The role of neophobia in a pioneer olfactory enrichment for amazons, macaws, and toucans / El papel de la neofobia en un enriquecimiento olfativo pionero para guacamayos, loros y tucanes

Abstract Introduction: Despite sensory enrichment being critical for ensuring the well-being of captive wild animals, smells are not being included in enrichment protocols for birds. For this group, neophobia can be a problem when it comes to implementing new enrichment devices. Objective: To explore how participation in an olfactory enrichment and latency times varies between bird taxonomic groups (Amazona spp. / Ara spp. / Ramphastos spp.). Methods: We exposed 257 birds to a scent enrichment, and we recorded which individuals engaged with it and the time they took to interact with it. Results: We discovered that participation by toucans in the enrichment was higher compared to amazons and macaws. Furthermore, latency time to interact with the enrichment was higher in amazons that in the other species. Our findings could suggest that toucans are neophilic species which could benefit from higher exploration rates. Amazons on the contrary seem to be particularly neophobic, possibly because of their less opportunistic feeding habits compared to toucans and their higher vulnerability to predation compared to macaws. Conclusion: These results point out that toucans would be more inclined to engage in environmental enrichments, while a more natural design using smells inside familiar objects could be a more successful enrichment for psittacids.

Resumen Introducción: A pesar de que el enriquecimiento sensorial es fundamental para garantizar el bienestar de los animales silvestres en cautiverio, los olores no son incluidos de forma rutinaria en los protocolos de enriquecimiento para aves. Además, en el caso de estos animales, la neofobia puede ser un problema a la hora de implementar nuevos dispositivos de enriquecimiento. Objetivo: Explorar cómo varía la participación y la latencia en la interacción con un enriquecimiento olfativo entre grupos taxonómicos de aves (Amazona spp. / Ara spp. / Ramphastos spp.). Métodos: Expusimos a 257 aves a un enriquecimiento olfativo y registramos qué individuos participaron y el tiempo que tardaron en interactuar con él. Resultados: La participación en el enriquecimiento fue mayor en los tucanes en comparación con las amazonas y los guacamayos. Además, el tiempo de latencia para interactuar con el enriquecimiento fue mayor en las amazonas que en las otras especies. Nuestros hallazgos sugieren que los tucanes son especies neofílicas que podrían beneficiarse de tasas de exploración más altas. Por otro lado, las amazonas parecen ser particularmente neofóbicas, posiblemente debido a sus hábitos alimenticios menos oportunistas en comparación con los tucanes y a su mayor vulnerabilidad a la depredación en comparación con los guacamayos. Conclusión: Estos resultados señalan que los tucanes serían más proclives a participar en enriquecimientos ambientales, mientras que un diseño que utilice olores dentro de objetos más naturales o familiares podría ser más exitoso para las psitácidas.

Central China as LGM plant refugia: Insights from biome reconstruction for palaeoclimate information.

The demonstration of survival of forest stands in relatively stable refugia during cold glacial stages has offered an increased understanding of the response of vegetation to climate change, but also provides insight into considerations for the conversation of biodiversity hotspots. However, refugia studies in China remain in question due to the lack of plant macrofossils, especially those of endemic and relict species. Palynology, while more broad brush, provides a method for exploring whether refugia occur, and can provide some details of palaeovegetation composition and temporal dynamics. Here, three pollen records derived from subalpine wetlands in central China, spanning the Last Glacial Maximum (LGM), have been coupled with biome and mean annual precipitation (MAP) reconstructions to identify the presence of trees that endured cold climate. The results indicated that some forest, including temperate deciduous broadleaf forest and cool mixed forest, survived the LGM at the three locations, and was thus at odds with the hypothesis that forests were replaced by herbs and grasses in central China at that time. Refugia favored by protection from cold air drainage and the availability of adequate water can explain the survival of the trees during otherwise harsh episodes. Our findings are consistent with other records from central China that argue for tree dominated refugia during the LGM.

Predictable patterns within the kelp forest can indirectly create temporary refugia from ocean acidification.

