Imprints of indirect interactions on a resource-mediated ant-plant network across different levels of network organization.

Indirect interactions are pivotal in the evolution of interacting species and the assembly of populations and communities. Nevertheless, despite recently being investigated in plant-animal mutualism at the community level, indirect interactions have not been studied in resource-mediated mutualisms involving plant individuals that share different animal species as partners within a population (i.e., individual-based networks). Here, we analyzed an individual-based ant-plant network to evaluate how resource properties affect indirect interaction patterns and how changes in indirect links leave imprints in the network across multiple levels of network organization. Using complementary analytical approaches, we described the patterns of indirect interactions at the micro-, meso-, and macro-scale. We predicted that plants offering intermediate levels of nectar quantity and quality interact with more diverse ant assemblages. The increased number of ant species would cause a higher potential for indirect interactions in all scales evaluated. We found that nectar properties modified patterns of indirect interactions of plant individuals that share mutualistic partners, leaving imprints across different network scales. To our knowledge, this is the first study tracking indirect interactions in multiple scales within an individual-based network. We show that functional traits of interacting species, such as nectar properties, may lead to changes in indirect interactions, which could be tracked across different levels of the network organization evaluated.

To rewire or not to rewire: To what extent rewiring to surviving partners can avoid extinction?

Research Highlight: Leimberger, K.G., Hadley, A.S., & Betts, M.G. (2023). Plant-hummingbird pollination networks exhibit minimal rewiring after experimental removal of a locally abundant plant species. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13935. In this paper, Leimberger, Hadley and Betts (2023) explore the effects of removing a locally abundant plant species on plant-hummingbird pollination networks. They experimentally prevented access of hummingbirds to flowers of Heliconia tortuosa and assessed subsequent changes in the interactions between plants and hummingbirds. Their main hypothesis postulated that the loss of a highly connected species would lead to interaction rewiring and niche expansions by hummingbirds, decreasing individual, species and network specialization. However, they found that the overall structure of the plant-hummingbird networks remains mostly unaltered, with limited rewiring and minimal changes in specialization. The main contributions of this study can be summarized as (i) it adds to a limited number of manipulative studies on the capacity of species to rewire their interactions following the loss of partners, and importantly, it is the first study from the tropics and with vertebrate pollinators, for which experimental studies at appropriate scales is intrinsically more challenging; and (ii) innovates by evaluating change in specialization for the individual level, carried out through pollen sampling on the body of hummingbirds. The limited change in species interactions highlights that network stability through interaction rewiring may have been overestimated in previous studies, calling for further manipulative studies in the field. At the same time, it also indicated that even the loss of a highly abundant plant species has an overall small effect on network structure. Thus, this study contributes timely findings regarding the capacity of ecological communities to respond to species extinctions.

Fission-fusion dynamics in the social networks of a North American pitviper.

Many animal species exist in fission-fusion societies, where the size and composition of conspecific groups change spatially and temporally. To help investigate such phenomena, social network analysis (SNA) has emerged as a powerful conceptual and analytical framework for assessing patterns of interconnectedness and quantifying group-level interactions. We leveraged behavioral observations via radiotelemetry and genotypic data from a long-term (>10 years) study on the pitviper Crotalus atrox (western diamondback rattlesnake) and used SNA to quantify the first robust demonstration of social network structures for any free-living snake. Group-level interactions among adults in this population resulted in structurally modular networks (i.e., distinct clusters of interacting individuals) for fidelis use of communal winter dens (denning network), mating behaviors (pairing network), and offspring production (parentage network). Although the structure of each network was similar, the size and composition of groups varied among them. Specifically, adults associated with moderately sized social groups at winter dens but often engaged in reproductive behaviors-both at and away from dens-with different and fewer partners. Additionally, modules formed by individuals in the pairing network were frequently different from those in the parentage network, likely due to multiple mating, long-term sperm storage by females, and resultant multiple paternity. Further evidence for fission-fusion dynamics exhibited by this population-interactions were rare when snakes were dispersing to and traversing their spring-summer home ranges (to which individuals show high fidelity), despite ample opportunities to associate with numerous conspecifics that had highly overlapping ranges. Taken together, we show that long-term datasets incorporating SNA with spatial and genetic information provide robust and unique insights to understanding the social structure of cryptic taxa that are understudied.

