Barcoding of episodic memories in the hippocampus of a food-caching bird.

The hippocampus is critical for episodic memory. Although hippocampal activity represents place and other behaviorally relevant variables, it is unclear how it encodes numerous memories of specific events in life. To study episodic coding, we leveraged the specialized behavior of chickadees-food-caching birds that form memories at well-defined moments in time whenever they cache food for subsequent retrieval. Our recordings during caching revealed very sparse, transient barcode-like patterns of firing across hippocampal neurons. Each "barcode" uniquely represented a caching event and transiently reactivated during the retrieval of that specific cache. Barcodes co-occurred with the conventional activity of place cells but were uncorrelated even for nearby cache locations that had similar place codes. We propose that animals recall episodic memories by reactivating hippocampal barcodes. Similarly to computer hash codes, these patterns assign unique identifiers to different events and could be a mechanism for rapid formation and storage of many non-interfering memories.

Reef-building corals farm and feed on their photosynthetic symbionts.

Coral reefs are highly diverse ecosystems that thrive in nutrient-poor waters, a phenomenon frequently referred to as the Darwin paradox1. The energy demand of coral animal hosts can often be fully met by the excess production of carbon-rich photosynthates by their algal symbionts2,3. However, the understanding of mechanisms that enable corals to acquire the vital nutrients nitrogen and phosphorus from their symbionts is incomplete4-9. Here we show, through a series of long-term experiments, that the uptake of dissolved inorganic nitrogen and phosphorus by the symbionts alone is sufficient to sustain rapid coral growth. Next, considering the nitrogen and phosphorus budgets of host and symbionts, we identify that these nutrients are gathered through symbiont 'farming' and are translocated to the host by digestion of excess symbiont cells. Finally, we use a large-scale natural experiment in which seabirds fertilize some reefs but not others, to show that the efficient utilization of dissolved inorganic nutrients by symbiotic corals established in our laboratory experiments has the potential to enhance coral growth in the wild at the ecosystem level. Feeding on symbionts enables coral animals to tap into an important nutrient pool and helps to explain the evolutionary and ecological success of symbiotic corals in nutrient-limited waters.

Interhemispheric competition during sleep.

Our understanding of the functions and mechanisms of sleep remains incomplete, reflecting their increasingly evident complexity1-3. Likewise, studies of interhemispheric coordination during sleep4-6 are often hard to connect precisely to known sleep circuits and mechanisms. Here, by recording from the claustra of sleeping bearded dragons (Pogona vitticeps), we show that, although the onsets and offsets of Pogona rapid-eye-movement (REMP) and slow-wave sleep are coordinated bilaterally, these two sleep states differ markedly in their inter-claustral coordination. During slow-wave sleep, the claustra produce sharp-wave ripples independently of one another, showing no coordination. By contrast, during REMP sleep, the potentials produced by the two claustra are precisely coordinated in amplitude and time. These signals, however, are not synchronous: one side leads the other by about 20 ms, with the leading side switching typically once per REMP episode or in between successive episodes. The leading claustrum expresses the stronger activity, suggesting bilateral competition. This competition does not occur directly between the two claustra or telencephalic hemispheres. Rather, it occurs in the midbrain and depends on the integrity of a GABAergic (γ-aminobutyric-acid-producing) nucleus of the isthmic complex, which exists in all vertebrates and is known in birds to underlie bottom-up attention and gaze control. These results reveal that a winner-take-all-type competition exists between the two sides of the brain of Pogona, which originates in the midbrain and has precise consequences for claustrum activity and coordination during REMP sleep.

Logged tropical forests have amplified and diverse ecosystem energetics.

Old-growth tropical forests are widely recognized as being immensely important for their biodiversity and high biomass1. Conversely, logged tropical forests are usually characterized as degraded ecosystems2. However, whether logging results in a degradation in ecosystem functions is less clear: shifts in the strength and resilience of key ecosystem processes in large suites of species have rarely been assessed in an ecologically integrated and quantitative framework. Here we adopt an ecosystem energetics lens to gain new insight into the impacts of tropical forest disturbance on a key integrative aspect of ecological function: food pathways and community structure of birds and mammals. We focus on a gradient spanning old-growth and logged forests and oil palm plantations in Borneo. In logged forest there is a 2.5-fold increase in total resource consumption by both birds and mammals compared to that in old-growth forests, probably driven by greater resource accessibility and vegetation palatability. Most principal energetic pathways maintain high species diversity and redundancy, implying maintained resilience. Conversion of logged forest into oil palm plantation results in the collapse of most energetic pathways. Far from being degraded ecosystems, even heavily logged forests can be vibrant and diverse ecosystems with enhanced levels of ecological function.