Kelps are recognized for providing many ecosystem services in coastal areas and considered in ocean acidification (OA) mitigation. However, assessing OA modification requires an understanding of the multiple parameters involved in carbonate chemistry, especially in highly dynamic systems. We studied the effects of sugar kelp (Saccharina latissima) on an experimental farm at the north end of Hood Canal, Washington-a low retentive coastal system. In this field mesocosm study, two oyster species (Magallana gigas, Ostrea lurida) were exposed at locations in the mid, edge, and outside the kelp array. The Hood Head Sugar Kelp Farm Model outputs were used to identify dominating factors in spatial and temporal kelp dynamics, while wavelet spectrum analyses helped in understanding predictability patterns. This was linked to the measured biological responses (dissolution, growth, isotopes) of the exposed organisms. Positioned in an area of high (sub)-diel tidal fluxes with low retention potential, there were no measurable alterations of the seawater pH at the study site, demonstrating that the kelp array could not induce a direct mitigating effect against OA. However, beneficial responses in calcifiers were still observed, which are linked to two causes: increased pH predictability and improved provisioning through kelp-derived particulate organic resource utilization and as such, kelp improved habitat suitability and indirectly created refugia against OA. This study can serve as an analogue for many coastal bay habitats where prevailing physical forcing drives chemical changes. Future macrophyte studies that investigate OA mitigating effects should focus also on the importance of predictability patterns, which can additionally improve the conditions for marine calcifiers and ecosystem services vulnerable to or compromised by OA, including aquaculture sustainability.

Hotspot shelters stimulate frog resistance to chytridiomycosis.

Many threats to biodiversity cannot be eliminated; for example, invasive pathogens may be ubiquitous. Chytridiomycosis is a fungal disease that has spread worldwide, driving at least 90 amphibian species to extinction, and severely affecting hundreds of others1-4. Once the disease spreads to a new environment, it is likely to become a permanent part of that ecosystem. To enable coexistence with chytridiomycosis in the field, we devised an intervention that exploits host defences and pathogen vulnerabilities. Here we show that sunlight-heated artificial refugia attract endangered frogs and enable body temperatures high enough to clear infections, and that having recovered in this way, frogs are subsequently resistant to chytridiomycosis even under cool conditions that are optimal for fungal growth. Our results provide a simple, inexpensive and widely applicable strategy to buffer frogs against chytridiomycosis in nature. The refugia are immediately useful for the endangered species we tested and will have broader utility for amphibian species with similar ecologies. Furthermore, our concept could be applied to other wildlife diseases in which differences in host and pathogen physiologies can be exploited. The refugia are made from cheap and readily available materials and therefore could be rapidly adopted by wildlife managers and the public. In summary, habitat protection alone cannot protect species that are affected by invasive diseases, but simple manipulations to microhabitat structure could spell the difference between the extinction and the persistence of endangered amphibians.

Does coevolution in refugia drive mimicry in bumble bees? Insights from a South Asian mimicry group.

Müllerian mimicry was proposed to be an example of a coevolved mutualism promoted by population isolation in glacial refugia. This, however, has not been well supported in butterfly models. Here, we use genomic data to test this theory while examining the population genetics behind mimetic diversification in a pair of co-mimetic bumble bees, Bombus breviceps Smith and Bombus trifasciatus Smith. In both lineages, populations were structured by geography but not as much by color pattern, suggesting sharing of color alleles across regions of restricted gene flow and formation of mimicry complexes in the absence of genetic differentiation. Demographic analyses showed mismatches between historical effective population size changes and glacial cycles, and niche modeling revealed only mild habitat retraction during glaciation. Moreover, mimetic subpopulations of the same color form in the two lineages only in some cases exhibit similar population history and genetic divergence. Therefore, the current study supports a more complex history in this comimicry than a simple refugium-coevolution model.

Assessing phenotypic variation and plasticity of endemic gastropods from thermal water refugia using complex morphometric techniques: A case study of Lake Pețea melanopsids.