Horizontal Transposon Transfer and Their Ecological Drivers: The Case of Flower-breeding Drosophila.

Understanding the mechanisms that shape the architecture, diversity, and adaptations of genomes and their ecological and genetic interfaces is of utmost importance to understand biological evolution. Transposable elements (TEs) play an important role in genome evolution, due to their ability to transpose within and between genomes, providing sites of nonallelic recombination. Here we investigate patterns and processes of TE-driven genome evolution associated with niche diversification. Specifically, we compared TE content, TE landscapes, and frequency of horizontal transposon transfers (HTTs) across genomes of flower-breeding Drosophila (FBD) with different levels of specialization on flowers. Further, we investigated whether niche breadth and ecological and geographical overlaps are associated with a potential for HTT rates. Landscape analysis evidenced a general phylogenetic pattern, in which species of the D. bromeliae group presented L-shaped curves, indicating recent transposition bursts, whereas D. lutzii showed a bimodal pattern. The great frequency of highly similar sequences recovered for all FBD suggests that these species probably experienced similar ecological pressures and evolutionary histories that contributed to the diversification of their mobilomes. Likewise, the richness of TEs superfamilies also appears to be associated with ecological traits. Furthermore, the two more widespread species, the specialist D. incompta and the generalist D. lutzii, presented the highest frequency of HTT events. Our analyses also revealed that HTT opportunities are positively influenced by abiotic niche overlap but are not associated with phylogenetic relationships or niche breadth. This suggests the existence of intermediate vectors promoting HTTs between species that do not necessarily present overlapping biotic niches.

Mechanisms underlying interaction frequencies and robustness in a novel seed dispersal network: lessons for restoration.

As human-caused extinctions and invasions accumulate across the planet, understanding the processes governing ecological functions mediated by species interactions, and anticipating the effect of species loss on such functions become increasingly urgent. In seed dispersal networks, the mechanisms that influence interaction frequencies may also influence the capacity of a species to switch to alternative partners (rewiring), influencing network robustness. Studying seed dispersal interactions in novel ecosystems on O'ahu island, Hawai'i, we test whether the same mechanisms defining interaction frequencies can regulate rewiring and increase network robustness to simulated species extinctions. We found that spatial and temporal overlaps were the primary mechanisms underlying interaction frequencies, and the loss of the more connected species affected networks to a greater extent. Further, rewiring increased network robustness, and morphological matching and spatial and temporal overlaps between partners were more influential on network robustness than species abundances. We argue that to achieve self-sustaining ecosystems, restoration initiatives can consider optimal morphological matching and spatial and temporal overlaps between consumers and resources to maximize chances of native plant dispersal. Specifically, restoration initiatives may benefit from replacing invasive species with native species possessing characteristics that promote frequent interactions and increase the probability of rewiring (such as long fruiting periods, small seeds and broad distributions).

Plant height and spatial context influence individual connectivity and specialization on seed dispersers in a tree population.

While network analyses have stimulated a renewed interest in understanding patterns and drivers of specialization within communities, few studies have explored specialization within populations. Thus, in plant populations, causes and consequences of individual variation in their interactions with mutualistic animals remain poorly understood. Studying a Brazilian pepper (Schinus terebinthifolia) population, we measured the extent of individual variation in interactions with seed dispersers and tested whether connectivity (number of seed dispersers) and specialization (exclusiveness of partners) are associated with phenotypic and phenological traits of individuals and their spatial context. We found that: (i) individuals varied broadly in their connectivity and specialization on seed dispersers; (ii) phenotypic traits and spatial context matter more than fruiting duration in determining how many and how exclusive are seed dispersers of an individual; (iii) the individual-based network was nested and indicated that the less connected individuals were shorter, occurred in neighborhoods with fewer fruits, and tended to interact with a subset of the partners of more generalist individuals which, in turn, were taller and inserted in higher fruit density neighborhoods; (iv) modularity indicated the existence of subsets of individuals that interacted disproportionately with distinct groups of partners, which may occur due to differences in bird habitat use across the landscape. Our study underlines a remarkable interindividual variation that is overlooked when interactions are compiled to describe species-level interactions. Traits and spatial contexts that define variation among individuals may have important implications not only for fitness but also for sampling and description of interactions at species level.