Limited potential for bird migration to disperse plants to cooler latitudes.

Climate change is forcing the redistribution of life on Earth at an unprecedented velocity1,2. Migratory birds are thought to help plants to track climate change through long-distance seed dispersal3,4. However, seeds may be consistently dispersed towards cooler or warmer latitudes depending on whether the fruiting period of a plant species coincides with northward or southward migrations. Here we assess the potential of plant communities to keep pace with climate change through long-distance seed dispersal by migratory birds. To do so, we combine phenological and migration information with data on 949 seed-dispersal interactions between 46 bird and 81 plant species from 13 woodland communities across Europe. Most of the plant species (86%) in these communities are dispersed by birds migrating south, whereas only 35% are dispersed by birds migrating north; the latter subset is phylogenetically clustered in lineages that have fruiting periods that overlap with the spring migration. Moreover, the majority of this critical dispersal service northwards is provided by only a few Palaearctic migrant species. The potential of migratory birds to assist a small, non-random sample of plants to track climate change latitudinally is expected to strongly influence the formation of novel plant communities, and thus affect their ecosystem functions and community assembly at higher trophic levels.

Migratory birds modulate niche tradeoffs in rhythm with seasons and life history.

Movement is a key means by which animals cope with variable environments. As they move, animals construct individual niches composed of the environmental conditions they experience. Niche axes may vary over time and covary with one another as animals make tradeoffs between competing needs. Seasonal migration is expected to produce substantial niche variation as animals move to keep pace with major life history phases and fluctuations in environmental conditions. Here, we apply a time-ordered principal component analysis to examine dynamic niche variance and covariance across the annual cycle for four species of migratory crane: common crane (Grus grus, n = 20), demoiselle crane (Anthropoides virgo, n = 66), black-necked crane (Grus nigricollis, n = 9), and white-naped crane (Grus vipio, n = 9). We consider four key niche components known to be important to aspects of crane natural history: enhanced vegetation index (resources availability), temperature (thermoregulation), crop proportion (preferred foraging habitat), and proximity to water (predator avoidance). All species showed a primary seasonal niche "rhythm" that dominated variance in niche components across the annual cycle. Secondary rhythms were linked to major species-specific life history phases (migration, breeding, and nonbreeding) as well as seasonal environmental patterns. Furthermore, we found that cranes' experiences of the environment emerge from time-dynamic tradeoffs among niche components. We suggest that our approach to estimating the environmental niche as a multidimensional and time-dynamical system of tradeoffs improves mechanistic understanding of organism-environment interactions.

Persistent species relationships characterize migrating bird communities across stopover sites and seasons.

Global migrations of diverse animal species often converge along the same routes, bringing together seasonal assemblages of animals that may compete, prey on each other, and share information or pathogens. These interspecific interactions, when energetic demands are high and the time to complete journeys is short, may influence survival, migratory success, stopover ecology, and migratory routes. Numerous accounts suggest that interspecific co-migrations are globally distributed in aerial, aquatic, and terrestrial systems, although the study of migration to date has rarely investigated species interactions among migrating animals. Here, we test the hypothesis that migrating animals are communities engaged in networks of ecological interactions. We leverage over half a million records of 50 bird species from five bird banding sites collected over 8 to 23 y to test for species associations using social network analyses. We find strong support for persistent species relationships across sites and between spring and fall migration. These relationships may be ecologically meaningful: They are often stronger among phylogenetically related species with similar foraging behaviors and nonbreeding ranges even after accounting for the nonsocial contributions to associations, including overlap in migration timing and habitat use. While interspecific interactions could result in costly competition or beneficial information exchange, we find that relationships are largely positive, suggesting limited competitive exclusion at the scale of a banding station during migratory stopovers. Our findings support an understanding of animal migrations that consist of networked communities rather than random assemblages of independently migrating species, encouraging future studies of the nature and consequences of co-migrant interactions.

