Dissimilarity in flea and host assemblages and their interaction networks along a spatial distance gradient: different patterns revealed by different network dissimilarity metrics.

We investigated the distance-decay pattern (an increase in dissimilarity with increasing geographic distance) in regional assemblages of fleas and their small mammalian hosts, as well as their interaction networks, in four biogeographic realms. Dissimilarity of assemblages (ßtotal) was partitioned into species richness differences (ßrich) and species replacement (ßrepl) components. Dissimilarity of networks was assessed using two metrics: (a) whole network dissimilarity (ßWN) partitioned into species replacement (ßST) and interaction rewiring (ßOS) components and (b) D statistics, measuring dissimilarity in the pure structure of the networks, without using information on species identities and calculated for hosts-shared-by-fleas networks (Dh) and fleas-shared-by-hosts networks (Df). We asked whether the distance-decay pattern (a) occurs among interactor assemblages or their interaction networks; (b) depends on the network dissimilarity metric used; and (c) differs between realms. The ßtotal and ßrepl of flea and host assemblages increased with distance in all realms except for host assemblages in the Afrotropics. ßrich for flea and host assemblages increased with distance in the Nearctic only. In networks, ßWN and ßST demonstrated a distance-decay pattern, whereas ßOS was mainly spatially invariant except in the Neotropics. Correlations of Dh or Df and geographic distance were mostly non-significant. We conclude that investigations of dissimilarity in interaction networks should include both types of dissimilarity metrics (those that consider partner identities and those that consider the pure structure of networks). This will allow elucidating the predictability of some facets of network dissimilarity and the unpredictability of other facets.

Urbanization alters the spatiotemporal dynamics of plant-pollinator networks in a tropical megacity.

Urbanization is a major driver of biodiversity change but how it interacts with spatial and temporal gradients to influence the dynamics of plant-pollinator networks is poorly understood, especially in tropical urbanization hotspots. Here, we analysed the drivers of environmental, spatial and temporal turnover of plant-pollinator interactions (interaction ß-diversity) along an urbanization gradient in Bengaluru, a South Indian megacity. The compositional turnover of plant-pollinator interactions differed more between seasons and with local urbanization intensity than with spatial distance, suggesting that seasonality and environmental filtering were more important than dispersal limitation for explaining plant-pollinator interaction ß-diversity. Furthermore, urbanization amplified the seasonal dynamics of plant-pollinator interactions, with stronger temporal turnover in urban compared to rural sites, driven by greater turnover of native non-crop plant species (not managed by people). Our study demonstrates that environmental, spatial and temporal gradients interact to shape the dynamics of plant-pollinator networks and urbanization can strongly amplify these dynamics.

Habitat fragmentation increases specialization of multi-trophic interactions by high species turnover.

Habitat fragmentation is altering species interactions worldwide. However, the mechanisms underlying the response of network specialization to habitat fragmentation remain unknown, especially for multi-trophic interactions. We here collected a large dataset consisting of 2670 observations of tri-trophic interactions among plants, sap-sucking aphids and honeydew-collecting ants on 18 forested islands in the Thousand Island Lake, China. For each island, we constructed an antagonistic plant-aphid and a mutualistic aphid-ant network, and tested how network specialization varied with island area and isolation. We found that both networks exhibited higher specialization on smaller islands, while only aphid-ant networks had increased specialization on more isolated islands. Variations in network specialization among islands was primarily driven by species turnover, which was interlinked across trophic levels as fragmentation increased the specialization of both antagonistic and mutualistic networks through bottom-up effects via plant and aphid communities. These findings reveal that species on small and isolated islands display higher specialization mainly due to effects of fragmentation on species turnover, with behavioural changes causing interaction rewiring playing only a minor role. Our study highlights the significance of adopting a multi-trophic perspective when exploring patterns and processes in structuring ecological networks in fragmented landscapes.

The reliability of regional ecological knowledge to build local interaction networks: a test using seed-dispersal networks across land-bridge islands.