Structural resilience and high interaction dissimilarity of plant-pollinator interaction networks in fire-prone grasslands.

Fire is a frequent disturbance in most grasslands around the world, being key for the structure and dynamics of the biodiversity in such ecosystems. While grassland species may be resilient, little is known on how plant-pollinator networks reassemble after fire. Here, we investigate the structure and dynamics of plant-pollinator networks and the variation in species roles over a 2-year post-fire chronosequence on grassland communities in Southern Brazil. We found that both network specialization and modularity were similar over the chronosequence of time-since-fire, but in freshly burnt areas, there were more species acting as network hubs. Species roles exhibited high variation, with plant and pollinator species shifting roles along the post-disturbance chronosequence. Interaction dissimilarity was remarkably high in networks irrespective of times-since-fire. Interaction dissimilarity was associated more with rewiring than with species turnover, indicating that grassland plant and pollinator species are highly capable of switching partners. Time-since-fire had little influence on network structure but influenced the identity and diversity of pollinators playing key roles in the networks. These findings suggest that pollination networks in naturally fire-prone ecosystems are highly dynamic and resilient to fire with both plants and pollinators being highly capable of adjusting their interactions and network structure after disturbance.

ATLANTIC POLLINATION: a data set of flowers and interaction with nectar-feeding vertebrates from the Atlantic Forest.

Flowering plant species and their nectar-feeding vertebrates exemplify some of the most remarkable biotic interactions in the Neotropics. In the Brazilian Atlantic Forest, several species of birds (especially hummingbirds), bats, and non-flying mammals, as well as one lizard feed on nectar, often act as pollinators and contribute to seed output of flowering plants. We present a dataset containing information on flowering plants visited by nectar-feeding vertebrates and sampled at 166 localities in the Brazilian Atlantic Forest. This dataset provides information on 1902 unique interactions among 515 species of flowering plants and 129 species of potential vertebrate pollinators and the patterns of species diversity across latitudes. All plant-vertebrate interactions compiled were recorded through direct observations of visits, and no inferences of pollinators based on floral syndromes were included. We also provide information on the most common plant traits used to understand the interactions between flowers and nectar-feeding vertebrates: plant growth form, corolla length, rate of nectar production per hour in bagged flowers, nectar concentration, flower color and shape, time of anthesis, presence or absence of perceptible fragrance by human, and flowering phenology as well as the plant's threat status by International Union for Conservation of Nature (IUCN) classification. For the vertebrates, status of threat by IUCN classification, body mass, bill or rostrum size are provided. Information on the frequency of visits and pollen deposition on the vertebrate's body is provided from the original source when available. The highest number of unique interactions is recorded for birds (1771) followed by bats (110). For plants, Bromeliaceae contains the highest number of unique interactions (606), followed by Fabaceae (242) and Gesneriaceae (104). It is evident that there was geographical bias of the studies throughout the southeast of the Brazilian Atlantic Forest and that most effort was directed to flower-hummingbird interactions. However, it reflects a worldwide tendency of more plants interacting with birds compared with other vertebrate species. The lack of similar protocols among studies to collect basic data limits the comparisons among areas and generalizations. Nevertheless, this dataset represents a notable effort to organize and highlight the importance of vertebrate pollinators in this hotspot of biodiversity on Earth and represents the data currently available. No copyright or proprietary restrictions are associated with the use of this data set. Please cite this data paper when the data are used in publications or scientific events.

Modularity and specialization in bat-fly interaction networks are remarkably consistent across patches within urbanized landscapes and spatial scales.