Significant shifts in latitudinal optima of North American birds.

Changes in climate can alter environmental conditions faster than most species can adapt. A prediction under a warming climate is that species will shift their distributions poleward through time. While many studies focus on range shifts, latitudinal shifts in species' optima can occur without detectable changes in their range. We quantified shifts in latitudinal optima for 209 North American bird species over the last 55 y. The latitudinal optimum (m) for each species in each year was estimated using a bespoke flexible non-linear zero-inflated model of abundance vs. latitude, and the annual shift in m through time was quantified. One-third (70) of the bird species showed a significant shift in their optimum. Overall, mean peak abundances of North American birds have shifted northward, on average, at a rate of 1.5 km per year (±0.58 SE), corresponding to a total distance moved of 82.5 km (±31.9 SE) over the last 55 y. Stronger poleward shifts at the continental scale were linked to key species' traits, including thermal optimum, habitat specialization, and territoriality. Shifts in the western region were larger and less variable than in the eastern region, and they were linked to species' thermal optimum, habitat density preference, and habitat specialization. Individual species' latitudinal shifts were most strongly linked to their estimated thermal optimum, clearly indicating a climate-driven response. Displacement of species from their historically optimal realized niches can have dramatic ecological consequences. Effective conservation must consider within-range abundance shifts. Areas currently deemed "optimal" are unlikely to remain so.

Climate change drives migratory range shift via individual plasticity in shearwaters.

How individual animals respond to climate change is key to whether populations will persist or go extinct. Yet, few studies investigate how changes in individual behavior underpin these population-level phenomena. Shifts in the distributions of migratory animals can occur through adaptation in migratory behaviors, but there is little understanding of how selection and plasticity contribute to population range shift. Here, we use long-term geolocator tracking of Balearic shearwaters (Puffinus mauretanicus) to investigate how year-to-year changes in individual birds' migrations underpin a range shift in the post-breeding migration. We demonstrate a northward shift in the post-breeding range and show that this is brought about by individual plasticity in migratory destination, with individuals migrating further north in response to changes in sea-surface temperature. Furthermore, we find that when individuals migrate further, they return faster, perhaps minimizing delays in return to the breeding area. Birds apparently judge the increased distance that they will need to migrate via memory of the migration route, suggesting that spatial cognitive mechanisms may contribute to this plasticity and the resulting range shift. Our study exemplifies the role that individual behavior plays in populations' responses to environmental change and highlights some of the behavioral mechanisms that might be key to understanding and predicting species persistence in response to climate change.

Altruism and natural selection in a variable environment.

Hamilton's rule provides the cornerstone for our understanding of the evolution of all forms of social behavior, from altruism to spite, across all organisms, from viruses to humans. In contrast to the standard prediction from Hamilton's rule, recent studies have suggested that altruistic helping can be favored even if it does not benefit relatives, as long as it decreases the environmentally induced variance of their reproductive success ("altruistic bet-hedging"). However, previous predictions both rely on an approximation and focus on variance-reducing helping behaviors. We derived a version of Hamilton's rule that fully captures environmental variability. This shows that decreasing (or increasing) the variance in the absolute reproductive success of relatives does not have a consistent effect-it can either favor or disfavor the evolution of helping. We then empirically quantified the effect of helping on the variance in reproductive success across 15 species of cooperatively breeding birds. We found that a) helping did not consistently decrease the variance of reproductive success and often increased it, and b) the mean benefits of helping across environments consistently outweighed other variability components of reproductive success. Altogether, our theoretical and empirical results suggest that the effects of helping on the variability components of reproductive success have not played a consistent or strong role in favoring helping.

Predicting resilience of migratory birds to environmental change.

