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.

Birds advancing lay dates with warming springs face greater risk of chick mortality.

In response to a warming planet with earlier springs, migratory animals are adjusting the timing of essential life stages. Although these adjustments may be essential for keeping pace with resource phenology, they may prove insufficient, as evidenced by population declines in many species. However, even when species can match the tempo of climate change, other consequences may emerge when exposed to novel conditions earlier in the year. Here, using three long-term datasets on bird reproduction, daily insect availability, and weather, we investigated the complex mechanisms affecting reproductive success in an aerial insectivore, the tree swallow (Tachycineta bicolor). By examining breeding records over nearly half a century, we discovered that tree swallows have continuously advanced their egg laying by ∼3 d per decade. However, earlier-hatching offspring are now exposed to inclement weather events twice as often as they were in the 1970s. Our long-term daily insect biomass dataset shows no long-term trends over 25 y but precipitous drops in flying insect numbers on days with low ambient temperatures. Insect availability has a considerable impact on chick survival: Even a single inclement weather event can reduce offspring survival by >50%. Our results highlight the multifaceted threats that climate change poses on migrating species. The decoupling between cold snap occurrence and generally warming spring temperatures can affect reproductive success and threaten long-term persistence of populations. Understanding the exact mechanisms that endanger aerial insectivores is especially timely because this guild is experiencing the steepest and most widespread declines across North America and Europe.

The evolutionary ecology of fatty-acid variation: Implications for consumer adaptation and diversification.

The nutritional diversity of resources can affect the adaptive evolution of consumer metabolism and consumer diversification. The omega-3 long-chain polyunsaturated fatty acids eicosapentaenoic acid (EPA; 20:5n-3) and docosahexaenoic acid (DHA; 22:6n-3) have a high potential to affect consumer fitness, through their widespread effects on reproduction, growth and survival. However, few studies consider the evolution of fatty acid metabolism within an ecological context. In this review, we first document the extensive diversity in both primary producer and consumer fatty acid distributions amongst major ecosystems, between habitats and amongst species within habitats. We highlight some of the key nutritional contrasts that can shape behavioural and/or metabolic adaptation in consumers, discussing how consumers can evolve in response to the spatial, seasonal and community-level variation of resource quality. We propose a hierarchical trait-based approach for studying the evolution of consumers' metabolic networks and review the evolutionary genetic mechanisms underpinning consumer adaptation to EPA and DHA distributions. In doing so, we consider how the metabolic traits of consumers are hierarchically structured, from cell membrane function to maternal investment, and have strongly environment-dependent expression. Finally, we conclude with an outlook on how studying the metabolic adaptation of consumers within the context of nutritional landscapes can open up new opportunities for understanding evolutionary diversification.

Emergent Freshwater Insects Serve as Subsidies of Methylmercury and Beneficial Fatty Acids for Riparian Predators Across an Agricultural Gradient.

Aquatic-to-terrestrial subsidies have the potential to provide riparian consumers with benefits in terms of physiologically important organic compounds like omega-3 long-chain polyunsaturated fatty acids (n-3 LCPUFAs). However, they also have a "dark side" in the form of exposure to toxicants such as mercury. Human land use intensity may also determine whether subsidies provide benefits or come at a cost for riparian predators. We sampled insects as well as Eastern Phoebe (Sayornis phoebe) chicks in 2015-2016 within the southern Finger Lakes region to understand how food quality, in terms of n-3 LCPUFAs and methylmercury (MeHg), of emergent freshwater insects compared with that of terrestrial insects and how land use affected the quality of prey, predator diet composition, and MeHg exposure. Across the landscape, freshwater insects had a significantly higher percentage of the n-3 LCPUFA eicosapentaenoic acid (EPA) compared to terrestrial insects and contained significantly more MeHg than terrestrial insects did. In spite of differences in MeHg concentrations between aquatic and terrestrial insects, chick MeHg concentrations were not related to diet composition. Instead, chick MeHg concentrations increased with several metrics of human land use intensity, including percent agriculture. Our findings suggest that freshwater subsidies provide predators with both risks and benefits, but that predator MeHg exposure can vary with human land use intensity.

Reconstructing avian mercury concentrations through time using museum specimens from New York State.