Understanding the underlying reasons for phenotypic plasticity and resulting morphological disparity is one of the key topics of evolutionary research. The phenotypic plasticity of extant and fossil melanopsids has been widely documented. Yet millennial-resolution, well-dated records from small aquatic habitats harboring endemics are scarce. The thermal spring-fed Lake Pețea is an ice age refugia harboring a unique endemic warm-water fauna. Subfossil melanopsids display incredible morphological variability from smooth to keeled, elongated to ribbed, shouldered forms. Numerous morphotypes have been considered as individual taxa with a fluent succession from the smooth elongated to the ribbed, shouldered types. This study presents an extensive morphometric analysis of subfossil melanopsids (ca. 3500 specimens) derived from stratified samples with an independent chronology. The aim was to separate morphotypes for investigations of temporal morphological disparity. Our results challenge the widely accepted hypothesis that proposes the evolution of shouldered, compressed, ribbed shells through a two-step process from smooth elongated spindle-shaped shells. Instead, it suggests that the subfossil shells belong to two distinct taxa present throughout the available stratigraphic data. The main components of shape variation, shape globularity, and shell coiling seem allometry-related. Ribs, striation, and keels appear randomly. High-spired spindle-shaped forms were considered to represent specimens of Microcolpia daudebartii hazayi. Bulkier low-spired and shouldered specimens represent phenotypes of Mi. parreyssii parreyssii. The collective and random distribution of morphotypes from the early stages of the lake's history also refutes the idea of a continuous transformation of the elongated forms into compressed, shouldered ones. Rather points to multiple events and environmental stimuli triggering development. Melanopsids appear in Late Glacial horizons, with Theodoxus prevostianus preferring temperatures above 23°C which may indicate the subordinate presence of hot water microhabitats in cooler waters.

Hot spring oases in the periglacial desert as the Last Glacial Maximum refugia for temperate trees in Central Europe.

Northern glacial refugia are a hotly debated concept. The idea that many temperate organisms survived the Last Glacial Maximum (LGM; ~26.5 to 19 thousand years) in several sites across central and northern Europe stems from phylogeographic analyses, yet direct fossil evidence has thus far been missing. Here, we present the first unequivocal proof that thermophilous trees such as oak (Quercus), linden (Tilia), and common ash (Fraxinus excelsior) survived the LGM in Central Europe. The persistence of the refugium was promoted by a steady influx of hydrothermal waters that locally maintained a humid and warm microclimate. We reconstructed the geological and palaeohydrological factors responsible for the emergence of hot springs during the LGM and argue that refugia of this type, allowing the long-term survival and rapid post-LGM dispersal of temperate elements, were not exceptional in the European periglacial zone.

Mapping climate adaptation corridors for biodiversity-A regional-scale case study in Central America.

Climate adaptation corridors are widely recognized as important for promoting biodiversity resilience under climate change. Central America is part of the Mesoamerican biodiversity hotspot, but there have been no regional-scale analyses of potential climate adaptation corridors in Central America. We identified 2375 potential corridors throughout Central America that link lowland protected areas (≤ 500 m) with intact, high-elevation forests (≥ 1500 m) that represent potential climate change refugia. Whereas we found potential corridors in all Central American countries, potential corridors in Panama, Belize, and Honduras were most protected (medians = 64%, 49%, and 47%, respectively) and potential corridors in El Salvador were least protected (median = 10%). We also developed a corridor priority index based on the ecological characteristics and protected status of potential corridors and their associated start and end points. Compared to low- and medium-priority corridors, high-priority corridors (n = 160; top 7% of all corridors) were generally more protected, forested, and distributed across wider elevational gradients and more Key Biodiversity Areas, but also generally linked larger lowland protected areas to target areas that were larger, more protected, and spanned wider elevational gradients. For example, based on median values, high-priority corridors were 9% more protected and overlapped with 2-3 more Key Biodiversity Areas than low- and medium-priority corridors. Although high-elevation targets spanned considerably wider elevational gradients than lowland protected areas (medians = 695 vs. 142 m, respectively) and thus may be more likely to support refugia, they were considerably smaller than lowland protected areas (medians = 11 vs. 50 km2 respectively) and mostly unprotected (median = 4% protection). This initial, regional assessment can help prioritize locations for finer-scale research, conservation, and restoration activities in support of climate adaptation corridors throughout Central America and highlights the need for greater conservation of potential high-elevation refugia.

