Macroevolution of the plant-hummingbird pollination system.

Plant-hummingbird interactions are considered a classic example of coevolution, a process in which mutually dependent species influence each other's evolution. Plants depend on hummingbirds for pollination, whereas hummingbirds rely on nectar for food. As a step towards understanding coevolution, this review focuses on the macroevolutionary consequences of plant-hummingbird interactions, a relatively underexplored area in the current literature. We synthesize prior studies, illustrating the origins and dynamics of hummingbird pollination across different angiosperm clades previously pollinated by insects (mostly bees), bats, and passerine birds. In some cases, the crown age of hummingbirds pre-dates the plants they pollinate. In other cases, plant groups transitioned to hummingbird pollination early in the establishment of this bird group in the Americas, with the build-up of both diversities coinciding temporally, and hence suggesting co-diversification. Determining what triggers shifts to and away from hummingbird pollination remains a major open challenge. The impact of hummingbirds on plant diversification is complex, with many tropical plant lineages experiencing increased diversification after acquiring flowers that attract hummingbirds, and others experiencing no change or even a decrease in diversification rates. This mixed evidence suggests that other extrinsic or intrinsic factors, such as local climate and isolation, are important covariables driving the diversification of plants adapted to hummingbird pollination. To guide future studies, we discuss the mechanisms and contexts under which hummingbirds, as a clade and as individual species (e.g. traits, foraging behaviour, degree of specialization), could influence plant evolution. We conclude by commenting on how macroevolutionary signals of the mutualism could relate to coevolution, highlighting the unbalanced focus on the plant side of the interaction, and advocating for the use of species-level interaction data in macroevolutionary studies.

Warming underpins community turnover in temperate freshwater and terrestrial communities.

Rising temperatures are leading to increased prevalence of warm-affinity species in ecosystems, known as thermophilisation. However, factors influencing variation in thermophilisation rates among taxa and ecosystems, particularly freshwater communities with high diversity and high population decline, remain unclear. We analysed compositional change over time in 7123 freshwater and 6201 terrestrial, mostly temperate communities from multiple taxonomic groups. Overall, temperature change was positively linked to thermophilisation in both realms. Extirpated species had lower thermal affinities in terrestrial communities but higher affinities in freshwater communities compared to those persisting over time. Temperature change's impact on thermophilisation varied with community body size, thermal niche breadth, species richness and baseline temperature; these interactive effects were idiosyncratic in the direction and magnitude of their impacts on thermophilisation, both across realms and taxonomic groups. While our findings emphasise the challenges in predicting the consequences of temperature change across communities, conservation strategies should consider these variable responses when attempting to mitigate climate-induced biodiversity loss.

Land-use intensity influences European tetrapod food webs.

Land use intensification favours particular trophic groups which can induce architectural changes in food webs. These changes can impact ecosystem functions, services, stability and resilience. However, the imprint of land management intensity on food-web architecture has rarely been characterized across large spatial extent and various land uses. We investigated the influence of land management intensity on six facets of food-web architecture, namely apex and basal species proportions, connectance, omnivory, trophic chain lengths and compartmentalization, for 67,051 European terrestrial vertebrate communities. We also assessed the dependency of this influence of intensification on land use and climate. In addition to more commonly considered climatic factors, the architecture of food webs was notably influenced by land use and management intensity. Intensification tended to strongly lower the proportion of apex predators consistently across contexts. In general, intensification also tended to lower proportions of basal species, favoured mesopredators, decreased food webs compartmentalization whereas it increased their connectance. However, the response of food webs to intensification was different for some contexts. Intensification sharply decreased connectance in Mediterranean and Alpine settlements, and it increased basal tetrapod proportions and compartmentalization in Mediterranean forest and Atlantic croplands. Besides, intensive urbanization especially favoured longer trophic chains and lower omnivory. By favouring mesopredators in most contexts, intensification could undermine basal tetrapods, the cascading effects of which need to be assessed. Our results support the importance of protecting top predators where possible and raise questions about the long-term stability of food webs in the face of human-induced pressures.

When cheating turns into a stabilizing mechanism of plant-pollinator communities.