Patterns of specialization and the structure of interactions between bats and ectoparasitic flies have been studied mostly on non-urban environments and at local scales. Thus, how anthropogenic disturbances influence species interactions and network structure in this system remain poorly understood. Here, we investigated patterns of interaction between Phyllostomidae bats and ectoparasitic Streblidae flies, and variations in network specialization and structure across Cerrado patches within urbanized landscapes in Brazil and between local and regional scales. We found high similarity in the richness and composition of bat and fly species across communities, associated with low turnover of interactions between networks. The high specialization of bat-streblid interactions resulted in little connected and modular networks, with the emergence of modules containing subsets of species that interact exclusively or primarily with each other. Such similarities in species and interaction composition and network structure across communities and scales suggest that bat-fly interactions within Cerrado patches are little affected by the degree of human modification in the surrounding matrix. This remarkable consistency is likely promoted by specific behaviors, the tolerance of Phyllostomidae bats to surrounding urbanized landscapes as well as by the specificity of the streblid-bat interactions shaped over evolutionary time.

Ecological correlates of species' roles in highly invaded seed dispersal networks.

Ecosystems with a mix of native and introduced species are increasing globally as extinction and introduction rates rise, resulting in novel species interactions. While species interactions are highly vulnerable to disturbance, little is known about the roles that introduced species play in novel interaction networks and what processes underlie such roles. Studying one of the most extreme cases of human-modified ecosystems, the island of O'ahu, Hawaii, we show that introduced species there shape the structure of seed dispersal networks to a greater extent than native species. Although both neutral and niche-based processes influenced network structure, niche-based processes played a larger role, despite theory predicting neutral processes to be predominantly important for islands. In fact, ecological correlates of species' roles (morphology, behavior, abundance) were largely similar to those in native-dominated networks. However, the most important ecological correlates varied with spatial scale and trophic level, highlighting the importance of examining these factors separately to unravel processes determining species contributions to network structure. Although introduced species integrate into interaction networks more deeply than previously thought, by examining the mechanistic basis of species' roles we can use traits to identify species that can be removed from (or added to) a system to improve crucial ecosystem functions, such as seed dispersal.

Drivers of the structure of plant-hummingbird interaction networks at multiple temporal scales.

In semi-arid environments, the marked contrast in temperature and precipitation over the year strongly shapes ecological communities. The composition of species and their ecological interactions within a community may vary greatly over time. Although intra-annual variations are often studied, empirical information on how plant-bird relationships are structured within and among years, and how their drivers may change over time are still limited. In this study, we analyzed the temporal dynamics of the structure of plant-hummingbird interaction networks by evaluating changes in species richness, diversity of interactions, modularity, network specialization, nestedness, and ß-diversity of interactions throughout four years in a Mexican xeric shrubland landscape. We also evaluated if the relative importance of abundance, phenology, morphology, and nectar sugar content consistently explains the frequency of pairwise interactions between plants and hummingbirds across different years. We found that species richness, diversity of interactions, nestedness, and network specialization did vary within and among years. We also observed that the ß-diversity of interactions was high among years and was mostly associated with species turnover (i.e., changes in species composition), with a minor contribution of interaction rewiring (i.e., shifting partner species at different times). Finally, the temporal co-occurrence of hummingbird and plant species among months was the best predictor of the frequency of pairwise interactions, and this pattern was consistent within and among years. Our study underscores the importance of considering the temporal scale to understand how changes in species phenologies, and the resulting temporal co-occurrences influence the structure of interaction networks.

Drivers of bat roles in Neotropical seed dispersal networks: abundance is more important than functional traits.

While functional traits can facilitate or constrain interactions between pair of species in ecological communities, relative abundances regulate the probabilities of encounter among individuals. However, the relative importance of traits and relative abundances for the role species play in seed dispersion networks remains poorly explored. Here, we analyzed 20 Neotropical seed dispersal networks distributed from Mexico to southeastern Brazil to evaluate how relative abundance and functional traits influence bat species' roles in seed dispersal networks. We tested how bat relative abundance and traits relate to species contribution to between-module (c metric) and within-module connectivity (z metric) and their position and potential to mediate indirect effects between species (betweenness centrality). Our results indicate that relative abundance is the main determinant of the role bats play in the networks, while traits such as aspect ratio show modest yet statistically significant importance in predicting specific roles. Moreover, all seed dispersal networks presented two or three superabundant obligatory frugivore species that interacted with a high number of plants. The modest influence of the functional traits on species' roles is likely related to the low variation of morphological traits related to foraging ecology, which reduces the chances of morphological mismatching between consumers and resources in the system. In this scenario, abundant bats have higher chances of encountering resources and being capable of consuming them which leads such species to play critical roles in the community by acting as module hubs and network connectors.

