Plant-hummingbird pollination networks exhibit limited rewiring after experimental removal of a locally abundant plant species.

Mutualistic relationships, such as those between plants and pollinators, may be vulnerable to the local extinctions predicted under global environmental change. However, network theory predicts that plant-pollinator networks can withstand species loss if pollinators switch to alternative floral resources (rewiring). Whether rewiring occurs following species loss in natural communities is poorly known because replicated species exclusions are difficult to implement at appropriate spatial scales. We experimentally removed a hummingbird-pollinated plant, Heliconia tortuosa, from within tropical forest fragments to investigate how hummingbirds respond to temporary loss of an abundant resource. Under the rewiring hypothesis, we expected that behavioural flexibility would allow hummingbirds to use alternative resources, leading to decreased ecological specialization and reorganization of the network structure (i.e. pairwise interactions). Alternatively, morphological or behavioural constraints-such as trait-matching or interspecific competition-might limit the extent to which hummingbirds alter their foraging behaviour. We employed a replicated Before-After-Control-Impact experimental design and quantified plant-hummingbird interactions using two parallel sampling methods: pollen collected from individual hummingbirds ('pollen networks', created from >300 pollen samples) and observations of hummingbirds visiting focal plants ('camera networks', created from >19,000 observation hours). To assess the extent of rewiring, we quantified ecological specialization at the individual, species and network levels and examined interaction turnover (i.e. gain/loss of pairwise interactions). H. tortuosa removal caused some reorganization of pairwise interactions but did not prompt large changes in specialization, despite the large magnitude of our manipulation (on average, >100 inflorescences removed in exclusion areas of >1 ha). Although some individual hummingbirds sampled through time showed modest increases in niche breadth following Heliconia removal (relative to birds that did not experience resource loss), these changes were not reflected in species- and network-level specialization metrics. Our results suggest that, at least over short time-scales, animals may not necessarily shift to alternative resources after losing an abundant food resource-even in species thought to be highly opportunistic foragers, such as hummingbirds. Given that rewiring contributes to theoretical predictions of network stability, future studies should investigate why pollinators might not expand their diets after a local resource extinction.

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.

Predator discrimination of prey promotes the predator-mediated coexistence of prey species.

The predator discrimination of prey can affect predation intensity and the prey density dependence of predators, which has the potential to alter the coexistence of prey species. We used a predator-prey population dynamics model accounting for the predator's adaptive diet choice and predator discrimination of prey to investigate how the latter influences prey coexistence. The model revealed that (i) prey species that are perceived as belonging to the same species by a predator are attacked in the same manner, and it is more difficult for them to coexist than those that are recognized as different prey species, and (ii) prey species that are not discriminated by a predator-and therefore cannot coexist-may coexist in the presence of an alternative predator that does discriminate between them. These results suggest that prey diversity, which favours the predator discrimination of prey, and the different capabilities of predators to identify prey species both enhance prey coexistence.

Phenology and flowering overlap drive specialisation in plant-pollinator networks.

Variation in dietary specialisation stems from fundamental interactions between species and their environment. Consequently, understanding the drivers of this variation is key to understanding ecological and evolutionary processes. Dietary specialisation in wild bees has received attention due to their close mutualistic dependence on plants, and because both groups are threatened by biodiversity loss. Many principles governing pollinator specialisation have been identified, but they remain largely unvalidated. Organismal phenology has the potential to structure realised specialisation by determining concurrent resource availability and pollinator foraging activity. We evaluate this principle using mechanistic models of adaptive foraging in pollinators within plant-pollinator networks. While temporal resource overlap has little impact on specialisation in pollinators with extended flight periods, reduced overlap increases specialisation as pollinator flight periods decrease. These results are corroborated empirically using pollen load data taken from bees with shorter and longer flight periods across environments with high and low temporal resource overlap.

Rapid evolution promotes fluctuation-dependent species coexistence.

Recent studies have demonstrated that rapid contemporary evolution can play a significant role in regulating population dynamics on ecological timescales. Here we identify a previously unrecognised mode by which rapid evolution can promote species coexistence via temporal fluctuations and a trade-off between competitive ability and the speed of adaptive evolution. We show that this interaction between rapid evolution and temporal fluctuations not only increases the range of coexistence conditions under a gleaner-opportunist trade-off (i.e. low minimum resource requirement [R* ] vs. high maximum growth rate) but also yields stable coexistence in the absence of a classical gleaner-opportunist trade-off. Given the propensity for both oscillatory dynamics and different rates of adaptation between species (including rapid evolution and phenotypic plasticity) in the real world, we argue that this expansion of fluctuation-dependent coexistence theory provides an important overlooked solution to the so-called 'paradox of the plankton'.

Mutualistic networks: moving closer to a predictive theory.