Mutualistic interactions, such as plant-mycorrhizal or plant-pollinator interactions, are widespread in ecological communities and frequently exploited by cheaters, species that profit from interactions without providing benefits in return. Cheating usually negatively affects the fitness of the individuals that are cheated on, but the effects of cheating at the community level remains poorly understood. Here, we describe 2 different kinds of cheating in mutualistic networks and use a generalized Lotka-Volterra model to show that they have very different consequences for the persistence of the community. Conservative cheating, where a species cheats on its mutualistic partners to escape the cost of mutualistic interactions, negatively affects community persistence. In contrast, innovative cheating occurs with species with whom legitimate interactions are not possible, because of a physiological or morphological barrier. Innovative cheating can enhance community persistence under some conditions: when cheaters have few mutualistic partners, cheat at low or intermediate frequency and the cost associated with mutualism is not too high. Under these conditions, the negative effects of cheating on partner persistence are overcompensated at the community level by the positive feedback loops that arise in diverse mutualistic communities. Using an empirical dataset of plant-bird interactions (hummingbirds and flowerpiercers), we found that observed cheating patterns are highly consistent with theoretical cheating patterns found to increase community persistence. This result suggests that the cheating patterns observed in nature could contribute to promote species coexistence in mutualistic communities, instead of necessarily destabilizing them.

The geography of climate and the global patterns of species diversity.

Climate's effect on global biodiversity is typically viewed through the lens of temperature, humidity and resulting ecosystem productivity1-6. However, it is not known whether biodiversity depends solely on these climate conditions, or whether the size and fragmentation of these climates are also crucial. Here we shift the common perspective in global biodiversity studies, transitioning from geographic space to a climate-defined multidimensional space. Our findings suggest that larger and more isolated climate conditions tend to harbour higher diversity and species turnover among terrestrial tetrapods, encompassing more than 30,000 species. By considering both the characteristics of climate itself and its geographic attributes, we can explain almost 90% of the variation in global species richness. Half of the explanatory power (45%) may be attributed either to climate itself or to the geography of climate, suggesting a nuanced interplay between them. Our work evolves the conventional idea that larger climate regions, such as the tropics, host more species primarily because of their size7,8. Instead, we underscore the integral roles of both the geographic extent and degree of isolation of climates. This refined understanding presents a more intricate picture of biodiversity distribution, which can guide our approach to biodiversity conservation in an ever-changing world.

Accelerated body size evolution in upland environments is correlated with recent speciation in South American freshwater fishes.

Speciation rates vary greatly among taxa and regions and are shaped by both biotic and abiotic factors. However, the relative importance and interactions of these factors are not well understood. Here we investigate the potential drivers of speciation rates in South American freshwater fishes, the most diverse continental vertebrate fauna, by examining the roles of multiple biotic and abiotic factors. We integrate a dataset on species geographic distribution, phylogenetic, morphological, climatic, and habitat data. We find that Late Neogene-Quaternary speciation events are strongly associated with body-size evolution, particularly in lineages with small body sizes that inhabit higher elevations near the continental periphery. Conversely, the effects of temperature, area, and diversity-dependence, often thought to facilitate speciation, are negligible. By evaluating multiple factors simultaneously, we demonstrate that habitat characteristics associated with elevation, as well as body size evolution, correlate with rapid speciation in South American freshwater fishes. Our study emphasizes the importance of integrative approaches that consider the interplay of biotic and abiotic factors in generating macroecological patterns of species diversity.

Interannual climate variability improves niche estimates for ectothermic but not endothermic species.

Climate is an important limiting factor of species' niches and it is therefore regularly included in ecological applications such as species distribution models (SDMs). Climate predictors are often used in the form of long-term mean values, yet many species experience wide climatic variation over their lifespan and within their geographical range which is unlikely captured by long-term means. Further, depending on their physiology, distinct groups of species cope with climate variability differently. Ectothermic species, which are directly dependent on the thermal environment are expected to show a different response to temporal or spatial variability in temperature than endothermic groups that can decouple their internal temperature from that of their surroundings. Here, we explore the degree to which spatial variability and long-term temporal variability in temperature and precipitation change niche estimates for ectothermic (730 amphibian, 1276 reptile), and endothermic (1961 mammal) species globally. We use three different species distribution modelling (SDM) algorithms to quantify the effect of spatial and temporal climate variability, based on global range maps of all species and climate data from 1979 to 2013. All SDMs were cross-validated and accessed for their performance using the Area under the Curve (AUC) and the True Skill Statistic (TSS). The mean performance of SDMs using only climatic means as predictors was TSS = 0.71 and AUC = 0.90. The inclusion of spatial variability offers a significant gain in SDM performance (mean TSS = 0.74, mean AUC = 0.92), as does the inclusion of temporal variability (mean TSS = 0.80, mean AUC = 0.94). Including both spatial and temporal variability in SDMs shows the highest scores in AUC and TSS. Accounting for temporal rather than spatial variability in climate improved the SDM prediction especially in ectotherm groups such as amphibians and reptiles, while for endothermic mammals no such improvement was observed. These results indicate that including long term climate interannual climate variability into niche estimations matters most for ectothermic species that cannot decouple their physiology from the surrounding environment as endothermic species can.