The pace and scale of environmental change represent major challenges to many organisms. Animals that move long distances, such as migratory birds, are especially vulnerable to change since they need chains of intact habitat along their migratory routes. Estimating the resilience of such species to environmental changes assists in targeting conservation efforts. We developed a migration modeling framework to predict past (1960s), present (2010s), and future (2060s) optimal migration strategies across five shorebird species (Scolopacidae) within the East Asian-Australasian Flyway, which has seen major habitat deterioration and loss over the last century, and compared these predictions to empirical tracks from the present. Our model captured the migration strategies of the five species and identified the changes in migrations needed to respond to habitat deterioration and climate change. Notably, the larger species, with single or few major stopover sites, need to establish new migration routes and strategies, while smaller species can buffer habitat loss by redistributing their stopover areas to novel or less-used sites. Comparing model predictions with empirical tracks also indicates that larger species with the stronger need for adaptations continue to migrate closer to the optimal routes of the past, before habitat deterioration accelerated. Our study not only quantifies the vulnerability of species in the face of global change but also explicitly reveals the extent of adaptations required to sustain their migrations. This modeling framework provides a tool for conservation planning that can accommodate the future needs of migratory species.

Extreme elevational migration spurred cryptic speciation in giant hummingbirds.

The ecoevolutionary drivers of species niche expansion or contraction are critical for biodiversity but challenging to infer. Niche expansion may be promoted by local adaptation or constrained by physiological performance trade-offs. For birds, evolutionary shifts in migratory behavior permit the broadening of the climatic niche by expansion into varied, seasonal environments. Broader niches can be short-lived if diversifying selection and geography promote speciation and niche subdivision across climatic gradients. To illuminate niche breadth dynamics, we can ask how "outlier" species defy constraints. Of the 363 hummingbird species, the giant hummingbird (Patagona gigas) has the broadest climatic niche by a large margin. To test the roles of migratory behavior, performance trade-offs, and genetic structure in maintaining its exceptional niche breadth, we studied its movements, respiratory traits, and population genomics. Satellite and light-level geolocator tracks revealed an >8,300-km loop migration over the Central Andean Plateau. This migration included a 3-wk, ~4,100-m ascent punctuated by upward bursts and pauses, resembling the acclimatization routines of human mountain climbers, and accompanied by surging blood-hemoglobin concentrations. Extreme migration was accompanied by deep genomic divergence from high-elevation resident populations, with decisive postzygotic barriers to gene flow. The two forms occur side-by-side but differ almost imperceptibly in size, plumage, and respiratory traits. The high-elevation resident taxon is the world's largest hummingbird, a previously undiscovered species that we describe and name here. The giant hummingbirds demonstrate evolutionary limits on niche breadth: when the ancestral niche expanded due to evolution (or loss) of an extreme migratory behavior, speciation followed.

It pays to follow the leader: Metabolic cost of flight is lower for trailing birds in small groups.

Many bird species commonly aggregate in flocks for reasons ranging from predator defense to navigation. Available evidence suggests that certain types of flocks-the V and echelon formations of large birds-may provide a benefit that reduces the aerodynamic cost of flight, whereas cluster flocks typical of smaller birds may increase flight costs. However, metabolic flight costs have not been directly measured in any of these group flight contexts [Zhang and Lauder, J. Exp. Biol. 226, jeb245617 (2023)]. Here, we measured the energetic benefits of flight in small groups of two or three birds and the requirements for realizing those benefits, using metabolic energy expenditure and flight position measurements from European Starlings flying in a wind tunnel. The starlings continuously varied their relative position during flights but adopted a V formation motif on average, with a modal spanwise and streamwise spacing of [0.81, 0.91] wingspans. As measured via CO2 production, flight costs for follower birds were significantly reduced compared to their individual solo flight benchmarks. However, followers with more positional variability with respect to leaders did less well, even increasing their costs above solo flight. Thus, we directly demonstrate energetic costs and benefits for group flight followers in an experimental context amenable to further investigation of the underlying aerodynamics, wake interactions, and bird characteristics that produce these metabolic effects.

Albatrosses employ orientation and routing strategies similar to yacht racers.

