Abstract
Understanding how bird species from white sand ecosystems (WSEs) have
managed to inhabit and specialize in an insular environment in the
middle of the Amazon Rainforest is fundamental in order to understand
the evolutionary processes in birds restricted to one type of habitat.
We sought to evaluate the diversification processes of the specialist
bird species of the white sand ecosystems of the Rio Negro basin by
comparing them with the pool of bird species of riparian environments.
Many WSEs may be ancient riverbeds, which may favor current riparian
species to be potential colonizers and settle within the WSEs. For this,
we used an extension of biogeographic evolutionary models to verify
state-dependent speciation and extinction models that specifically
explain the presence of unmeasured factors that can affect the estimated
diversification rates for the states of any observed trait. Thus, it was
possible to evaluate the evolutionary processes that most acted in the
formation of bird communities of WSEs. The results showed that WSEs
specialist bird species have different functional diversity to what was
expected on a random basis and evolutionary models have higher
extinction and speciation rates in WSEs specialist bird communities.
This evidences that source-sink processes maintain WSEs over time, and
that they receive generalist and specialist species from riparian
ecosystems. According to the models analyzed, once the species have the
high degree of adaptation required by an ecosystem with severe
conditions, they cannot colonize other ecosystems. Extinction is an
important process for the dynamics of biodiversity in the Amazon since,
as many species are lost, there is also speciation and high adaptation.
This work is one of the first to use local evolutionary analyses in
Amazonian ecosystems and was effective in showing that extinction is
recurrent, which is a cause for concern due to the severe and rapid
ecological changes currently occurring.
Keywords: Amazon, poor soils, communities, evolutionary process
Introduction
Ecological communities are composed of species that co-occur in a given
geographic space and period, which can change in terms of variation in
composition and richness (Kreft & Jetz, 2010; Schluter & Pennell,
2017). The composition of these communities is determined by temporal
biotic, abiotic and ecological factors (Whittaker et al., 2001; Webb et
al., 2002; Cavender-Bares et al., 2009). However, different groups of
animals and plants respond differently to eco-evolutionary processes,
which creates a puzzle in relation to the history of the formation of
communities, both in the composition of their species, and in the
ecomorphological adaptation of the species and to what extent they are
able manage to disperse . The composition of the species is a reflection
of their ecomorphological adaptation and dispersal capacity, which are
fundamental for the conquest of new habitats (Weeks et al. 2022).
Without abundant sources of evidence or other records showing the past
geographic distribution of a lineage, the difference between in
situ adaptation and colonization is difficult to investigate.
Studying the modifications of the natural history of species is
fundamental in order to understand the evolution of the planet’s
ecosystems (Condamine et al., 2013). Environmental changes and
extinctions are part of history, and shape the future of current
ecosystems and their species. The past can favor the understanding of
what can happen in this current moment of severe and rapid changes in
the environment (Barnosky et al., 2011, Naeem et al., 2012). By
understanding historical changes and their directions, we can assess the
likely consequences in advance. According to ecological modifications,
organisms and their characteristics mediate adaptation and dispersal
potential (Stroud and Losos, 2016). Intense environmental pressures in
certain regions can influence the characteristics of species and
pressure them to similar adaptations, even if these are unrelated.
Studies show that different families of plants that inhabit equally dry
environments in different parts of the Earth, have leaves adapted for
the storeage of water (Vicentini, 2004; Eggli & Nyffeler, 2009). The
richness of birds, mammals and amphibians is similar, and responds to
environmental gradients, but, according to most studies, not to
competition between taxa .
Thus, biodiversity patterns need to be studied at spatial and temporal
scales, taking into account the multiple forms of variation embedded in
the complex concept of biodiversity (Antonelli et al., 2018; Diniz-filho
et al., 2009), and should seek to find the specific mechanisms of
characteristics (traits) and lineages, with the integration of the idea
that ecological and historical biogeographic processes can act strongly
in metacommunities (Vellend, 2010). Studying communities and their
ecological characteristics is essential in order to understand the paths
of diversification and recolonization of species in isolated places,
such as islands of ecosystems surrounded by a matrix or forest fragments
(Claramunt et al., 2012; Cadotte, 2017; Antonelli et al., 2018). Such
transitions between environmentally different areas can allow a species
maintain its characteristics and its ancestral ecological niches, which
can be explained by the conservatism hypothesis .