Ecological mechanisms explaining interactions within plant-hummingbird networks: morphological matching increases towards lower latitudes.

Interactions between species are influenced by different ecological mechanisms, such as morphological matching, phenological overlap and species abundances. How these mechanisms explain interaction frequencies across environmental gradients remains poorly understood. Consequently, we also know little about the mechanisms that drive the geographical patterns in network structure, such as complementary specialization and modularity. Here, we use data on morphologies, phenologies and abundances to explain interaction frequencies between hummingbirds and plants at a large geographical scale. For 24 quantitative networks sampled throughout the Americas, we found that the tendency of species to interact with morphologically matching partners contributed to specialized and modular network structures. Morphological matching best explained interaction frequencies in networks found closer to the equator and in areas with low-temperature seasonality. When comparing the three ecological mechanisms within networks, we found that both morphological matching and phenological overlap generally outperformed abundances in the explanation of interaction frequencies. Together, these findings provide insights into the ecological mechanisms that underlie geographical patterns in resource specialization. Notably, our results highlight morphological constraints on interactions as a potential explanation for increasing resource specialization towards lower latitudes.

Structure, spatial dynamics, and stability of novel seed dispersal mutualistic networks in Hawai'i.

Increasing rates of human-caused species invasions and extinctions may reshape communities and modify the structure, dynamics, and stability of species interactions. To investigate how such changes affect communities, we performed multiscale analyses of seed dispersal networks on O'ahu, Hawai'i. Networks consisted exclusively of novel interactions, were largely dominated by introduced species, and exhibited specialized and modular structure at local and regional scales, despite high interaction dissimilarity across communities. Furthermore, the structure and stability of the novel networks were similar to native-dominated communities worldwide. Our findings suggest that shared evolutionary history is not a necessary process for the emergence of complex network structure, and interaction patterns may be highly conserved, regardless of species identity and environment. Introduced species can quickly become well integrated into novel networks, making restoration of native ecosystems more challenging than previously thought.

The influence of spatial sampling scales on ant-plant interaction network architecture.

Despite great interest in metrics to quantify the structure of ecological networks, the effects of sampling and scale remain poorly understood. In fact, one of the most challenging issues in ecology is how to define suitable scales (i.e., temporal or spatial) to accurately describe and understand ecological systems. Here, we sampled a series of ant-plant interaction networks in the southern Brazilian Amazon rainforest in order to determine whether the spatial sampling scale, from local to regional, affects our understanding of the structure of these networks. To this end, we recorded ant-plant interactions in adjacent 25 × 30 m subplots (local sampling scale) nested within twelve 250 × 30 m plots (regional sampling scale). Moreover, we combined adjacent or random subplots and plots in order to increase the spatial sampling scales at the local and regional levels. We then calculated commonly used binary and quantitative network-level metrics for both sampling scales (i.e., number of species and interactions, nestedness, specialization and modularity), all of which encompass a wide array of structural patterns in interaction networks. We observed increasing species and interactions across sampling scales, and while most network descriptors remained relatively constant at the local level, there was more variation at the regional scale. Among all metrics, specialization was most constant across different spatial sampling scales. Furthermore, we observed that adjacent assembly did not generate more variation in network descriptor values compared to random assembly. This finding indicates that the spatially aggregated distribution of species/individuals and abiotic conditions does not affect the organization of these interacting assemblages. Our results have a direct impact on our empirical and theoretical understanding of the ecological dynamics of species interactions by demonstrating that small spatial sampling scales should suffice to record some patterns commonly found in ant-plant interaction networks in a highly diverse tropical rainforest.