The way goal-oriented birds adjust their travel direction and route in response to wind significantly affects their travel costs. This is expected to be particularly pronounced in pelagic seabirds, which utilize a wind-dependent flight style called dynamic soaring. Dynamic soaring seabirds in situations without a definite goal, e.g. searching for prey, are known to preferentially fly with crosswinds or quartering-tailwinds to increase the speed and search area, and reduce travel costs. However, little is known about their reaction to wind when heading to a definite goal, such as homing. Homing tracks of wandering albatrosses (Diomedea exulans) vary from beelines to zigzags, which are similar to those of sailboats. Here, given that both albatrosses and sailboats travel slower in headwinds and tailwinds, we tested whether the time-minimizing strategies used by yacht racers can be compared to the locomotion patterns of wandering albatrosses. We predicted that when the goal is located upwind or downwind, albatrosses should deviate their travel directions from the goal on the mesoscale and increase the number of turns on the macroscale. Both hypotheses were supported by track data from albatrosses and racing yachts in the Southern Ocean confirming that albatrosses qualitatively employ the same strategy as yacht racers. Nevertheless, albatrosses did not strictly minimize their travel time, likely making their flight robust against wind fluctuations to reduce flight costs. Our study provides empirical evidence of tacking in albatrosses and demonstrates that man-made movement strategies provide a new perspective on the laws underlying wildlife movement.

Shifting fire regimes cause continent-wide transformation of threatened species habitat.

Human actions are causing widespread increases in fire size, frequency, and severity in diverse ecosystems globally. This alteration of fire regimes is considered a threat to numerous animal species, but empirical evidence of how fire regimes are shifting within both threatened species' ranges and protected areas is scarce, particularly at large spatial and temporal scales. We used a big data approach to quantify multidecadal changes in fire regimes in southern Australia from 1980 to 2021, spanning 415 reserves (21.5 million ha) and 129 threatened species' ranges including birds, mammals, reptiles, invertebrates, and frogs. Most reserves and threatened species' ranges within the region have experienced declines in unburnt vegetation (≥30 y without fire), increases in recently burnt vegetation (≤5 y since fire), and increases in fire frequency. The mean percentage of unburnt vegetation within reserves declined from 61 to 36% (1980 to 2021), whereas the mean percentage of recently burnt vegetation increased from 20 to 35%, and mean fire frequency increased by 32%, with the latter two trends primarily driven by the record-breaking 2019 to 2020 fire season. The strongest changes occurred for high-elevation threatened species, and reserves of high elevation, high productivity, and strong rainfall decline, particularly in the southeast of the continent. Our results provide evidence for the widely held but poorly tested assumption that threatened species are experiencing widespread declines in unburnt habitat and increases in fire frequency. This underscores the imperative for developing management strategies that conserve fire-threatened species in an increasingly fiery future.

The evolution of sex roles: The importance of ecology and social environment.

Males and females often have different roles in reproduction, although the origin of these differences has remained controversial. Explaining the enigmatic reversed sex roles where males sacrifice their mating potential and provide full parental care is a particularly long-standing challenge in evolutionary biology. While most studies focused on ecological factors as the drivers of sex roles, recent research highlights the significance of social factors such as the adult sex ratio. To disentangle these propositions, here, we investigate the additive and interactive effects of several ecological and social factors on sex role variation using shorebirds (sandpipers, plovers, and allies) as model organisms that provide the full spectrum of sex role variation including some of the best-known examples of sex-role reversal. Our results consistently show that social factors play a prominent role in driving sex roles. Importantly, we show that reversed sex roles are associated with both male-skewed adult sex ratios and high breeding densities. Furthermore, phylogenetic path analyses provide general support for sex ratios driving sex role variations rather than being a consequence of sex roles. Together, these important results open future research directions by showing that different mating opportunities of males and females play a major role in generating the evolutionary diversity of sex roles, mating system, and parental care.

Sensory pollutants alter bird phenology and fitness across a continent.

Expansion of anthropogenic noise and night lighting across our planet1,2 is of increasing conservation concern3-6. Despite growing knowledge of physiological and behavioural responses to these stimuli from single-species and local-scale studies, whether these pollutants affect fitness is less clear, as is how and why species vary in their sensitivity to these anthropic stressors. Here we leverage a large citizen science dataset paired with high-resolution noise and light data from across the contiguous United States to assess how these stimuli affect reproductive success in 142 bird species. We find responses to both sensory pollutants linked to the functional traits and habitat affiliations of species. For example, overall nest success was negatively correlated with noise among birds in closed environments. Species-specific changes in reproductive timing and hatching success in response to noise exposure were explained by vocalization frequency, nesting location and diet. Additionally, increased light-gathering ability of species' eyes was associated with stronger advancements in reproductive timing in response to light exposure, potentially creating phenological mismatches7. Unexpectedly, better light-gathering ability was linked to reduced clutch failure and increased overall nest success in response to light exposure, raising important questions about how responses to sensory pollutants counteract or exacerbate responses to other aspects of global change, such as climate warming. These findings demonstrate that anthropogenic noise and light can substantially affect breeding bird phenology and fitness, and underscore the need to consider sensory pollutants alongside traditional dimensions of the environment that typically inform biodiversity conservation.

