Southeast Brazil is a neotropical region composed of a mosaic of different tropical habitats and mountain chains, which allowed for the formation of bird-rich communities with distinct ecological niches. Although this region has the potential to harbor a remarkable variety of avian parasites, there is a lack of information about the diversity of malarial parasites. We used molecular approaches to characterize the lineage diversity of Plasmodium and Haemoproteus in bird communities from three different habitats in southeast Brazil based on the prevalence, richness and composition of lineages. We observed an overall prevalence of 35.3%, with a local prevalence ranging from 17.2% to 54.8%. Moreover, no significant association between prevalence and habitat type could be verified (p>0.05). We identified 89 Plasmodium and 22 Haemoproteus lineages, with 86% of them described for the first time here, including an unusual infection of a non-columbiform host by a Haemoproteus (Haemoproteus) parasite. The composition analyses of the parasite communities showed that the lineage composition from Brazilian savannah and tropical dry forest was similar, but it was different from the lineage composition of Atlantic rainforest, reflecting the greater likeness of the former habitats with respect to seasonality and forest density. No significant effects of habitat type on lineage richness were observed based on GLM analyses. We also found that sites whose samples had a greater diversity of bird species showed a greater diversity of parasite lineages, providing evidence that areas with high bird richness also have high parasite richness. Our findings point to the importance of the neotropical region (southeast Brazil) as a major reservoir of new haemosporidian lineages.
How are ecological systems assembled? Here, we aim to contribute to answering this question by harnessing the framework of a novel integrative hypothesis. We shed light on the assembly rules of a multilayer network formed by frugivory and nectarivory interactions between bats and plants in the Neotropics. Our results suggest that, at a large scale, phylogenetic trade-offs separate species into different layers and modules. At an intermediate scale, the modules are also shaped by geographic trade-offs. And at a small scale, the network shifts to a nested structure within its modules, probably as a consequence of resource breadth processes. Finally, once the topology of the network is shaped, morphological traits related to consuming fruits or nectar determine which species are central or peripheral. Our results help understand how different processes contribute to the assemblage of ecological systems at different scales, resulting in a compound topology.
Identifying the mechanisms driving the distribution and diversity of parasitic organisms and characterizing the structure of parasite assemblages are critical to understanding host–parasite evolution, community dynamics, and disease transmission risk. Haemosporidian parasites of the genera Plasmodium and Haemoproteus are a diverse and cosmopolitan group of bird pathogens. Despite their global distribution, the ecological and historical factors shaping the diversity and distribution of these protozoan parasites across avian communities and geographic regions remain unclear. Here we used a region of the mitochondrial cytochrome b gene to characterize the diversity, biogeographical patterns, and phylogenetic relationships of Plasmodium and Haemoproteus infecting Amazonian birds. Specifically, we asked whether, and how, host community similarity and geography (latitude and area of endemism) structure parasite assemblages across 15 avian communities in the Amazon Basin. We identified 265 lineages of haemosporidians recovered from 2661 sampled birds from 330 species. Infection prevalence varied widely among host species, avian communities, areas of endemism, and latitude. Composition analysis demonstrated that both malarial parasites and host communities differed across areas of endemism and as a function of latitude. Thus, areas with similar avian community composition were similar in their parasite communities. Our analyses, within a regional biogeographic context, imply that host switching is the main event promoting diversification in malarial parasites. Although dispersal of haemosporidian parasites was constrained across six areas of endemism, these pathogens are not dispersal‐limited among communities within the same area of endemism. Our findings indicate that the distribution of malarial parasites in Amazonian birds is largely dependent on local ecological conditions and host evolutionary relationships.
One of the unresolved issues in the ecology of parasites is the relationship between host specificity and performance. Previous studies tested this relationship in different systems and obtained all possible outcomes. This led to the proposal of two hypotheses to explain conflicting results: the trade-off and resource breadth hypotheses, which are treated as mutually exclusive in the literature and were corroborated by different studies. In the present study, we used an extensive database on avian malaria from Brazil and combined analyses based on specificity indices and network theory, in order to test which of those hypotheses might best explain our model system. Contrary to our expectations, there was no correlation between specificity and prevalence, which contradicts both hypotheses. In addition, we detected a strong modular structure in our host-parasite network and found that its modules were not composed of geographically close, but of phylogenetically close, host species. Based on our results, we reached the conclusion that trade-off and resource breadth hypotheses are not really mutually exclusive. As a conceptual solution we propose "The Integrative Hypothesis of Parasite Specialization", a novel theoretical model that explains the contradictory results found in our study and reported to date in the literature.