Building ecological networks is the fundamental basis of depicting how species in communities interact, but sampling complex interaction networks is extremely labour intensive. Recently, indirect ecological information has been applied to build interaction networks. Here we propose to extend the source of indirect ecological information, and applied regional ecological knowledge to build local interaction networks. Using a high-resolution dataset consisting of 22 locally observed networks with 17 572 seed-dispersal events, we test the reliability of indirectly derived local networks based on regional ecological knowledge (REK) across islands. We found that species richness strongly influenced 'local interaction rewiring' (i.e. the proportion of locally observed interactions among regionally interacting species), and all network properties were biased using REK-based networks. Notably, species richness and local interaction rewiring strongly affected estimations of REK-based network structures. However, locally observed and REK-based networks detected the same trends of how network structure correlates to island area and isolation. These results suggest that we should use REK-based networks cautiously for reflecting actual interaction patterns of local networks, but highlight that REK-based networks have great potential for comparative studies across environmental gradients. The use of indirect regional ecological information may thus advance our understanding of biogeographical patterns of species interactions.

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.

A keystone mutualism promotes resistance to invasion.

It is not uncommon for one or a few species, and their interactions, to have disproportionate effects on other species in ecological communities. Such keystone interactions might affect how communities respond to the invasion of non-native species by preventing or inhibiting the establishment, spread or impact of non-native species. We explore whether a keystone mutualism among a hummingbird-mistletoe-marsupial promotes ecological resistance to an invasive pollinator, the bumblebee Bombus terrestris, by comparing data collected at sites prior to bumblebee invasion to data collected 11 years after the invasion in sites with and without the keystone mutualism. We built pollination networks and focused on network motifs, regarded as building blocks of networks, to identify the central pollinators and estimate the change in their interactions after invasion of B. terrestris. We also estimated the interaction rewiring across the season in post-invasion networks and tested it as a possible mechanism explaining how the keystone mutualism increased ecological resistance to invasion. We found two times more species in post-invasion sites with the keystone mutualism than in post-invasion sites without the keystone mutualism. Moreover, we found that invasive bumblebee reduced the strength and interaction niche of the five central pollinator species while increasing its own strength and interaction niche, suggesting a replacement of interactions. Also, we found that the keystone mutualism promoted resistance to B. terrestris invasion by reducing its negative impacts on central species. In the presence of the keystone mutualism, central species had three times more direct interactions than in sites without this keystone mutualism. The higher interaction rewiring, after invasion of B. terrestris, in sites with the keystone mutualism indicates greater chances of central pollinators to form new interactions and reduces their competence for resources with the non-native bumblebee. Our results demonstrate that a keystone mutualism can enhance community resistance against the impacts of a non-native invasive pollinator by increasing species diversity and promoting interaction rewiring in the community. This study suggests that the conservation of mutualisms, especially those considered keystone, could be essential for long-term preservation of natural communities under current and future impacts of global change.

Es común que una o unas pocas especies y sus interacciones tengan efectos desproporcionado sobre otras especies en las comunidades. Estas especies y sus interacciones claves podrían afectar el modo en que las comunidades responden a la invasión de especies no nativas al prevenir o disminuir su establecimiento, su propagación o el impacto de las mismas. En este estudio evaluamos si un mutualismo clave entre un colibrí, un muérdago y un marsupial promueve la resistencia de la comunidad frente a un polinizador invasor, el abejorro Bombus terrestris, mediante la comparación de datos colectados en sitios previos a la invasión del abejorro y datos colectados 11 años después de su invasión, en sitios con y sin el mutualismo clave. Construimos redes ecológicas planta-polinizador y nos centramos en los modos de interacción ("interaction motifs"), los cuales son usados como bloques en la construcción de las redes, para identificar los polinizadores centrales y estimar el cambio en sus interacciones después de la invasión de B. terrestris. Además, en las redes posteriores a la invasión estimamos la reconexión de interacciones a lo largo de la temporada y la evaluamos como un posible mecanismo mediante la cual el mutualismo clave aumentó la resistencia a la invasión. En sitios posteriores a la invasión con el mutualismo clave encontramos dos veces más especies que en sitios posteriores a la invasión ausentes de éste. Además, en los sitios ausentes del mutualismo clave, encontramos que el abejorro invasor redujo la fuerza y el nicho de interacción de los cinco polinizadores centrales mientras incrementó su propia fuerza y nicho de interacciones, sugiriendo un reemplazo de interacciones. Asimismo, encontramos que el mutualismo clave promovió la resistencia de la comunidad a la invasión de B. terrestris al reducir sus impactos negativos sobre las especies centrales. En presencia del mutualismo clave, las especies centrales presentaron tres veces más interacciones directas que en sitios ausentes de esta interacción. La gran reconexión de interacciones encontrada en sitios posteriores a la invasión con el mutualismo clave indica mayores probabilidades de que los polinizadores centrales formen nuevas interacciones y reduzcan la competencia por recursos con el abejorro no nativo. Nuestros resultados demuestran que un mutualismo clave puede mejorar la resistencia de la comunidad frente a los impactos de especies invasoras al incrementar la diversidad de especies y promover la reconexión de interacciones en la comunidad. Este estudio sugiere que la conservación de las interacciones mutualistas, principalmente aquellas consideradas claves, podría ser esencial para preservar las comunidades naturales frente a los impactos del cambio global.