We examined how variation in MeHg concentrations through time is reflected in birds, a taxon commonly used as a biological indicator of ecosystem health. Using museum specimens collected from 1880 to 2016, we measured feather MeHg concentrations in six species of birds that breed in New York State and have distinct dietary and habitat preferences. We predicted that MeHg concentrations in feathers would mirror Hg emission patterns in New York State and increase through time until 1980 then decrease thereafter in response to increased regulation of anthropogenic Hg emissions. We found that MeHg concentrations increased with δ15N, and that MeHg feather concentrations for some individuals from four of the six species examined exceeded concentrations known to cause negative sublethal effects in birds. In contrast to our prediction, MeHg concentrations in feathers did not parallel global or local Hg emissions through time and varied by species, even after controlling for possible changes in diet and habitat. MeHg concentrations varied substantially within species and individual specimens, suggesting that high within-individual variation in feather MeHg concentrations caused by spatiotemporal variation in molt, environmental Hg exposure, or mobility decoupling Hg uptake from breeding sites, may obscure trends in MeHg through time. Our study provides a unique assessment of feather MeHg in six species not typically analyzed using this retrospective approach.

Omega-3 long-chain polyunsaturated fatty acids support aerial insectivore performance more than food quantity.

Once-abundant aerial insectivores, such as the Tree Swallow (Tachycineta bicolor), have declined steadily in the past several decades, making it imperative to understand all aspects of their ecology. Aerial insectivores forage on a mixture of aquatic and terrestrial insects that differ in fatty acid composition, specifically long-chain omega-3 polyunsaturated fatty acid (LCPUFA) content. Aquatic insects contain high levels of both LCPUFA and their precursor omega-3 PUFA, alpha-linolenic acid (ALA), whereas terrestrial insects contain much lower levels of both. We manipulated both the quantity and quality of food for Tree Swallow chicks in a full factorial design. Diets were either high-LCPUFA or low in LCPUFA but high in ALA, allowing us to separate the effects of direct LCPUFA in diet from the ability of Tree Swallows to convert their precursor, ALA, into LCPUFA. We found that fatty acid composition was more important for Tree Swallow chick performance than food quantity. On high-LCPUFA diets, chicks grew faster, were in better condition, and had greater immunocompetence and lower basal metabolic rates compared with chicks on both low LCPUFA diets. Increasing the quantity of high-LCPUFA diets resulted in improvements to all metrics of performance while increasing the quantity of low-LCPUFA diets only resulted in greater immunocompetence and lower metabolic rates. Chicks preferentially retained LCPUFA in brain and muscle when both food quantity and LCPUFA were limited. Our work suggests that fatty acid composition is an important dimension of aerial insectivore nutritional ecology and reinforces the importance of high-quality aquatic habitat for these declining birds.

Conversion efficiency of α-linolenic acid to omega-3 highly unsaturated fatty acids in aerial insectivore chicks.

Food availability and quality are both critical for growing young animals. In nature, swallows (Tachycineta bicolor) and other aerial insectivores feed on both aquatic insects, which are rich in omega-3 highly unsaturated fatty acids (HUFAs), and terrestrial insects, which contain considerably lower amounts of omega-3 HUFAs. Carnivorous mammals and fishes must obtain omega-3 HUFAs from their diet, as they have lost the capacity to convert the precursor omega-3 α-linolenic acid (ALA) into omega-3 HUFAs. Thus, the relative value of aquatic versus terrestrial insects depends not only on the fatty acid composition of the prey but also on the capacity of consumers to convert ALA into omega-3 HUFAs. We used a combination of stable-isotope-labeled fatty acid tracers to ask whether, and how efficiently, tree swallows can deposit newly synthesized omega-3 HUFAs into tissue. Our data show for the first time that tree swallows can convert ALA into omega-3 HUFAs deposited in liver and skeletal muscle. However, high tree swallow demand for omega-3 HUFAs combined with low ALA availability in natural terrestrial foods may strain their modest conversion ability. This suggests that while tree swallows can synthesize omega-3 HUFAs de novo, omega-3 HUFAs are ecologically essential nutrients in natural systems. Our findings thus provide mechanistic support for our previous findings and the importance of omega-3 HUFA-rich aquatic insects for tree swallows and most likely other aerial insectivores with similar niches.

Export of dietary lipids via emergent insects from eutrophic fishponds.

Fishponds, despite being globally abundant, have mainly been considered as food production sites and have received little scientific attention in terms of their ecological contributions to the surrounding terrestrial environment. Emergent insects from fishponds may be important contributors of lipids and essential fatty acids to terrestrial ecosystems. In this field study, we investigated nine eutrophic fishponds in Austria from June to September 2020 to examine how Chlorophyll-a concentrations affect the biomass of emergent insect taxa (i.e., quantity of dietary subsidies; n = 108) and their total lipid and long-chain polyunsaturated fatty acid content (LC-PUFA, i.e., quality of dietary subsidies; n = 94). Chironomidae and Chaoboridae were the most abundant emergent insect taxa, followed by Trichoptera, Ephemeroptera, and Odonata. A total of 1068 kg of emergent insect dry mass were exported from these ponds (65.3 hectares). Chironomidae alone exported 103 kg of total lipids and 9.4 kg of omega-3 PUFA. Increasing Chl-a concentrations were associated with decreasing biomass export and a decrease in total lipid and LC-PUFA export via emergent Chironomidae. The PUFA composition of emergent insect taxa differed significantly from dietary algae, suggesting selective PUFA retention by insects. The export of insect biomass from these eutrophic carp ponds was higher than that previously reported from oligotrophic lakes. However, lower biomass and diversity are exported from the fishponds compared to managed ponds. Nonetheless, our data suggest that fishponds provide crucial ecosystem services to terrestrial consumers by contributing essential dietary nutrients to consumer diets via emergent insects. Supplementary Information: The online version contains supplementary material available at 10.1007/s10750-022-05040-2.