13The architecture of interaction networks has been extensively studied in the past 14 decades, and different topologies have been observed in natural systems. Despite 15 several phenomenological explanations proposed, we still understand little of the 16 mechanisms that generate those topologies. Here we present a mechanistic model based 17on the integrative hypothesis of specialization, which aims at explaining the emergence 18 of topology and specialization in consumer-resource networks. By following three first-19 principles and adjusting five parameters, our model was able to generate synthetic 20 weighted networks that show the main patterns of topology and specialization observed 21 in nature. Our results prove that topology emergence is possible without network-level 22 selection. In our simulations, the intensity of trade-offs in the performance of each 23 consumer species on different resource species is the main factor driving network 24 topology. We predict that interaction networks with low species diversity and low 25 dissimilarity between resources should have a nested topology, although more diverse 26 networks with large dissimilarity should have a compound topology. Additionally, our 27 results highlight scale as a key factor. Our model generates predictions consistent with 28 ecological and evolutionary theories and real-world observations. Therefore, it supports 29 the IHS as a useful conceptual framework to study the architecture of interaction 30 networks. 31
Nestedness and modularity have been recurrently observed in species interaction networks. Some studies argue that those topologies result from selection against unstable networks, and others propose that they likely emerge from processes driving the interactions between pairs of species. Here we present a model that simulates the evolution of consumer species using resource species following simple rules derived from the integrative hypothesis of specialization (IHS). Without any selection on stability, our model reproduced all commonly observed network topologies. Our simulations demonstrate that resource heterogeneity drives network topology. On the one hand, systems containing only homogeneous resources form generalized nested networks, in which generalist consumers have higher performance on each resource than specialists. On the other hand, heterogeneous systems tend to have a compound topology: modular with internally nested modules, in which generalists that divide their interactions between modules have low performance. Our results demonstrate that all real‐world topologies likely emerge through processes driving interactions between pairs of species. Additionally, our simulations suggest that networks containing similar species differ from heterogeneous networks and that modules may not present the topology of entire networks.
Is there a prevalent pattern among interaction networks: nestedness or modularity? Must consumers always trade-off generalism for average performance in resource exploitation? These two questions have been addressed in various systems, with contradictory results. A recent integrative hypothesis combines both questions within a common theoretical framework, proposing that ecological specialization is structured by different prevailing processes in smaller and larger network units. This should produce both a compound interaction network, formed by internally nested modules, and a scale-dependence on the relationship between consumer performance and generalism. Here, we confirm both predictions in a large dataset on host-parasite interactions. We show that modules indeed constrain nestedness at the whole network level, and that the relationship between parasite generalism and performance on their hosts changed from negative at large to positive at small scales. Our results shed light on both debates, and provide some clues to their integration and solution.
Plant secondary chemistry is known to be an important driver of plant–insect community structure across ecological scales. Recently, the concept of phytochemical diversity (PD) has been introduced to help describe variation in plant secondary chemistry and explain how this variation affects community structure. Previous studies show that PD among individuals and species results in phytochemical mosaics, known as the phytochemical landscape. However, plant traits can vary at finer scales, such as within individuals, and even a single host plant may be perceived as an entire phytochemical landscape by an interacting insect. Using the neotropical shrub Piper amalago, we tested and compared how herbivory, caterpillar biodiversity and plant–herbivore network structure are affected by the compositional (number and concentration of compounds) and structural (diversity of distinct chemical structures) dimensions of PD. We analysed variation among individual plants and among‐plant height strata within individual plants. This allowed us to decompose PD within and among plant individuals and analyse how variation at both scales affects the plant–herbivore network. We found that both within and among plants greater structural diversity decreased herbivore feeding damage. Furthermore, each dimension of PD has different effects on herbivore biodiversity and network structure depending on the scale of biological organization. Within plants, the compositional dimension, specifically low concentrations of compounds tentatively identified as Piper amides, increased herbivore biodiversity. This dimension also increased the capacity of strata within plants to mediate ecological cascades through direct and indirect effects on herbivore abundance in the plant–herbivore network. In contrast, a greater structural diversity among plants decreased herbivore biodiversity and the capacity of plants to affect all other herbivores and plants directly and indirectly in the network. Synthesis. Based on our results we expand the concept of the phytochemical landscape to multiple scales of biological organization and provide evidence that PD may be maintained by how its multiple dimensions have distinct roles across scales of biological organization.
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