% of the observed
variation in species richness (Fig. 2). It was found that ΔT has a stronger direct effect
on species richness than other variables (β ¼ 0.716, P > 0.001). There was a weak
direct effect of the ΔP on species richness (β ¼ 0.140, P > 0.001). Regarding the
influence of climatic extremes, the path involving the effects of Tmin mediated
through ΔT is stronger (β ¼ 0.637 [0.89 x  0.716], P > 0.001) than its direct
effects on species richness (β ¼ 0.433, P > 0.001). In addition, the effects of Pmin on
species richness were not directly significant (β ¼ 0.018, P ¼ 0.313) while the path
Species Richness and Beta Diversity Patterns of American Marsupials 7

Fig. 1 Spatial distribution of marsupial species richness. (a) Observed species richness across the
Americas and (b) relationship between marsupial species richness and latitude. Each point in (b)
represents the marsupial species richness (in 1
by 1
cells) at a given latitude. Dashed lines delimit
the tropical region
8 F. O. Cerezer et al.

Fig. 2 Structural equation model (SEM) showing the paths and coefficients of the relationship
between marsupial species richness and predictor variables. Positive effects are indicated by solid
arrows and negative effects by dashed arrows. Values on arrows represent standardized regression
coefficients (β). NS represents a nonsignificant effect. Abbreviations: Tmean (annual mean temper-
ature); NPP (net primary productivity); FVS (forest vertical structure); Topography (topographic
complexity); Tmin (minimum temperature of the coldest month); ΔT (temperature seasonality); ΔP
(precipitation seasonality); Pmin (precipitation of driest month). The total effect of a predictor
variable on species richness is equal to the sum of direct and indirect effects. The indirect effects
are estimated simply by multiplying the standardized paths involved

indirectly mediated through ΔP was significant but very weak (β ¼ 0.093 [0.671
x  0.140], P > 0.001). The direct effects of Tmean on species richness were stronger
(β ¼ 0.324, P > 0.001) than their indirect effects mediated by NPP (β ¼ 0.104 [0.346
x 0.302], P > 0.001). Similarly, NPP directly influences species richness (β ¼ 0.302,
P > 0.001), but the indirect effects through the FVS were weak (β ¼ 0.029 [0.504 x
0.059], P ¼ 0.001). The FVS was weakly associated with species richness
(β ¼ 0.059, P ¼ 0.001). Interestingly, the topographic complexity was negatively
and weakly associated with the variation in richness of American marsupials
(β ¼ 0.089, P > 0.001).

Compositional Dissimilarity

The taxonomic composition of marsupial species was spatially heterogeneous

throughout the Americas (Fig. 3a). In general, the composition of marsupial species
was quite homogeneous among cells located in the tropical region of South America
(Fig. 3b) and shifted gradually toward the subtropical region of the South American
continent (Fig. 3b). However, species composition changes abruptly between Trop-
ical South America and Central America (Fig. 3b). The latter communities form a
distinct cluster together with North American ones, implying a markedly different
composition than that of South American cells (Fig. 3a).
A comparison between northern and southern hemispheres revealed that the
contribution of geographic and climatic distance on marsupial beta diversity varied
across these regions (Fig. 4). More specifically in the northern hemisphere, the
Species Richness and Beta Diversity Patterns of American Marsupials 9

Fig. 3 Spatial variation in the taxonomic composition of American marsupial. (a) Changes in
taxonomic composition represented by ordering scores (ranging from 0.4 to 0.5). (b) Changes in
taxonomic composition between different regions of the northern and southern hemisphere (SNH
10 F. O. Cerezer et al.

turnover component was more strongly related to geographic distance (r2 ¼ 0.22;
p < 0.05) than climatic distance (r2 ¼ 0; p < 0.05), with an important portion of
variation shared between space and climate (r2 ¼ 0.26; p < 0.05; Fig. 4a). These
results indicate that the decrease in species similarity in the northern hemisphere is
mainly associated with spatial factors (Fig. 5a and b). In the southern hemisphere,
the turnover component was closely associated with both geographic (r2 ¼ 0.10;
p < 0.05) and climatic (r2 ¼ 0.06; p < 0.05) distances (Fig. 4b). Therefore, the
similarity between marsupial communities decreases with geographic and climatic
distance (Fig. 5c and d), although the shared variance explained by space and climate
is more important in the southern hemisphere (r2 ¼ 0.29; p < 0.05; Fig. 4b).