Diet overlap and spatial segregation between two neotropical marsupials revealed by multiple analytical approaches.

Species co-existence depends on how organisms utilize their environment and resources. When two sympatric species are similar in some ecological requirements, their coexistence may arise from differences in resource use over time and/or space. Interactions among coexisting marsupials remain poorly understood, especially in the Neotropics. Here we combine spatial niche measurements, individual-resource networks, and isotopic niche approaches, to investigate the ecological strategies used by the Neotropical marsupials Didelphis aurita and Metachirus nudicaudatus to co-occur in an area of Serra do Mar State Park (southeast of Brazil). Both individual-resource networks and isotopic niche approaches indicate similar patterns of omnivory for both species. Isotopic analysis showed the species' trophic niche to be similar, with 52% of overlap, and no differences between proportional contributions of each resource to their diets. Moreover, individual-resource network analysis found no evidence of diet nestedness or segregation. The trophic niche overlap observed was associated with spatial segregation between species. Despite using the same area over the year, D. aurita and M. nudicaudatus exhibited spatial segregation among seasons. These results illustrate that the detection of spatial segregation is scale-dependent and must be carefully considered. In conclusion, our findings provide a new perspective on the ecology of these two Neotropical marsupials by illustrating how the association of distinct but complementary methods can be applied to reach a more complete understanding of resource partitioning and species coexistence.

The potential indirect effects among plants via shared hummingbird pollinators are structured by phenotypic similarity.

Plant species within communities may overlap in pollinators' use and influence visitation patterns of shared pollinators, potentially engaging in indirect interactions (e.g., facilitation or competition). While several studies have explored the mechanisms regulating insect-pollination networks, there is a lack of studies on bird-pollination systems, particularly in species-rich tropical areas. Here, we evaluated if phenotypic similarity, resource availability (floral abundance), evolutionary relatedness and flowering phenology affect the potential for indirect effects via shared pollinators in hummingbird-pollinated plant species within four communities in the Brazilian Atlantic forest. Among the evaluated factors, phenotypic similarity (corolla length and anther height) was the most important variable, while resource availability (floral abundance) had a secondary importance. On the other hand, evolutionary relatedness and flowering phenology were less important, which altogether highlights the relevance of convergent evolution and that the contribution of a plant to the diet of the pollinators of another plant is independent of the level of temporal overlap in flowering in this tropical system. Interestingly, our findings contrast with results from multiple insect-pollinated plant communities, mostly from temperate regions, in which floral abundance was the most important driver, followed by evolutionary relatedness and phenotypic similarity. We propose that these contrasting results are due to high level of specialization inherent to tropical hummingbird-pollination systems. Moreover, our results demonstrated that factors defining linkage rules of plant-hummingbird networks also determinate plant-plant potential indirect effects. Future studies are needed to test if these findings can be generalized to other highly specialized systems. Overall, our results have important implications for the understanding of ecological processes due resource sharing in mutualistic systems.

High proportion of smaller ranged hummingbird species coincides with ecological specialization across the Americas.

Ecological communities that experience stable climate conditions have been speculated to preserve more specialized interspecific associations and have higher proportions of smaller ranged species (SRS). Thus, areas with disproportionally large numbers of SRS are expected to coincide geographically with a high degree of community-level ecological specialization, but this suggestion remains poorly supported with empirical evidence. Here, we analysed data for hummingbird resource specialization, range size, contemporary climate, and Late Quaternary climate stability for 46 hummingbird-plant mutualistic networks distributed across the Americas, representing 130 hummingbird species (ca 40% of all hummingbird species). We demonstrate a positive relationship between the proportion of SRS of hummingbirds and community-level specialization, i.e. the division of the floral niche among coexisting hummingbird species. This relationship remained strong even when accounting for climate, furthermore, the effect of SRS on specialization was far stronger than the effect of specialization on SRS, suggesting that climate largely influences specialization through species' range-size dynamics. Irrespective of the exact mechanism involved, our results indicate that communities consisting of higher proportions of SRS may be vulnerable to disturbance not only because of their small geographical ranges, but also because of their high degree of specialization.