Survival in nunatak and peripheral glacial refugia of three alpine plant species is partly predicted by altitudinal segregation.

Mountain biota survived the Quaternary cold stages most probably in peripheral refugia and/or ice-free peaks within ice-sheets (nunataks). While survival in peripheral refugia has been broadly demonstrated, evidence for nunatak refugia is still scarce. We generated RADseq data from three mountain plant species occurring at different elevations in the southeastern European Alps to investigate the role of different glacial refugia during the Last Glacial Maximum (LGM). We tested the following hypotheses. (i) The deep Piave Valley forms the deepest genetic split in the species distributed across it, delimiting two peripheral refugia. (ii) The montane to alpine species Campanula morettiana and Primula tyrolensis survived the LGM in peripheral refugia, while high-alpine to subnival Saxifraga facchinii likely survived in several nunatak refugia. (iii) The lower elevation species suffered a strong population decline during the LGM. By contrast, the higher elevation species shows long-term stability of population sizes due to survival on permanently ice-free peaks and small population sizes at present. We found peripheral refugia on both sides of the Piave Valley, which acted as a major genetic barrier. Demographic modelling confirmed nunatak survival not only for S. facchinii but also for montane to alpine C. morettiana. Altitudinal segregation influenced the species' demographic fluctuations, with the lower elevation species showing a significant population increase at the end of the LGM, and the higher elevation species either showing decrease towards the present or stable population sizes with a short bottleneck. Our results highlight the role of nunatak survival and species ecology in the demographic history of mountain species.

Distinct communities under the snow: describing characteristics of subnivium arthropod communities.

Arthropods are active during the winter in temperate regions. Many use the seasonal snowpack as a buffer against harsh ambient conditions and are active in a refugium known as the subnivium. While the use of the subnivium by arthropods is well established, far less is known about subnivium community composition, abundance, biomass, and diversity and how these characteristics compare with the community in the summer. Understanding subnivium communities is especially important given the observed and anticipated changes in snowpack depth and duration due to the changing climate. We compared subnivium arthropod communities with those active during the summer using pitfall trapping in northern New Hampshire. We found that compositions of ground-active arthropod communities in the subnivium differed from those in the summer. The subnivium arthropod community featured moderate levels of richness and other measures of diversity that tended to be lower than the summer community. More strikingly, the subnivium community was much lower in overall abundance and biomass. Interestingly, some arthropods were dominant in the subnivium but either rare or absent in summer collections. These putative "subnivium specialists" included the spider Cicurina brevis (Emerton 1890) (Araneae: Hahniidae) and 3 rove beetles (Coleoptera: Staphylinidae): Arpedium cribratum Fauvel, 1878, Lesteva pallipes LeConte, 1863, and Porrhodites inflatus (Hatch, 1957). This study provides a detailed account of the subnivium arthropod community, establishes baseline information on arthropod communities in temperate forests of northeastern North America, and explores the idea of subnivium specialist taxa that are highly active in winter and might be especially vulnerable to climate change.

Restoring spatiotemporal variability to enhance the capacity for dispersal-limited species to track climate change.

Climate refugia are areas where species can persist through climate change with little to no movement. Among the factors associated with climate refugia are high spatial heterogeneity, such that there is only a short distance between current and future optimal climates, as well as biotic or abiotic environmental factors that buffer against variability in time. However, these types of climate refugia may be declining due to anthropogenic homogenization of environments and degradation of environmental buffers. To quantify the potential for restoration of refugia-like environmental conditions to increase population persistence under climate change, we simulated a population's capacity to track their temperature over space and time given different levels of spatial and temporal variability in temperature. To determine how species traits affected the efficacy of restoring heterogeneity, we explored an array of values for species' dispersal ability, thermal tolerance, and fecundity. We found that species were more likely to persist in environments with higher spatial heterogeneity and lower environmental stochasticity. When simulating a management action that increased the spatial heterogeneity of a previously homogenized environment, species were more likely to persist through climate change, and population sizes were generally higher, but there was little effect with mild temperature change. The benefits of heterogeneity restoration were greatest for species with limited dispersal ability. In contrast, species with longer dispersal but lower fecundity were more likely to benefit from a reduction in environmental stochasticity than an increase in spatial heterogeneity. Our results suggest that restoring environments to refugia-like conditions could promote species' persistence under the influence of climate change in addition to conservation strategies such as assisted migration, corridors, and increased protection.