How cougars and feral donkeys change desert wetlands: Novel interactions between native predators and non-native megaherbivores shape trophic cascades in the Anthropocene.

Research Highlight: Lundgren, E. J., Ramp, D., Middleton, O. S., Wooster, E. I. F., Kusch, E., Balisi, M., Ripple, W. J., Hasselerharm, C. D., Sanchez, J. N., Mills, M. & Wallach, A. D. (2022) A novel trophic cascade between cougars and feral donkeys shapes desert wetlands. Journal of Animal Ecology, (91, 2010-2022). https://doi.org/10.1111/1365-2656.13766. Despite being absent from most regions of the contemporary world, megafauna species dominated the dynamics of ecological communities until the late Pleistocene. Trophic rewilding is a promising approach to restoring megafauna interactions, their functional roles and the consequent trophic cascades. Unintentional rewilding with large non-native herbivores, such as equids, offers outstanding opportunities for ecologists to understand the outcomes of using replacement species to restore the ecological functions of extinct native megafauna. In this context, it is relevant to understand the extent to which extant native predators can impose top-down control on non-native megaherbivores and how trophic cascades arising from novel predator-prey interactions influences biodiversity and ecosystem functions. In Death Valley National Park (United States), Lundgren et al. depict a natural experiment showing compelling evidence of native cougars overcoming ecological naïveté-that is, the mismatches between predator and prey species that do not share a common evolutionary history-and are now successfully preying on younger individuals of feral donkeys. These non-native donkeys, whose growing wild populations threaten the native biota, became cougars' most frequent dietary item in that region. In areas with cougars, donkeys changed their spatiotemporal foraging patterns, becoming diurnal and less active. On the other hand, donkeys remain more active and forage throughout the day and night in areas without cougars. The cougar-donkey interaction triggered a behaviourally mediated trophic cascade emerging from a 'landscape of fear', that is, from the perception of spatial heterogeneity in predation risk by donkeys. Areas with cougars have less trampled ground, fewer donkey trails, and much more canopy cover and vegetation around water. Donkeys concentrate their activity mostly in topologically plain terrains lacking proper sites for the ambush behaviour of cougars and with more intense human presence, likely acting as a shield against the predators. Lundgren et al. present a promising model system for studying the effects of fearful grazers on community structure in the context of novel ecological interactions being established in the Anthropocene. Whether the emerging cascade is transient or persistent, the relative roles of consumptive and non-consumptive effects as underlying mechanisms, and their consequences for food web structure, functioning and stability, are questions of general interest. Addressing them can help us to elucidate the costs and benefits of using non-native megaherbivores in the functional restoration of permanently invaded ecosystems.