Discussion

Species Richness

There is a latitudinal gradient in marsupial species richness across the America

(Fig. 1a and b), with higher species richness located in the tropical region. Using
structural equation models, temperature seasonality and climatic extremes, as well as
energy variables, contribute significantly to the latitudinal pattern, while topographic
complexity, forest vertical structure, and precipitation seasonality are weak pre-
dictors of spatial variation in species richness.
Seasonality and climatic extremes of temperature (ΔT and Tmin) were the variables
most strongly related to the observed pattern of marsupial species richness (Fig. 2).
These results indicate that there are few marsupial species in areas where the
temperature is seasonally unstable and colder. Similarly, some studies have also
recorded how latitudinal gradients in species richness can be affected by seasonality
and climatic extremes of temperature (Williams and Middleton 2008; Šímová et al.
2011; Stevens et al. 2013; Spasojevic et al. 2014). For example, it has been shown
that species richness is lower in climatically unstable areas (i.e., greater seasonality)
because of the reduced degree of species specialization, linked with resource scarcity
in such areas (Evans et al. 2005; Tello and Stevens 2010). Regarding climatic
extremes, it has been suggested that colder environments support a smaller number
of species because few species can physiologically tolerate stressful conditions
(Currie et al. 2004; Šímová et al. 2011). Once seasonality and climatic extremes of
temperature are collinear (Fig. 2), it is difficult to discern the effects of both
processes on species richness across latitudes. However, most marsupial species

Fig. 3 (continued) ¼ > 23.4
; TROP ¼ 23.4
to 23.4
; SSH ¼ < 23.4
). Ordering scores were
obtained from a principal coordinate analysis (PCoA) using the turnover component of the pairwise
Jaccard dissimilarity. Note that the similarity in species composition declines abruptly toward the
northern hemisphere (indicated by black arrow). Abbreviations: SSH ¼ subtropical region of the
southern hemisphere; TROP ¼ tropical region; SNH ¼ subtropical region of the northern
hemisphere
Species Richness and Beta Diversity Patterns of American Marsupials 11

Fig. 4 Unique and joint

contributions of space and
climate on marsupial
compositional dissimilarity
(turnover component of
Jaccard dissimilarity) across
hemispheres. Effects of
geographic and climatic
distance on compositional
dissimilarity in the (a)
northern and (b) southern
hemispheres

cannot tolerate extreme conditions (Sánchez-Villagra 2013), especially regions with

cold and more seasonal temperatures at higher latitudes.
The current results also showed that Tmean and NPP are positively correlated with
the marsupial species richness (Fig. 2). Climatic determinants, mainly associated
with temperature and productivity, were one of the first explanations proposed for
global patterns in species richness (Rohde 1992) and are still being supported in
empirical studies (Brown 2014). The current results are consistent with the findings
of Figueiredo and Grelle (2018), which also point out the importance of environ-
mental energy for species richness of American marsupials. Although strong rela-
tionships between climate and diversity have been widely recorded (Evans et al.
2005), it has proved challenging to determine the mechanisms behind this phenom-
enon. These challenges are a reflection of different processes in which the climate
can affect diversity, including direct effects on the metabolism of organisms or
12 F. O. Cerezer et al.

Fig. 5 Relationship between similarity in species composition (1 minus the turnover component of
Jaccard dissimilarity) and geographic and climatic distances for all pairwise comparisons of
marsupial communities in the northern and southern hemispheres. The decay of compositional
similarity with (a) geographic distance and (b) climatic distance in the northern hemisphere. The
decay of compositional similarity with (c) geographic distance and (d) climatic distance in the
southern hemisphere

indirect effects operating on plant productivity (Storch 2012). Statistical models that
mechanistically try to disentangle the relative contribution of these processes are
important avenues to be explored in the future (see Cerezer et al. 2021). However,
this chapter is in line with other evidence observed in evolutionarily and ecologically
distinct groups (Currie et al. 2004; Evans et al. 2005) and shows that the energy is a
crucial determinant of species richness at large scales.
Surprisingly, variables associated with environmental heterogeneity had low
predictive power in the marsupial species richness. Topographic complexity was
negatively and weakly associated with species richness (Fig. 2). Indeed, a weak
relationship between species richness and topographic variability has been recorded
in some previous studies (Hawkins et al. 2003b; Diniz-Filho et al. 2004), suggesting
that the explanatory power of topographic complexity may be reduced over a large
geographical extent. Additionally, the forest vertical structure (FVS) measure had a
very weak effect on species richness (Fig. 2). Previous studies showed that species
richness in some continents and clades (primates and amphibians) are better
explained by the forest vertical structure, while for other clades this does not apply
Species Richness and Beta Diversity Patterns of American Marsupials 13

(birds and mammals) (Roll et al. 2015). American marsupials occupy a wide range of
habitat types and encompass diverse locomotor strategies, which may explain this
weak association found between species richness and FVS (in opposition to the
mostly arboreal primates). Therefore, it may be suggested that variables representing
energy and seasonality are more important than variables representing topographic
and habitat heterogeneity to predict broad-scale patterns of marsupial species
richness.