Climate velocities and species tracking in global mountain regions.

Mountain ranges contain high concentrations of endemic species and are indispensable refugia for lowland species that are facing anthropogenic climate change1,2. Forecasting biodiversity redistribution hinges on assessing whether species can track shifting isotherms as the climate warms3,4. However, a global analysis of the velocities of isotherm shifts along elevation gradients is hindered by the scarcity of weather stations in mountainous regions5. Here we address this issue by mapping the lapse rate of temperature (LRT) across mountain regions globally, both by using satellite data (SLRT) and by using the laws of thermodynamics to account for water vapour6 (that is, the moist adiabatic lapse rate (MALRT)). By dividing the rate of surface warming from 1971 to 2020 by either the SLRT or the MALRT, we provide maps of vertical isotherm shift velocities. We identify 17 mountain regions with exceptionally high vertical isotherm shift velocities (greater than 11.67 m per year for the SLRT; greater than 8.25 m per year for the MALRT), predominantly in dry areas but also in wet regions with shallow lapse rates; for example, northern Sumatra, the Brazilian highlands and southern Africa. By linking these velocities to the velocities of species range shifts, we report instances of close tracking in mountains with lower climate velocities. However, many species lag behind, suggesting that range shift dynamics would persist even if we managed to curb climate-change trajectories. Our findings are key for devising global conservation strategies, particularly in the 17 high-velocity mountain regions that we have identified.

Mapping the habitat refugia of Isidella elongata under climate change and trawling impacts to preserve Vulnerable Marine Ecosystems in the Mediterranean.

The bamboo-coral Isidella elongata is a key habitat-forming species in the deep Mediterranean Sea. This alcyonacean is listed as an indicator of Vulnerable Marine Ecosystems (VMEs) and as Critically Endangered due to bottom trawling impacts. In this work, a modeling approach was used to predict and map the habitat suitability of I. elongata in the Mediterranean Sea under current environmental conditions. Occurrence data were modeled as a function of environmental parameters. Using climate change scenarios and fishing effort data, the risk of climate change and fisheries impacts on habitat suitability were estimated, and climate refugia were identified. A drastic loss of habitat is predicted, and climate change scenarios suggest a loss of 60% of suitable habitats by 2100. In the central Mediterranean, climate refugia overlapped with active fishing grounds. This study represents the first attempt to identify hot spots for the protection of soft bottom Vulnerable Marine Ecosystems for the entire Mediterranean Sea, and highlights areas most at risk from trawling. This work is relevant to the objectives of the EU Marine Strategy Framework and Maritime Spatial Planning Directives, the Biodiversity Strategy for 2030 regarding priority areas for conservation.

Temporal and spatial refugia modify predation risk for non-native crabs in rocky intertidal habitats.

Populations of the non-native Asian shore crab, Hemigrapsus sanguineus, now dominate the rocky intertidal of southern New England, USA. High abundances suggest the recent invader may have experienced enhanced success as a result of enemy release. While larvae and juveniles may serve as a food source for ecologically important species, little is known about predation of mature H. sanguineus or the influence of habitat on predation pressure. To assess natural predation rates of adult H. sanguineus, crabs were tethered in the intertidal at Clarks Cove in New Bedford, MA. Crabs were left in situ for half of a tidal cycle then observed for signs of predation. Results of separate high and low tide trials showed that adult crabs were preyed upon at both high and low tide, though at a significantly higher rate during high tide during both daytime and nighttime, suggesting predation by aquatic species is greater than that by terrestrial species. To investigate the role of habitat as refuge from predation, a laboratory experiment manipulated the complexity of habitat provided to crabs in the presence of a native fish predator. Results indicate better refuge is provided by more complex shelter. Together, findings suggest that fish, crabs, and/or diving birds are important predators for H. sanguineus in the invaded range and that habitat refuge acts to reduce predation pressure.