Ecological barriers mediate spatiotemporal shifts of bird communities at a continental scale.

Species' range shifts and local extinctions caused by climate change lead to community composition changes. At large spatial scales, ecological barriers, such as biome boundaries, coastlines, and elevation, can influence a community's ability to shift in response to climate change. Yet, ecological barriers are rarely considered in climate change studies, potentially hindering predictions of biodiversity shifts. We used data from two consecutive European breeding bird atlases to calculate the geographic distance and direction between communities in the 1980s and their compositional best match in the 2010s and modeled their response to barriers. The ecological barriers affected both the distance and direction of bird community composition shifts, with coastlines and elevation having the strongest influence. Our results underscore the relevance of combining ecological barriers and community shift projections for identifying the forces hindering community adjustments under global change. Notably, due to (macro)ecological barriers, communities are not able to track their climatic niches, which may lead to drastic changes, and potential losses, in community compositions in the future.

Space weather disrupts nocturnal bird migration.

Space weather, including solar storms, can impact Earth by disturbing the geomagnetic field. Despite the known dependence of birds and other animals on geomagnetic cues for successful seasonal migrations, the potential effects of space weather on organisms that use Earth's magnetic field for navigation have received little study. We tested whether space weather geomagnetic disturbances are associated with disruptions to bird migration at a macroecological scale. We leveraged long-term radar data to characterize the nightly migration dynamics of the nocturnally migrating North American avifauna over 22 y. We then used concurrent magnetometer data to develop a local magnetic disturbance index associated with each radar station (ΔBmax), facilitating spatiotemporally explicit analyses of the relationship between migration and geomagnetic disturbance. After controlling for effects of atmospheric weather and spatiotemporal patterns, we found a 9 to 17% decrease in migration intensity in both spring and fall during severe space weather events. During fall migration, we also found evidence for decreases in effort flying against the wind, which may represent a depression of active navigation such that birds drift more with the wind during geomagnetic disturbances. Effort flying against the wind in the fall was most reduced under both overcast conditions and high geomagnetic disturbance, suggesting that a combination of obscured celestial cues and magnetic disturbance may disrupt navigation. Collectively, our results provide evidence for community-wide avifaunal responses to geomagnetic disturbances driven by space weather during nocturnal migration.

Albatross movement suggests sensitivity to infrasound cues at sea.

The ways in which seabirds navigate over very large spatial scales remain poorly understood. While olfactory and visual information can provide guidance over short distances, their range is often limited to 100s km, far below the navigational capacity of wide-ranging animals such as albatrosses. Infrasound is a form of low-frequency sound that propagates for 1,000s km in the atmosphere. In marine habitats, its association with storms and ocean surface waves could in effect make it a useful cue for anticipating environmental conditions that favor or hinder flight or be associated with profitable foraging patches. However, behavioral responses of wild birds to infrasound remain untested. Here, we explored whether wandering albatrosses, Diomedea exulans, respond to microbarom infrasound at sea. We used Global Positioning System tracks of 89 free-ranging albatrosses in combination with acoustic modeling to investigate whether albatrosses preferentially orientate toward areas of 'loud' microbarom infrasound on their foraging trips. We found that in addition to responding to winds encountered in situ, albatrosses moved toward source regions associated with higher sound pressure levels. These findings suggest that albatrosses may be responding to long-range infrasonic cues. As albatrosses depend on winds and waves for soaring flight, infrasonic cues may help albatrosses to identify environmental conditions that allow them to energetically optimize flight over long distances. Our results shed light on one of the great unresolved mysteries in nature, navigation in seemingly featureless ocean environments.