Compositional Dissimilarity

Species composition is broadly similar across communities located in the southern

hemisphere (Fig. 3a), with a slight decrease in the proportion of shared species
between the tropical and subtropical regions of this hemisphere (Fig. 3b). However,
species composition changed markedly between the southern and the northern
hemisphere (Fig. 3a), whereby marsupial communities in the Central and North
America are notably dissimilar compared to those observed in South America
(Fig. 3b).
In the northern hemisphere, geographic distance was the main driver structuring
the marsupial species turnover (Figs. 4a and 5a, b). In contrast, the distance-decay
pattern observed in the northern hemisphere cannot be explained by differences in
climate (Figs. 4a and 5b), suggesting that processes related to dispersal and/or
historical factors are more important for the turnover in such hemisphere. Marsupials
have more restricted physiological/climatic tolerances than placentals (Sánchez-
Villagra 2013), and a small number of species occurs in high temperate latitudes.
Although glaciation events were much more intense in the northern hemisphere and
cannot be ignored (Dunn et al. 2009; Baselga et al. 2012), the connection time
between South and Central-North America via Panama Isthmus during the Pliocene
(Woodburne 2010) should explain the turnover asymmetry between hemispheres.
Recent land connections in the American continents, along with the poor dispersive
capacity of marsupials (Schloss et al. 2012) and the presence of the Andes as a great
geographic barrier for dispersal (Rahbek et al. 2019), may have limited the coloni-
zation of didelphid marsupials from South America to Central and North Americas.
As the Panamanian land bridge was effectively created only recently (~2.5 mya;
Webb 1991), marsupials probably did not have enough time to colonize all environ-
ments, as occurred in South America where they are autochthonous (Voss and Jansa
2009). Thus, it can be argued that marsupial species that arrived in Central and North
America are not necessarily better colonizers than those that remained in South
America. In fact, some species may have had the chance to cross the Andes at
different moments, but difficulties in dispersion and establishment may have been
strongly imposed throughout Central and North America.
The species turnover between sites in the southern hemisphere was explained by a
combination of geographic and climatic distance (Figs. 4b and 5c, d). Factors
associated with space and climate were important in explaining the proportion of
marsupial species shared across communities in South America. Thus, the current
14 F. O. Cerezer et al.

results suggest that species distribution across South America appears to be struc-
tured by an interaction between ecological determinism (e.g., environmental filter-
ing) and stochasticity-driven assembly (e.g., dispersal limitation) (Gravel et al.
2006). Exponential decay of similarity to geographic and climatic distances can
have many explanations (Soininen et al. 2007). An attractive explanation may be
based on the complex biogeographic history of South America, involving the uplift
of the Andes mountain chain (Rahbek et al. 2019) and the frequent episodes of
expansion and contraction of forest and open environments (Giarla and Jansa 2014).
Additionally, extant marsupials are autochthonous to South America (Voss and Jansa
2009) and are highly influenced by the climate (Cerezer et al. 2021) so that the
isolation and species accumulation for a long time inside the continent may have
limited the expansion toward cold latitudes outside the tropics (Sánchez-Villagra
2013; Jansa et al. 2014). Collectively, all of these events may have left footprints in
the patterns of beta diversity and explain why deterministic and stochastic processes
are equally important.

Conclusion

This chapter shows that some specific measures of energy and seasonality are better
predictors of species richness of American marsupials than measures of environ-
mental heterogeneity. Therefore, a higher restriction of marsupial species in the
tropics may be a consequence of an environment with greater energy input and
climatically more stable. Concerning beta diversity, a hemispheric asymmetry was
recorded in the turnover component (compositional dissimilarity), whereby the
contribution of space and climate differs between the southern and northern hemi-
spheres. In summary, the influences of geographic and climatic distances were very
similar in the southern hemisphere. In contrast, geographic distance was the main
agent structuring the marsupial species turnover in the northern hemisphere, empha-
sizing the importance of dispersal limitation in this hemisphere. The authors claim
that the history of marsupials through the Cenozoic, including the historic biogeog-
raphy of land bridges and the appearance of geographic barriers (e.g., the Andes
mountains), was crucial to the American marsupial diversification.

Cross-References

▶ From Bergmann’s to Cope’s Rules: An Overview on the Trait Variation in

American Marsupials
▶ Impact of Habitat Loss and Fragmentation in Didelphid Marsupials of the Atlantic
Forest

Acknowledgments Financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível

Superior - Brasil (CAPES) - Finance Code 001 for Felipe O. Cerezer. Nilton Cáceres has a research
fellowship in Ecology (Process number 313191/2018-2), granted by the Brazilian Agency for
Species Richness and Beta Diversity Patterns of American Marsupials 15

Scientific Research (CNPq) during the chapter elaboration. We are grateful to Thaís Battistella for
their relevant comments on the chapter.

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