Plant-animal mutualistic networks sustain terrestrial biodiversity and human food security. Global environmental changes threaten these networks, underscoring the urgency for developing a predictive theory on how networks respond to perturbations. Here, I synthesise theoretical advances towards predicting network structure, dynamics, interaction strengths and responses to perturbations. I find that mathematical models incorporating biological mechanisms of mutualistic interactions provide better predictions of network dynamics. Those mechanisms include trait matching, adaptive foraging, and the dynamic consumption and production of both resources and services provided by mutualisms. Models incorporating species traits better predict the potential structure of networks (fundamental niche), while theory based on the dynamics of species abundances, rewards, foraging preferences and reproductive services can predict the extremely dynamic realised structures of networks, and may successfully predict network responses to perturbations. From a theoretician's standpoint, model development must more realistically represent empirical data on interaction strengths, population dynamics and how these vary with perturbations from global change. From an empiricist's standpoint, theory needs to make specific predictions that can be tested by observation or experiments. Developing models using short-term empirical data allows models to make longer term predictions of community dynamics. As more longer term data become available, rigorous tests of model predictions will improve.

Niche shift in three foraging insectivorous birds in lowland Malaysian forest patches.

With the rapid growth of agricultural areas globally, forest birds increasingly encounter fragmented landscapes in which forest patches are surrounded by an agricultural plantation matrix, yet how birds respond behaviourally to this fragmentation is poorly understood. Information on microhabitat requirements of birds is scarce, but nevertheless essential to predicting adaptation of bird species to the patchy landscapes. We investigated foraging patterns of three tropical insectivorous birds, Green Iora Aegithina viridissima, Pin-striped Tit-Babbler Macronus gularis and Chestnut-winged Babbler Cyanoderma erythropterum, to determine whether they vary in foraging methods in different forest patches. Our study area encompassed old-logged lowland forest; one continuous forest and three forest patches. Observations were performed for 15 days every month for a period of 13 months. Information on foraging height, substrate, attack manoeuvres, and foliage density was collected independently for each foraging bird individual. All three species used different foraging substrates and attack manoeuvres in different habitat types. The Green Iora frequently used lower strata when foraging in forest patches as opposed to continuous forest, while the Pin-striped Tit-Babbler tended to forage in more dense vegetation in patches. Only Chestnut-winged Babbler displayed complete foraging plasticity across all study parameters. Different habitat features (e.g., edges, microclimates) between continuous forest and forest patches significantly influenced the foraging strategies of the study species. These changes in foraging strategies suggest that some Malaysian forest birds (e.g. generalist species) can respond behaviourally to fragmentation and habitat loss. Although continuous forest has critically important characteristics that need to be conserved, remnant forest patches are also important as ecological movement corridors and foraging grounds for birds.

Adaptive Foraging of Pollinators Can Promote Pollination of a Rare Plant Species.

Most pollinators have the foraging flexibility to visit a wide variety of plant species. Yet few studies of pollinator-mediated processes in plants have considered the effects of variation in individual foraging patterns on plant reproductive success. In this study, we use an individual-based model of pollinator foraging economics to predict how visitation rates and pollination success of two coflowering plant species change with their frequency (relative abundance). Whereas previous studies suggested that adaptive foraging of pollinators always favors pollination of abundant plant species (positive frequency dependence), here we show that under certain conditions the per capita pollination success of a rare plant species can exceed that of a more abundant species. Specifically, when the overall flower density is sufficiently high and pollinators' perception ranges are sufficiently large, animals with limited memory of previously encountered rewards forage in a way that favors pollination of the rarer plant species. Moreover, even with perfectly informed foragers, a rare plant species benefits more from offering a higher floral reward than a more abundant species. Our results show that adaptive foraging of individual pollinators can have important implications for plant community dynamics and the persistence of rare plant species.

Interaction rewiring and the rapid turnover of plant-pollinator networks.

Whether species interactions are static or change over time has wide-reaching ecological and evolutionary consequences. However, species interaction networks are typically constructed from temporally aggregated interaction data, thereby implicitly assuming that interactions are fixed. This approach has advanced our understanding of communities, but it obscures the timescale at which interactions form (or dissolve) and the drivers and consequences of such dynamics. We address this knowledge gap by quantifying the within-season turnover of plant-pollinator interactions from weekly censuses across 3 years in a subalpine ecosystem. Week-to-week turnover of interactions (1) was high, (2) followed a consistent seasonal progression in all years of study and (3) was dominated by interaction rewiring (the reassembly of interactions among species). Simulation models revealed that species' phenologies and relative abundances constrained both total interaction turnover and rewiring. Our findings reveal the diversity of species interactions that may be missed when the temporal dynamics of networks are ignored.

Colonisation rate and adaptive foraging control the emergence of trophic cascades.

