The human touch: a meta-analysis of anthropogenic effects on plant-pollinator interaction networks.

Background: Anthropogenic activities significantly impact natural ecosystems, leading to alterations in plant and pollinator diversity and abundance. These changes often result in shifts within interacting communities, potentially reshaping the structure of plant-pollinator interaction networks. Given the escalating human footprint on habitats, evaluating the response of these networks to anthropization is critical for devising effective conservation and management strategies. Methods: We conducted a comprehensive review of the plant-pollinator network literature to assess the impact of anthropization on network structure. We assessed network metrics such as nestedness measure based on overlap and decreasing fills (NODF), network specialization (H2'), connectance (C), and modularity (Q) to understand structural changes. Employing a meta-analytical approach, we examined how anthropization activities, such as deforestation, urbanization, habitat fragmentation, agriculture, intentional fires and livestock farming, affect both plant and pollinator richness. Results: We generated a dataset for various metrics of network structure and 36 effect sizes for the meta-analysis, from 38 articles published between 2010 and 2023. Studies assessing the impact of agriculture and fragmentation were well-represented, comprising 68.4% of all studies, with networks involving interacting insects being the most studied taxa. Agriculture and fragmentation reduce nestedness and increase specialization in plant-pollinator networks, while modularity and connectance are mostly not affected. Although our meta-analysis suggests that anthropization decreases richness for both plants and pollinators, there was substantial heterogeneity in this regard among the evaluated studies. The meta-regression analyses helped us determine that the habitat fragment size where the studies were conducted was the primary variable contributing to such heterogeneity. Conclusions: The analysis of human impacts on plant-pollinator networks showed varied effects worldwide. Responses differed among network metrics, signaling nuanced impacts on structure. Activities like agriculture and fragmentation significantly changed ecosystems, reducing species richness in both pollinators and plants, highlighting network vulnerability. Regional differences stressed the need for tailored conservation. Despite insights, more research is crucial for a complete understanding of these ecological relationships.

Impacts of land use change on native plant-butterfly interaction networks from central Mexico.

Background: Land use change is a key catalyst of global biodiversity loss and ecosystem degradation. Deforestation and conversion of natural habitats to agricultural or urban areas can profoundly disrupt plant-flower visitor interactions by altering their abundances and distribution. Yet, specific studies analyzing the effects of land use change on the structure of networks of the interactions between particular groups of flower visitors and their plants are still scarce. Here, we aimed to analyze how converting native habitats affects the species composition of butterfly communities and their plants, and whether this, in turn, leads to changes in the structure of interaction networks in the modified habitats. Methods: We performed bi-monthly censuses for a year to record plant-butterfly interactions and assess species diversity across three habitat types, reflecting a land-use change gradient. From original native juniper forest to urban and agricultural zones in central Mexico, one site per land use type was surveyed. Interactions were summarized in matrices on which we calculated network descriptors: connectance, nestedness and modularity. Results: We found highest butterfly diversity in native forest, with the most unique species (i.e., species not shared with the other two sites). Agricultural and urban sites had similar diversity, yet the urban site featured more unique species. The plant species richness was highest in the urban site, and the native forest site had the lowest plant species richness, with most of the plants being unique to this site. Butterfly and plant compositions contrasted most between native forest and modified sites. Network analysis showed differences between sites in the mean number of links and interactions. The urban network surpassed agriculture and native forest networks in links, while the native forest network had more interactions than the agriculture and urban networks. Native plants had more interactions than alien species. All networks exhibited low connectance and significant nestedness and modularity, with the urban network featuring the most modules (i.e., 10 modules). Conclusions: Converting native habitats to urban or agricultural areas reshapes species composition, diversity and interaction network structure for butterfly communities and plants. The urban network showed more links and modules, suggesting intricate urban ecosystems due to diverse species, enhanced resources, and ecological niches encouraging interactions and coexistence. These findings emphasize the impacts of land use change on plant-butterfly interactions and the structure of their interaction networks.

The influence of floral traits on specialization and modularity of plant-pollinator networks in a biodiversity hotspot in the Peruvian Andes.