Diel niche partitioning of a plant-hummingbird network in the Atlantic forest of Brazil.

Niche partitioning is an important mechanism that allows species to coexist. Within mutualistic interaction networks, diel niche partitioning, i.e., partitioning of resources throughout the day, has been neglected. We explored diel niche partitioning of a plant-hummingbird network in the Brazilian Atlantic forest for nine months. To evaluate diel patterns of hummingbird visits and nectar production, we used time-lapse cameras on focal flowers and repeated nectar volume and concentration measures, respectively. Additionally, we measured flower abundance around focal flowers and flower morphological traits. We did not observe diel partitioning for either hummingbirds or plants. Instead, hummingbirds appeared to specialize in different plant species, consistent with trophic niche partitioning, potentially resulting from competition. In contrast, plant species that co-flowered and shared hummingbird visits produced nectar during similar times, consistent with facilitation. Our focus on the fine-scale temporal pattern revealed that plants and hummingbirds appear to have different strategies for promoting co-existence.

Morphology and niche evolution influence hummingbird speciation rates.

How traits affect speciation is a long-standing question in evolution. We investigate whether speciation rates are affected by the traits themselves or by the rates of their evolution, in hummingbirds, a clade with great variation in speciation rates, morphology and ecological niches. Further, we test two opposing hypotheses, postulating that speciation rates are promoted by trait conservatism or, alternatively, by trait divergence. To address these questions, we analyse morphological (body mass and bill length) and niche traits (temperature and precipitation position and breadth, and mid-elevation), using a variety of methods to estimate speciation rates and correlate them with traits and their evolutionary rates. When it comes to the traits, we find faster speciation in smaller hummingbirds with shorter bills, living at higher elevations and experiencing greater temperature ranges. As for the trait evolutionary rates, we find that speciation increases with rates of divergence in the niche traits, but not in the morphological traits. Together, these results reveal the interplay of mechanisms through which different traits and their evolutionary rates (conservatism or divergence) influence the origination of hummingbird diversity.

Hummingbird community structure and nectar resources modulate the response of interspecific competition to forest conversion.

On-going land-use change has profound impacts on biodiversity by filtering species that cannot survive in disturbed landscapes and potentially altering biotic interactions. In particular, how land-use change reshapes biotic interactions remains an open question. Here, we used selectivity experiments with nectar feeders in natural and converted forests to test the direct and indirect effects of land-use change on resource competition in Andean hummingbirds along an elevational gradient. Selectivity was defined as the time hummingbirds spent at high resource feeders when feeders with both low and high resource values were offered in the presence of other hummingbird species. Selectivity approximates the outcome of interspecific competition (i.e., the resource intake across competing species); in the absence of competition, birds should exhibit higher selectivity. We evaluated the indirect effect of forest conversion on selectivity, as mediated by morphological dissimilarity and flower resource abundance, using structural equation models. We found that forest conversion influenced selectivity at low and mid-elevations, but the influence of morphological dissimilarity and resource availability on selectivity varied between these elevations. At mid-elevation, selectivity was more influenced by the presence of morphologically similar competitors than by resource abundance while at low-elevation resource abundance was a more important predictor of selectivity. Our results suggest that selectivity is influenced by forest conversion, but that the drivers of these changes vary across elevation, highlighting the importance of considering context-dependent variation in the composition of resources and competitors when studying competition.

Analyzing trophic ecosystem functions with the interaction functional space.

Quantifying the vulnerability of ecosystems to global change requires a better understanding of how trophic ecosystem functions emerge. So far, trophic ecosystem functions have been studied from the perspective of either functional diversity or network ecology. To integrate these two perspectives, we propose the interaction functional space (IFS) a conceptual framework to simultaneously analyze the effects of traits and interactions on trophic functions. We exemplify the added value of our framework for seed dispersal and wood decomposition and show how species interactions influence the relationship between functional trait diversity and trophic functions. We propose future applications for a range of functions where the IFS can help to elucidate mechanisms underpinning trophic functions and facilitate understanding of functional changes in ecosystems amidst global change.