Ecological communities are assembled and sustained by colonisation. At the same time, predators make foraging decisions based on the local availabilities of potential resources, which reflects colonisation. We combined field and laboratory experiments with mathematical models to demonstrate that a feedback between these two processes determines emergent patterns in community structure. Namely, our results show that prey colonisation rate determines the strength of trophic cascades - a feature of virtually all ecosystems - by prompting behavioural shifts in adaptively foraging omnivorous fish predators. Communities experiencing higher colonisation rates were characterised by higher invertebrate prey and lower producer biomasses. Consequently, fish functioned as predators when colonisation rate was high, but as herbivores when colonisation rate was low. Human land use is changing habitat connectivity worldwide. A deeper quantitative understanding of how spatial processes modify individual behaviour, and how this scales to the community level, will be required to predict ecosystem responses to these changes.

Adaptive foraging behaviour of individual pollinators and the coexistence of co-flowering plants.

Although pollinators can play a central role in determining the structure and stability of plant communities, little is known about how their adaptive foraging behaviours at the individual level, e.g. flower constancy, structure these interactions. Here, we construct a mathematical model that integrates individual adaptive foraging behaviour and population dynamics of a community consisting of two plant species and a pollinator species. We find that adaptive foraging at the individual level, as a complementary mechanism to adaptive foraging at the species level, can further enhance the coexistence of plant species through niche partitioning between conspecific pollinators. The stabilizing effect is stronger than that of unbiased generalists when there is also strong competition between plant species over other resources, but less so than that of multiple specialist species. This suggests that adaptive foraging in mutualistic interactions can have a very different impact on the plant community structure from that in predator-prey interactions. In addition, the adaptive behaviour of individual pollinators may cause a sharp regime shift for invading plant species. These results indicate the importance of integrating individual adaptive behaviour and population dynamics for the conservation of native plant communities.

Environmental weakening of trophic interactions drives stability in stochastic food webs.

The physiological performance and behaviour of organisms are contingent on environmental conditions. When these conditions vary over time, this can have important consequences for the dynamics of individual populations and entire species communities. While the importance of environmental variation on the structuring and stability of natural food webs is recognised, little work has been done so far to build up a theoretical understanding of these processes. Here we investigate a simple model food web, where a consumer species forages flexibly upon two distinct, inter-competing resource species. Resource productivities or the resource intake rates by the consumer are assumed to depend on environmental conditions in a realistic manner. Fluctuations in these parameters drive variation in the strength of consumer-resource interactions, depending on whether the resource or the consumer is sensitive to environmental noise. The way resources and the consumer respond to changes in environmental conditions stems from the deterministic influence of each stochastic parameter on food web dynamics, which interact with the consumer adaptation process as well as between-resource competition. According to recent empirical reports, the mechanisms behind our results are likely to be relevant in natural systems and thus the model predictions are of potential importance in understanding food web responses to environmental stochasticity in general.

Trophic omnivory across a productivity gradient: intraguild predation theory and the structure and strength of species interactions.

Intraguild predation theory centres on two predictions: (i) for an omnivore and an intermediate predator (IG-prey) to coexist on shared resources, the IG-prey must be the superior resource competitor, and (ii) increasing resource productivity causes the IG-prey's equilibrium abundance to decline. I tested these predictions with a series of species-rich food webs along New Zealand's rocky shores, focusing on two predatory whelks, Haustrum haustorium, a trophic omnivore, and Haustrum scobina, the IG-prey. In contrast to theory, the IG-prey's abundance increased with productivity. Furthermore, feeding rates and allometric considerations indicate a competitive advantage for the omnivore when non-shared prey are considered, despite the IG-prey's superiority for shared prey. Nevertheless, clear and regular cross-gradient changes in network structure and interaction strengths were observed that challenge the assumptions of current theory. These insights suggest that the consideration of consumer-dependent functional responses, non-equilibrium dynamics, the dynamic nature of prey choice and non-trophic interactions among basal prey will be fruitful avenues for theoretical development.

The Adaptive Dynamics of Consumer Choice.

This article uses mathematical models to investigate the consequences of noninstantaneous choice between two prey types by a predator. The models are characterized by three features: sustained cycles in predator and prey population sizes, a trade-off between the predator's consumption rates of the two prey and adaptive adjustment of the consumption rates at a rate proportional to the change in predator fitness per unit change in consumption rates. Adaptive adjustment of consumption rates frequently prevents the system from achieving an ideal free distribution of predator foraging effort and frequently results in chaotic dynamics or alternative attractors. The process of switching to consume the more common prey can reduce the minimum density of one or both prey. These phenomena occur for a variety of different models, including models in which both prey are in the same or in distinct habitats. An ideal free distribution can often be attained by adding prey refuges or immigration, provided these have a large enough effect on the dynamics of the system. The dynamics of switching can be important in determining indirect interactions between prey species and other aspects of food web dynamics.