The role of vital dietary biomolecules in eco-evo-devo dynamics.

The physiological dependence of animals on dietary intake of vitamins, amino acids, and fatty acids is ubiquitous. Sharp differences in the availability of these vital dietary biomolecules among different resources mean that consumers must adopt a range of strategies to meet their physiological needs. We review the emerging work on omega-3 long-chain polyunsaturated fatty acids, focusing predominantly on predator-prey interactions, to illustrate that trade-off between capacities to consume resources rich in vital biomolecules and internal synthesis capacity drives differences in phenotype and fitness of consumers. This can then feedback to impact ecosystem functioning. We outline how focus on vital dietary biomolecules in eco-eco-devo dynamics can improve our understanding of anthropogenic changes across multiple levels of biological organization.

Climate change creates nutritional phenological mismatches.

Climate change is creating phenological mismatches between consumers and their resources. However, while the importance of nutritional quality in ecological interactions is widely appreciated, most studies of phenological mismatch focus on energy content alone. We argue that mismatches in terms of phenology and nutrition will increase with climate change.

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 songbird adjusts its heart rate and body temperature in response to season and fluctuating daily conditions.

In a seasonal world, organisms are continuously adjusting physiological processes relative to local environmental conditions. Owing to their limited heat and fat storage capacities, small animals, such as songbirds, must rapidly modulate their metabolism in response to weather extremes and changing seasons to ensure survival. As a consequence of previous technical limitations, most of our existing knowledge about how animals respond to changing environmental conditions comes from laboratory studies or field studies over short temporal scales. Here, we expanded beyond previous studies by outfitting 71 free-ranging Eurasian blackbirds (Turdus merula) with novel heart rate and body temperature loggers coupled with radio transmitters, and followed individuals in the wild from autumn to spring. Across seasons, blackbirds thermoconformed at night, i.e. their body temperature decreased with decreasing ambient temperature, but not so during daytime. By contrast, during all seasons blackbirds increased their heart rate when ambient temperatures became colder. However, the temperature setpoint at which heart rate was increased differed between seasons and between day and night. In our study, blackbirds showed an overall seasonal reduction in mean heart rate of 108 beats min-1 (21%) as well as a 1.2°C decrease in nighttime body temperature. Episodes of hypometabolism during cold periods likely allow the birds to save energy and, thus, help offset the increased energetic costs during the winter when also confronted with lower resource availability. Our data highlight that, similar to larger non-hibernating mammals and birds, small passerine birds such as Eurasian blackbirds not only adjust their heart rate and body temperature on daily timescales, but also exhibit pronounced seasonal changes in both that are modulated by local environmental conditions such as temperature. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

Stable isotopes of fatty acids: current and future perspectives for advancing trophic ecology.

To understand consumer dietary requirements and resource use across ecosystems, researchers have employed a variety of methods, including bulk stable isotope and fatty acid composition analyses. Compound-specific stable isotope analysis (CSIA) of fatty acids combines both of these tools into an even more powerful method with the capacity to broaden our understanding of food web ecology and nutritional dynamics. Here, we provide an overview of the potential that CSIA studies hold and their constraints. We first review the use of fatty acid CSIA in ecology at the natural abundance level as well as enriched physiological tracers, and highlight the unique insights that CSIA of fatty acids can provide. Next, we evaluate methodological best practices when generating and interpreting CSIA data. We then introduce three cutting-edge methods: hydrogen CSIA of fatty acids, and fatty acid isotopomer and isotopologue analyses, which are not yet widely used in ecological studies, but hold the potential to address some of the limitations of current techniques. Finally, we address future priorities in the field of CSIA including: generating more data across a wider range of taxa; lowering costs and increasing laboratory availability; working across disciplinary and methodological boundaries; and combining approaches to answer macroevolutionary questions. This article is part of the theme issue 'The next horizons for lipids as 'trophic biomarkers': evidence and significance of consumer modification of dietary fatty acids'.