Landscape dynamics and diversification of the megadiverse South American freshwater fish fauna.

Landscape dynamics are widely thought to govern the tempo and mode of continental radiations, yet the effects of river network rearrangements on dispersal and lineage diversification remain poorly understood. We integrated an unprecedented occurrence dataset of 4,967 species with a newly compiled, time-calibrated phylogeny of South American freshwater fishes-the most species-rich continental vertebrate fauna on Earth-to track the evolutionary processes associated with hydrogeographic events over 100 Ma. Net lineage diversification was heterogeneous through time, across space, and among clades. Five abrupt shifts in net diversification rates occurred during the Paleogene and Miocene (between 30 and 7 Ma) in association with major landscape evolution events. Net diversification accelerated from the Miocene to the Recent (c. 20 to 0 Ma), with Western Amazonia having the highest rates of in situ diversification, which led to it being an important source of species dispersing to other regions. All regional biotic interchanges were associated with documented hydrogeographic events and the formation of biogeographic corridors, including the Early Miocene (c. 23 to 16 Ma) uplift of the Serra do Mar and Serra da Mantiqueira and the Late Miocene (c. 10 Ma) uplift of the Northern Andes and associated formation of the modern transcontinental Amazon River. The combination of high diversification rates and extensive biotic interchange associated with Western Amazonia yielded its extraordinary contemporary richness and phylogenetic endemism. Our results support the hypothesis that landscape dynamics, which shaped the history of drainage basin connections, strongly affected the assembly and diversification of basin-wide fish faunas.

Linking human impacts to community processes in terrestrial and freshwater ecosystems.

Human impacts such as habitat loss, climate change and biological invasions are radically altering biodiversity, with greater effects projected into the future. Evidence suggests human impacts may differ substantially between terrestrial and freshwater ecosystems, but the reasons for these differences are poorly understood. We propose an integrative approach to explain these differences by linking impacts to four fundamental processes that structure communities: dispersal, speciation, species-level selection and ecological drift. Our goal is to provide process-based insights into why human impacts, and responses to impacts, may differ across ecosystem types using a mechanistic, eco-evolutionary comparative framework. To enable these insights, we review and synthesise (i) how the four processes influence diversity and dynamics in terrestrial versus freshwater communities, specifically whether the relative importance of each process differs among ecosystems, and (ii) the pathways by which human impacts can produce divergent responses across ecosystems, due to differences in the strength of processes among ecosystems we identify. Finally, we highlight research gaps and next steps, and discuss how this approach can provide new insights for conservation. By focusing on the processes that shape diversity in communities, we aim to mechanistically link human impacts to ongoing and future changes in ecosystems.

Blue and green food webs respond differently to elevation and land use.

While aquatic (blue) and terrestrial (green) food webs are parts of the same landscape, it remains unclear whether they respond similarly to shared environmental gradients. We use empirical community data from hundreds of sites across Switzerland and a synthesis of interaction information in the form of a metaweb to show that inferred blue and green food webs have different structural and ecological properties along elevation and among various land-use types. Specifically, in green food webs, their modular structure increases with elevation and the overlap of consumers' diet niche decreases, while the opposite pattern is observed in blue food webs. Such differences between blue and green food webs are particularly pronounced in farmland-dominated habitats, indicating that anthropogenic habitat modification modulates the climatic effects on food webs but differently in blue versus green systems. These findings indicate general structural differences between blue and green food webs and suggest their potential divergent future alterations through land-use or climatic changes.

Seasonal structure of interactions enhances multidimensional stability of mutualistic networks.

Community ecologists have made great advances in understanding how natural communities can be both diverse and stable by studying communities as interaction networks. However, focus has been on interaction networks aggregated over time, neglecting the consequences of the seasonal organization of interactions (hereafter 'seasonal structure') for community stability. Here, we extended previous theoretical findings on the topic in two ways: (i) by integrating empirical seasonal structure of 11 plant-hummingbird communities into dynamic models, and (ii) by tackling multiple facets of network stability together. We show that, in a competition context, seasonal structure enhances community stability by allowing diverse and resilient communities while preserving their robustness to species extinctions. The positive effects of empirical seasonal structure on network stability vanished when using randomized seasonal structures, suggesting that eco-evolutionary dynamics produce stabilizing seasonal structures. We also show that the effects of seasonal structure on community stability are mainly mediated by changes in network structure and productivity, suggesting that the seasonal structure of a community is an important and yet neglected aspect in the diversity-stability and diversity-productivity debates.