Refugia, climatic conditions and farm management factors as drivers of adaptation in Nematodirus battus populations.

Parasites are known for their ability to rapidly adapt to changing conditions. For parasitic helminths, changes in climate, along with farming and management practices associated with the intensification of livestock farming, provide novel challenges which can impact on their epidemiology and control. The sustainability of livestock production partially relies on effective control of helminth infection. Therefore, understanding changes in parasite behaviour, and what drives these, is of great importance. Nematodirus battus is an economically important helminth in the UK and temperate regions. Its infective larvae typically overwinter in eggs on pasture and hatch synchronously in spring, causing acute disease in lambs. Attempts to control disease typically rely on whole-flock benzimidazole (BZ) treatments. In recent years, the emergence of BZ-resistance, alongside the hatching of eggs without the classical over-winter 'chill stimulus', have made N. battus more difficult to control. In three previous studies, after collecting a large number of N. battus populations alongside farm management data from commercial farms, we explored the prevalence of genetic mutations associated with BZ-resistance (n = 253 farms), the ability of eggs to hatch with and without a chill stimulus (n = 90 farms) and how farm management practices varied throughout the UK (n = 187 farms). In the present study, we identify factors which may be acting as drivers, or barriers, to either the development of resistance or the variable hatching behaviour of N. battus eggs. Generalised linear mixed effect models were applied to regress experimental hatching and genotyping data on farm management and additional environmental data. Both variable hatching and resistance development appeared associated with the maintenance of parasite refugia as well as grazing management, particularly reseeding of pasture routinely grazed by young lambs each spring and the practice of set-stocked grazing. Effective quarantine measures were identified as the main protective factor for the development of BZ-resistance whereas set stocked grazing and population bottlenecks, resulting from reseeding heavily contaminated pastures, were risk factors. Spring maximum temperature and other climatic factors were associated with 'typical' hatching of eggs following a chill stimulus whilst several management factors were linked with hatching without prior chilling. For example, practices which reduce parasite numbers on pasture (e.g. re-seeding) or restrict availability of hosts (e.g. resting fields), were found to increase the odds of non-chill hatching. Retention of the timing of lambing and infection level of the host within the fitted model indicated that requirement for a chill stimulus prior to hatching may be plastic, perhaps subject to change throughout the grazing season, in response to immune development or parasite density-dependence within the host. Further investigation of the influence of the factors retained within the fitted models, particularly the theme of parasite refugia which was highlighted in relation to both the presence of BZ-resistance alleles and alternative hatching, is required to establish robust, sustainable parasite control and farm management strategies.

Life-history of Palaeoloxodon antiquus reveals Middle Pleistocene glacial refugium in the Megalopolis basin, Greece.

The Balkans are considered a major glacial refugium where flora and fauna survived glacial periods and repopulated the rest of Europe during interglacials. While it is also thought to have harboured Pleistocene human populations, evidence linking human activity, paleoenvironmental indicators and a secure temporal placement to glacial periods is scant. Here, we present the first intra-tooth multi-isotope analysis for the European straight-tusked elephant Palaeoloxodon antiquus, on an adult male individual excavated in association with lithic artefacts at the MIS 12 site Marathousa 1 (Megalopolis basin, Greece). The studied find also exhibits anthropogenic modifications, providing direct evidence of hominin presence. We employed strontium, carbon and oxygen isotope analysis on enamel bioapatite to investigate its foraging and mobility behaviour, using a sequential sampling strategy along the tooth growth axis of the third upper molar, to assess ecological changes during the last decade of life. We found a geographically restricted range, in a C3-dominated open woodland environment, and relatively stable conditions over the examined timeframe. Our results show that, despite the severity of the MIS 12 glacial, the Megalopolis basin sustained a mesic habitat, sufficient plant cover and limited seasonal fluctuations in resource availability, pointing to its role as a glacial refugium for both fauna and hominins.