In the Neotropics, changes in habitat over time show transitions of the
species from ancestral wet and forest habitats to drier environments
(Lanna et al., 2022; Tucker et al., 2017). Studies suggest that
investigation is essential to generalize these patterns, since one
should not just look at a community, but also act in a comparative mode
in relation to the diversification processes and the geographical
variation of the species. One should also verify the potential to
colonize and settle, and compare the species pool of a given region .
Drier environments, with extreme ecological conditions such as high
temperatures and water stress, require more specific adaptations for
species survival, thus restricting permanence and species richness
(Futuyma and Moreno, 1988; Zurita et al., 2017). One example of this
type of environment is the white-sand ecosystem (WSE) that is found in
the Amazon, which occurs in soils with strong water stress and which are
poor in nutrients, and are distributed in isolated patches in the middle
of a terra firme forest matrix . This ecosystem presents endemic
bird species adapted to its specific conditions that are similar to an
island, and whose connections between the patches are probably via
corridors of riparian ecosystems
Bird communities of WSEs show lower diversity and higher dominance of
some species, which is probably due to the limiting pressure of an
environment with low habitat complexity (Capurucho et al., 2020). Thus,
the distribution of bird communities in WSEs seems to be linked to the
adaptation of species to extreme conditions, their dispersal and
colonization capabilities, and may be driven by the size and isolation
of the spots (Borges et al., 2016). WSEs have two types of formations,
i.e., the northern and southern patches of the Amazon, which have
different characteristics and evolutionary histories (Matos et al.,
2016; Cracraft et al., 2020). Bird communities have species turnover
between the patches of WSEs across Amazon
The formation processes of WSEs in the northern Amazon have resulted in
greater heterogeneity of environments on the Guiana Shield (Adeney et
al., 2016; Rossetti et al., 2012), while the WSEs patches of the
southern Amazon feature fewer open areas and appear to be ancient
riverbeds (Ritter et al., 2021). Thus, the connectivity of WSE areas
with riparian environments are more evident in the north of the Amazon
at the present time (Capurucho et al., 2020). Genetic work by WSE bird
specialists corroborates a lower connectivity and recent isolation
between the populations of the north and south of the Negro River .
Herein, we evaluate whether (1) WSEs act as a phylogenetic and
functional filter and (2) whether WSE communities are self-sufficient in
forming and maintaining their diversity or are maintained by a dispersal
of species between WSEs and riparian ecosystems. Lanna et al. (2022)
show that forest habitats are older, favoring dispersal to open areas.
We thus expect more dispersal events from riparian forest ecosystems to
open ones of WSEs. We also expect more speciation events to occur in
riparian forest environments and extinction rates to be higher in WSEs
due to WSE being a restrictive environment.
Knowing the evolutionary
processes that play an important role in the formation of WSE specialist
bird communities and the evolution of bird characteristics will lead to
a better understanding of what happened in the Amazon over time,
especially in two important ecosystems that are currently threatened by
current climate changes.
Methods
We used two lists, one for the white-sand ecosystem (WSE) and another
for the riparian ecosystem. The WSE list has 147 species and 37 families
of birds, which were obtained from the work of Borges et al. (2016 (b)),
for an area located in the Negro River basin. For the riparian
ecosystem, we used the list from the work of Naka et al. (2020) with 439
bird species from 64 families for the Branco River, which is the main
tributary of the Negro River.
Based on the species list for white-sand ecosystems and riparian
environments, specimens of each of the species was measured. At least
three individuals per species were measured in the zoological
collections at INPA, the Goeldi Museum and the UFPE collection. Each
individual was measured three times and, each time, measurements of the
beak (height, length and width), tarsus, total wing length, and length
of secondary feathers were otained, and the Kipp index was calculated.
Via this, we obtained an average of the functional attribute for the
species. All individuals were measured by the same person, always using
a digital caliper and a ruler in millimeters. The functional attributes
that were measured are all linked to the ecological functions of
individuals in the environment (Supplementary Material 1). We
ecologically classified the species using the literature of Billerman et
al. (2022), Borges et al. (2016a, b) and Naka et al. (2020). Species
that are restricted to one type of ecosystem were classified as
specialist species, and species that are present in two or more types of
Amazonian ecosystems were classified generalists. In our database, the
restricted species of riparian ecosystems were represented by “0” (263
species), the restricted ones of white-sand ecosystem environments were
represented by “1” (18 species), and those that use the two types of
ecosystems represented by “01” (126 species).