Pesquisa em Destaque: Lundgren, E. J., Ramp, D., Middleton, O. S., Wooster, E. I. F., Kusch, E., Balisi, M., Ripple, W. J., Hasselerharm, C. D., Sanchez, J. N., Mills, M. & Wallach, A. D. (2022) A novel trophic cascade between cougars and feral donkeys shapes desert wetlands. Journal of Animal Ecology, 00:00-00. https://doi.org/10.1111/1365-2656.13766. Apesar de estarem ausentes da maioria das regiões do mundo contemporâneo, as espécies da megafauna dominaram a dinâmica das comunidades ecológicas até o Pleistoceno tardio. A refaunação trófica é uma abordagem promissora para a restauração das interações da megafauna, de seus papéis funcionais e das cascatas tróficas delas decorrentes. A refaunação não-intencional com grandes herbívoros não-nativos, tais como equídeos, oferece oportunidades extraordinárias para os ecólogos entenderem as consequências do uso de espécies substitutas para restaurar as funções ecológicas da extinta megafauna nativa. Nesse contexto, é relevante entendermos o quanto os predadores nativos atuais podem impor controle de cima para baixo sobre mega-herbívoros não-nativos, e como cascatas tróficas oriundas de novas interações predador-presa influenciam a biodiversidade e as funções ecossistêmicas. No Parque Nacional do Vale da Morte (Estados Unidos), Lundgren et al. reportam um experimento natural mostrando evidências contundentes de que onças pardas superaram a ingenuidade ecológica - i.e., os desajustes entre predadores e presas que não compartilham uma história evolutiva comum - e agora estão predando os indivíduos mais jovens de burros ferais com sucesso. Esses burros exóticos, cujas populações crescentes ameaçam a biota nativa, se tornaram o item mais frequente da dieta das onças pardas nessa região. Em áreas com onças pardas, os burros mudaram seus padrões espaço-temporais de forrageio, tornando-se diurnos e menos ativos. Por outro lado, os burros permanecem mais ativos e forrageiam durante o dia e à noite em áreas sem onças pardas. A interação entre onças pardas e burros desencadeou uma cascata trófica comportamentalmente mediada que emerge de uma "paisagem de medo", isto é, da percepção dos burros sobre a heterogeneidade espacial do risco de predação. Áreas com onças pardas tiveram menos solo pisoteado, menos trilhas de burros, e muito mais cobertura de dossel e vegetação no entorno da água. Os burros concentram a maior parte de suas atividades em terrenos topologicamente planos, os quais não apresentam lugares apropriados para o comportamento de emboscada das onças pardas e têm presença humana mais intensa, provavelmente agindo como escudos contra predadores. Lundgren et al. apresentam um sistema modelo promissor para o estudo de efeitos de pastadores temorosos sobre a estrutura comunitária no contexto de novas interações ecológicas em estabelecimento no Antropoceno. Se a cascata trófica emergente é transiente ou persistente, os papéis relativos dos efeitos diretos e indiretos como mecanismos subjacentes, e suas consequências para a estrutura, funcionamento e estabilidade da teia trófica são questões de interesse geral. Respondê-las pode nos ajudar a elucidar os custos e benefícios de usar mega-herbívoros não-nativos na restauração funcional de ecossistemas permanentemente invadidos.

Plant-centred sampling estimates higher beta diversity of interactions than pollinator-based sampling across habitats.

When describing plant-animal interaction networks, sampling can be performed using plant- or animal-centred approaches. Despite known effects of sampling on network structure, how samplings affect the estimates of interaction ß-diversity across networks is still unresolved. We investigated how the sampling method affects the assessment of ß-diversity of interactions, turnover and rewiring. We contrasted plant- and animal-centred sampling methods applied to pollination networks across habitats in a heterogeneous tropical landscape, the Pantanal Wetlands. We also asked whether plant traits influence the difference in interaction specialization according to sampling. Plant-centred networks resulted in higher ß-diversity of interactions in space than animal-centred networks. Turnover explained most of the ß-diversity in both methods, but rewiring was proportionately more important when using the animal-centred method. While the plant-centred method indicated lower network modularity and specialization, floral traits modulated the effects of the sampling method on species-level network metrics. Combining animal- and plant-centred approaches returned intermediate values for ß-diversity of interactions and network metrics. Distinct methods may also be better suited for answering questions at different scales. Our results point out that the method choice, or combination of methods, should always reflect the appropriate scale of the factors determining the interactions being investigated.

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.

Coevolution Slows the Disassembly of Mutualistic Networks.

Important groups of mutualistic species are threatened worldwide, and identifying factors that make them more or less fragile in the face of disturbance is becoming increasingly critical. Although much research has focused on identifying the ecological factors that favor the stability of communities rich in mutualists, much less has been devoted to understanding the role played by historical and contemporary evolution. Here we develop mathematical models and computer simulations of coevolving mutualistic communities that allow us to explore the importance of coevolution in stabilizing communities against anthropogenic disturbance. Our results demonstrate that communities with a long history of coevolution are substantially more robust to disturbance, losing individual species and interactions at lower rates. In addition, our results identify a novel phenomenon-coevolutionary rescue-that mitigates the impacts of ongoing anthropogenic disturbance by rewiring the network structure of the community in a way that compensates for the extinction of individual species and interactions.