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).