BACKGROUND AND AIMS: Modularity is a ubiquitous and important structural property of ecological networks which describes the relative strengths of sets of interacting species and gives insights into the dynamics of ecological communities. However, this has rarely been studied in species-rich, tropical plant-pollinator networks. Working in a biodiversity hotspot in the Peruvian Andes we assessed the structure of quantitative plant-pollinator networks in nine valleys, quantifying modularity among networks, defining the topological roles of species and the influence of floral traits on specialization. METHODS: A total of 90 transects were surveyed for plants and pollinators at different altitudes and across different life zones. Quantitative modularity (QuanBiMo) was used to detect modularity and six indices were used to quantify specialization. KEY RESULTS: All networks were highly structured, moderately specialized and significantly modular regardless of size. The strongest hubs were Baccharis plants, Apis mellifera, Bombus funebris and Diptera spp., which were the most ubiquitous and abundant species with the longest phenologies. Species strength showed a strong association with the modular structure of plant-pollinator networks. Hubs and connectors were the most centralized participants in the networks and were ranked highest (high generalization) when quantifying specialization with most indices. However, complementary specialization d' quantified hubs and connectors as moderately specialized. Specialization and topological roles of species were remarkably constant across some sites, but highly variable in others. Networks were dominated by ecologically and functionally generalist plant species with open access flowers which are closely related taxonomically with similar morphology and rewards. Plants associated with hummingbirds had the highest level of complementary specialization and exclusivity in modules (functional specialists) and the longest corollas. CONCLUSIONS: We have demonstrated that the topology of networks in this tropical montane environment was non-random and highly organized. Our findings underline that specialization indices convey different concepts of specialization and hence quantify different aspects, and that measuring specialization requires careful consideration of what defines a specialist.

Beyond neutral and forbidden links: morphological matches and the assembly of mutualistic hawkmoth-plant networks.

A major challenge in evolutionary ecology is to understand how co-evolutionary processes shape patterns of interactions between species at community level. Pollination of flowers with long corolla tubes by long-tongued hawkmoths has been invoked as a showcase model of co-evolution. Recently, optimal foraging models have predicted that there might be a close association between mouthparts' length and the corolla depth of the visited flowers, thus favouring trait convergence and specialization at community level. Here, we assessed whether hawkmoths more frequently pollinate plants with floral tube lengths similar to their proboscis lengths (morphological match hypothesis) against abundance-based processes (neutral hypothesis) and ecological trait mismatches constraints (forbidden links hypothesis), and how these processes structure hawkmoth-plant mutualistic networks from five communities in four biogeographical regions of South America. We found convergence in morphological traits across the five communities and that the distribution of morphological differences between hawkmoths and plants is consistent with expectations under the morphological match hypothesis in three of the five communities. In the two remaining communities, which are ecotones between two distinct biogeographical areas, interactions are better predicted by the neutral hypothesis. Our findings are consistent with the idea that diffuse co-evolution drives the evolution of extremely long proboscises and flower tubes, and highlight the importance of morphological traits, beyond the forbidden links hypothesis, in structuring interactions between mutualistic partners, revealing that the role of niche-based processes can be much more complex than previously known.

Influences of sampling effort on detected patterns and structuring processes of a Neotropical plant-hummingbird network.

Virtually all empirical ecological interaction networks to some extent suffer from undersampling. However, how limitations imposed by sampling incompleteness affect our understanding of ecological networks is still poorly explored, which may hinder further advances in the field. Here, we use a plant-hummingbird network with unprecedented sampling effort (2716 h of focal observations) from the Atlantic Rainforest in Brazil, to investigate how sampling effort affects the description of network structure (i.e. widely used network metrics) and the relative importance of distinct processes (i.e. species abundances vs. traits) in determining the frequency of pairwise interactions. By dividing the network into time slices representing a gradient of sampling effort, we show that quantitative metrics, such as interaction evenness, specialization (H2 '), weighted nestedness (wNODF) and modularity (Q; QuanBiMo algorithm) were less biased by sampling incompleteness than binary metrics. Furthermore, the significance of some network metrics changed along the sampling effort gradient. Nevertheless, the higher importance of traits in structuring the network was apparent even with small sampling effort. Our results (i) warn against using very poorly sampled networks as this may bias our understanding of networks, both their patterns and structuring processes, (ii) encourage the use of quantitative metrics little influenced by sampling when performing spatio-temporal comparisons and (iii) indicate that in networks strongly constrained by species traits, such as plant-hummingbird networks, even small sampling is sufficient to detect their relative importance for the frequencies of interactions. Finally, we argue that similar effects of sampling are expected for other highly specialized subnetworks.

Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird-plant network.

Understanding the relative importance of multiple processes on structuring species interactions within communities is one of the major challenges in ecology. Here, we evaluated the relative importance of species abundance and forbidden links in structuring a hummingbird-plant interaction network from the Atlantic rainforest in Brazil. Our results show that models incorporating phenological overlapping and morphological matches were more accurate in predicting the observed interactions than models considering species abundance. This means that forbidden links, by imposing constraints on species interactions, play a greater role than species abundance in structuring the ecological network. We also show that using the frequency of interaction as a proxy for species abundance and network metrics to describe the detailed network structure might lead to biased conclusions regarding mechanisms generating network structure. Together, our findings suggest that species abundance can be a less important driver of species interactions in communities than previously thought.