The contribution of mutualistic interactions to functional and phylogenetic diversity.

Reduction of functional diversity (FD) and phylogenetic diversity (PD) likely affects ecosystem functions and reduces the potential of communities to respond to changes, such as climate change. Mutualistic interactions are essential for maintaining diversity, but their role has largely been ignored in conservation planning. We propose using a species' interaction niche - the diversity of its interaction partners - to measure a species' contribution to the maintenance of FD and PD via mutualistic interactions, and thus identify species and interspecific interactions that are particularly important for the conservation of ecosystem functions and evolutionary lineages in ecological communities. Our approach represents a switch in perspective that allows a direct assessment of the importance of mutualistic interactions for the maintenance of biodiversity and ecosystem functioning.

Global plant-frugivore trait matching is shaped by climate and biogeographic history.

Species interactions are influenced by the trait structure of local multi-trophic communities. However, it remains unclear whether mutualistic interactions in particular can drive trait patterns at the global scale, where climatic constraints and biogeographic processes gain importance. Here we evaluate global relationships between traits of frugivorous birds and palms (Arecaceae), and how these relationships are affected, directly or indirectly, by assemblage richness, climate and biogeographic history. We leverage a new and expanded gape size dataset for nearly all avian frugivores, and find a positive relationship between gape size and fruit size, that is, trait matching, which is influenced indirectly by palm richness and climate. We also uncover a latitudinal gradient in trait matching strength, which increases towards the tropics and varies among zoogeographic realms. Taken together, our results suggest trophic interactions have consistent influences on trait structure, but that abiotic, biogeographic and richness effects also play important, though sometimes indirect, roles in shaping the functional biogeography of mutualisms.

Climate change shifts the timing of nutritional flux from aquatic insects.

Climate change can decouple resource supply from consumer demand, with the potential to create phenological mismatches driving negative consequences on fitness. However, the underlying ecological mechanisms of phenological mismatches between consumers and their resources have not been fully explored. Here, we use long-term records of aquatic and terrestrial insect biomass and egg-hatching times of several co-occurring insectivorous species to investigate temporal mismatches between the availability of and demand for nutrients that are essential for offspring development. We found that insects with aquatic larvae reach peak biomass earlier in the season than those with terrestrial larvae and that the relative availability of omega-3 long-chain polyunsaturated fatty acids (n-3 LCPUFAs) to consumers is almost entirely dependent on the phenology of aquatic insect emergence. This is due to the 4- to 34-fold greater n-3 LCPUFA concentration difference in insects emerging from aquatic as opposed to terrestrial habitats. From a long-sampled site (25 years) undergoing minimal land use conversion, we found that both aquatic and terrestrial insect phenologies have advanced substantially faster than those of insectivorous birds, shifting the timing of peak availability of n-3 LCPUFAs for birds during reproduction. For species that require n-3 LCPUFAs directly from diet, highly nutritious aquatic insects cannot simply be replaced by terrestrial insects, creating nutritional phenological mismatches. Our research findings reveal and highlight the increasing necessity of specifically investigating how nutritional phenology, rather than only overall resource availability, is changing for consumers in response to climate change.

A heterothermic spectrum in hummingbirds.

Many endotherms use torpor, saving energy by a controlled reduction of their body temperature and metabolic rate. Some species (e.g. arctic ground squirrels, hummingbirds) enter deep torpor, dropping their body temperature by 23-37°C, while others can only enter shallow torpor (e.g. pigeons, 3-10°C reduction). However, deep torpor in mammals can increase predation risk (unless animals are in burrows or caves), inhibit immune function and result in sleep deprivation, so even for species that can enter deep torpor, facultative shallow torpor might help balance energy savings with these potential costs. Deep torpor occurs in three avian orders, but the trade-offs of deep torpor in birds are unknown. Although the literature hints that some bird species (mousebirds and perhaps hummingbirds) can use both shallow and deep torpor, little empirical evidence of such an avian heterothermy spectrum within species exists. We infrared imaged three hummingbird species that are known to use deep torpor, under natural temperature and light cycles, to test whether they were also capable of shallow torpor. All three species used both deep and shallow torpor, often on the same night. Depending on the species, they used shallow torpor for 5-35% of the night. The presence of a heterothermic spectrum in these bird species indicates a capacity for fine-scale physiological and genetic regulation of avian torpid metabolism.