Seeking temporal refugia to heat stress: increasing nocturnal activity despite predation risk.

Flexibility in activity timing may enable organisms to quickly adapt to environmental changes. Under global warming, diurnally adapted endotherms may achieve a better energy balance by shifting their activity towards cooler nocturnal hours. However, this shift may expose animals to new or increased environmental challenges (e.g. increased predation risk, reduced foraging efficiency). We analysed a large dataset of activity data from 47 ibex (Capra ibex) in two protected areas, characterized by varying levels of predation risk (presence versus absence of the wolf-Canis lupus). We found that ibex increased nocturnal activity following warmer days and during brighter nights. Despite the considerable sexual dimorphism typical of this species and the consequent different predation-risk perception, males and females demonstrated consistent responses to heat in both predator-present and predator-absent areas. This supports the hypothesis that shifting activity towards nighttime may be a common strategy adopted by diurnal endotherms in response to global warming. As nowadays different pressures are pushing mammals towards nocturnality, our findings emphasize the urgent need to integrate knowledge of temporal behavioural modifications into management and conservation planning.

Mediterranean springs: Keystone ecosystems and biodiversity refugia threatened by global change.

Mediterranean spring ecosystems are unique habitats at the interface between surface water and groundwater. These ecosystems support a remarkable array of biodiversity and provide important ecological functions and ecosystem services. Spring ecosystems are influenced by abiotic, biotic, and anthropogenic factors such as the lithology of their draining aquifers, their climate, and the land use of their recharge area, all of which affect the water chemistry of the aquifer and the spring discharges. One of the most relevant characteristics of spring ecosystems is the temporal stability of environmental conditions, including physicochemical features of the spring water, across seasons and years. This stability allows a wide range of species to benefit from these ecosystems (particularly during dry periods), fostering an unusually high number of endemic species. However, global change poses important threats to these freshwater ecosystems. Changes in temperature, evapotranspiration, and precipitation patterns can alter the water balance and chemistry of spring water. Eutrophication due to agricultural practices and emergent pollutants, such as pharmaceuticals, personal care products, and pesticides, is also a growing concern for the preservation of spring biodiversity. Here, we provide a synthesis of the main characteristics and functioning of Mediterranean spring ecosystems. We then describe their ecological value and biodiversity patterns and highlight the main risks these ecosystems face. Moreover, we identify existing knowledge gaps to guide future research in order to fully uncover the hidden biodiversity within these habitats and understand the main drivers that govern them. Finally, we provide a brief summary of recommended actions that should be taken to effectively manage and preserve Mediterranean spring ecosystems for future generations. Even though studies on Mediterranean spring ecosystems are still scarce, our review shows there are sufficient data to conclude that their future viability as functional ecosystems is under severe threat.

Diversification of refugia types needed to secure the future of coral reefs subject to climate change.

Identifying locations of refugia from the thermal stresses of climate change for coral reefs and better managing them is one of the key recommendations for climate change adaptation. We review and summarize approximately 30 years of applied research focused on identifying climate refugia to prioritize the conservation actions for coral reefs under rapid climate change. We found that currently proposed climate refugia and the locations predicted to avoid future coral losses are highly reliant on  excess heat metrics, such as degree heating weeks. However, many existing alternative environmental, ecological, and life-history variables could be used to identify other types of refugia that lead to the desired diversified portfolio for coral reef conservation. To improve conservation priorities for coral reefs, there is a need to evaluate and validate the predictions of climate refugia with long-term field data on coral abundance, diversity, and functioning. There is also the need to identify and safeguard locations displaying resistance toprolonged exposure to heat waves and the ability to recover quickly after thermal exposure. We recommend using more metrics to identify a portfolio of potential refugia sites for coral reefs that can avoid, resist, and recover from exposure to high ocean temperatures and the consequences of climate change, thereby shifting past efforts focused on avoidance to a diversified risk-spreading portfolio that can be used to improve strategic coral reef conservation in a rapidly warming climate.

Diversificación de los tipos de refugio necesarios para asegurar el futuro de los arrecifes de coral sujetos al cambio climático Resumen Una de las principales recomendaciones para la adaptación al cambio climático es identificar los refugios de los arrecifes de coral frente al estrés térmico del cambio climático y mejorar su gestión. Revisamos y resumimos ∼30 años de investigación aplicada centrada en la identificación de refugios climáticos para priorizar las acciones de conservación de los arrecifes de coral bajo un rápido cambio climático. Descubrimos que los refugios climáticos propuestos actualmente y las ubicaciones que pueden evitarlos dependen en gran medida de métricas de exceso de calor, como las semanas de calentamiento en grados (SCG). Sin embargo, existen muchas variables alternativas de historia vital, ambientales y ecológicas que podrían utilizarse para identificar otros tipos de refugios que resulten en el acervo diversificado que se desea para la conservación de los arrecifes de coral. Para mejorar las prioridades de conservación de los arrecifes de coral, es necesario evaluar y validar las predicciones sobre refugios climáticos con datos de campo a largo plazo sobre abundancia, diversidad y funcionamiento de los corales. También es necesario identificar y salvaguardar lugares que muestren resistencia a la exposición climática prolongada a olas de calor y la capacidad de recuperarse rápidamente tras la exposición térmica. Recomendamos utilizar más métricas para identificar un acervo de posibles lugares de refugio para los arrecifes de coral que puedan evitar, resistir y recuperarse de la exposición a las altas temperaturas oceánicas y las consecuencias del cambio climático, para así desplazar los esfuerzos pasados centrados en la evitación hacia un acervo diversificado de riesgos que pueda utilizarse para mejorar la conservación estratégica de los arrecifes de coral en un clima que se calienta rápidamente.

Tillandsia landbeckii phyllosphere and laimosphere as refugia for bacterial life in a hyperarid desert environment.

BACKGROUND: The lack of water is a major constraint for microbial life in hyperarid deserts. Consequently, the abundance and diversity of microorganisms in common habitats such as soil are strongly reduced, and colonization occurs primarily by specifically adapted microorganisms that thrive in particular refugia to escape the harsh conditions that prevail in these deserts. We suggest that plants provide another refugium for microbial life in hyperarid deserts. We studied the bacterial colonization of Tillandsia landbeckii (Bromeliaceae) plants, which occur in the hyperarid regions of the Atacama Desert in Chile, one of the driest and oldest deserts on Earth. RESULTS: We detected clear differences between the bacterial communities being plant associated to those of the bare soil surface (PERMANOVA, R2 = 0.187, p = 0.001), indicating that Tillandsia plants host a specific bacterial community, not only dust-deposited cells. Moreover, the bacterial communities in the phyllosphere were distinct from those in the laimosphere, i.e., on buried shoots (R2 = 0.108, p = 0.001), indicating further habitat differentiation within plant individuals. The bacterial taxa detected in the phyllosphere are partly well-known phyllosphere colonizers, but in addition, some rather unusual taxa (subgroup2 Acidobacteriae, Acidiphilum) and insect endosymbionts (Wolbachia, "Candidatus Uzinura") were found. The laimosphere hosted phyllosphere-associated as well as soil-derived taxa. The phyllosphere bacterial communities showed biogeographic patterns across the desert (R2 = 0.331, p = 0.001). These patterns were different and even more pronounced in the laimosphere (R2 = 0.467, p = 0.001), indicating that different factors determine community assembly in the two plant compartments. Furthermore, the phyllosphere microbiota underwent temporal changes (R2 = 0.064, p = 0.001). CONCLUSIONS: Our data demonstrate that T. landbeckii plants host specific bacterial communities in the phyllosphere as well as in the laimosphere. Therewith, these plants provide compartment-specific refugia for microbial life in hyperarid desert environments. The bacterial communities show biogeographic patterns and temporal variation, as known from other plant microbiomes, demonstrating environmental responsiveness and suggesting that bacteria inhabit these plants as viable microorganisms. Video Abstract.