Phytoplankton biodiversity is more important for ecosystem functioning in highly variable thermal environments

The 21st century has seen an acceleration of anthropogenic climate change and biodiversity loss, with both stressors deemed to affect ecosystem functioning. However, we know little about the interactive effects of both stressors and in particular about the interaction of increased climatic variability and biodiversity loss on ecosystem functioning. This should be remedied because larger climatic variability is one of the main features of climate change. Here, we demonstrated that temperature fluctuations led to changes in the importance of biodiversity for ecosystem functioning. We used microcosm communities of different phytoplankton species richness and exposed them to a constant, mild, and severe temperature-fluctuating environment. Wider temperature fluctuations led to steeper biodiversity–ecosystem functioning slopes, meaning that species loss had a stronger negative effect on ecosystem functioning in more fluctuating environments. For severe temperature fluctuations, the slope increased through time due to a decrease of the productivity of species-poor communities over time. We developed a theoretical competition model to better understand our experimental results and showed that larger differences in thermal tolerances across species led to steeper biodiversity–ecosystem functioning slopes. Species-rich communities maintained their ecosystem functioning with increased fluctuation as they contained species able to resist the thermally fluctuating environments, while this was on average not the case in species-poor communities. Our results highlight the importance of biodiversity for maintaining ecosystem functions and services in the context of increased climatic variability under climate change.

Climate change and biodiversity loss are two of the most pressing ecological issues of the century (1, 2). Because biodiversity is positively related to ecosystem functioning (3–8), the accelerating species loss is expected to lead to a decrease in ecosystem functioning and ecosystem services (9–13).Climate change increases both the mean and variance in temperature (1, 14), which can further hamper ecosystem functioning (15–17). Increased temperature variance in particular is expected to pose a greater risk to biodiversity than increased mean (18, 19). However, much less is known about the potential interactive effects of biodiversity loss and climate change on ecosystem functioning (but refer to refs. 20 to 23) and particularly between the potential interactive effects of biodiversity loss and temperature fluctuations. To better understand the potential impacts of increased climatic variation and biodiversity loss on ecosystems, it is thus important to investigate the effect of temperature fluctuations on the biodiversity–ecosystem functioning (BEF) relationship.Climate change has complex effects on biodiversity and ecosystem functioning. Warmer climates can lead to both a loss (24–29) and an increase in biodiversity (30, 31). At the local scale, the effect of increased temperature on species richness shows mixed trends, with studies finding declines (32–34), increases (30, 35), or no discernible trend (36, 37). The effects of increased thermal variability also remain unclear: positive, negative, or no effects on richness have been reported (16, 38–42). Furthermore, climate change can alter ecosystem functioning, either directly or indirectly through changes in biodiversity (16, 43–47).In addition to affecting diversity and ecosystem functioning, increased temperature mean and variation can modify the relationship between biodiversity and ecosystem functioning. In bacteria and phytoplankton, warmer temperatures resulted in a steeper slope of the relationship between log ecosystem functioning and log species richness (21, 22, 48). Steeper slopes of the BEF relationship indicate that the effect of biodiversity on ecosystem functioning is stronger in warmer environments: that is, the loss of one species has a more detrimental effect on ecosystem functioning as temperatures increase. Interestingly, a recent study on picophytoplankton showed that the steepness of the biodiversity–ecosystem functioning slope relied on both short-term temperature and community evolutionary history (23). Less is known about the effect of temperature fluctuations on BEF relationships. A study on protozoan–bacteria consumer–resource relationships showed that the slope between diversity and biomass became shallower with increased fluctuations (49); another study on fungal assemblages showed that polycultures decomposed leaves better than monocultures under fluctuating temperatures (50).Several mechanisms might lead to a change in the relationship between biodiversity and ecosystem functioning with temperature fluctuations. We focus on three mechanisms of potential relevance on fluctuating environments: tolerance differences, species interactions, and temporal asynchrony. First, different species within a community have different thermal tolerances, that is, they handle thermal stress differently. When temperature mean or fluctuation increases, these underlying interspecific differences can manifest more strongly. This, in turn, can lead species-rich communities to perform better than species-poor communities due to their containing of species able to resist the stressful conditions, leading to increased slopes of BEF with stress (51). This was the case in marine phytoplankton communities, where differences in species thermal tolerances led to a larger effect of biodiversity on ecosystem functioning in more physiologically stressful, warmer environments (22). Theory suggests that when the environment becomes too stressful and exceeds the thermal tolerances of all species, the slopes of BEF become shallower again (48, 51). In a context of increased temperature fluctuations, one can expect that differences in average tolerances to the varying environmental conditions among species would lead to variation in the relationship of ecosystem functioning with species richness. Thus, we expect that communities with a larger spread in thermal tolerances should have a steeper BEF relationship.Second, species interactions can change in response to changes in the thermal environment. Strong competition among species can lead to shallower BEF slopes, where adding one species does not increase ecosystem functioning much when species compete for the same resources [i.e., small niche differences (52, 53)]. On the contrary, large niche differences or facilitative interactions can lead to opposite relationships, where adding one species strongly increases overall ecosystem functioning. If increased temperature fluctuations cause a change in competitive interactions, this in turn can lead to a modification of the BEF slope. Models investigating the effect of temperature mean and variation on BEF relationships have suggested that temperature-driven changes in the intensity of competition could indeed play a role in driving the relationship (49).Third, asynchrony in species temporal dynamics within a community, for instance due to temperature fluctuations, can lead to increased ecosystem productivity and temporal stability through an insurance effect (5, 54). This can lead to a community that is dominated by different species depending on their tolerance to the current environmental conditions (e.g., “warm-adapted” species increasing in abundance and dominating when temperature is hotter, and “cold-adapted” species dominating when temperature is cooler). Such mechanism would lead more diverse communities to perform better in thermally fluctuating environments than species-poor communities. These three mechanisms can co-occur and lead to changes in BEF with temperature fluctuations.The effects of biodiversity on ecosystem functioning often increases through time (55, 56). Thus, the impact of species loss on functioning is larger as ecosystems assemble. Such temporal effects can arise from a temporal increase in productivity of species-rich communities (e.g., through increases in complementarity through time, for instance when legumes increase nutrient availability for other plant species by fixing atmospheric nitrogen), a decrease in productivity of species-poor communities (e.g., through increases in abundance of antagonistic soil microorganisms in plant communities), or a combination of both (55, 57, 58). Temporal fluctuations could, in turn, interfere with ecosystem temporal dynamics, and it is worth investigating whether this could lead to changes in the biodiversity–ecosystem relationships over time.Here, we used a proof-of-concept experiment and a theoretical model to understand how increasing temperature fluctuations affected BEF relationships and whether these relationships changed over time. We experimentally manipulated the species richness of phytoplankton communities at a control temperature of 25 °C, a moderate temperature fluctuation treatment of between 22 and 28 °C every other day, and a severe fluctuation treatment of between 19 and 31 °C every other day using a random partitioning experimental design (ref. 59, Fig. 1). We quantified the impact of temperature fluctuations and temporal scale (i.e., after 5 and 15 d) on the relationship between biodiversity and ecosystem production. This experimental design allowed quantifying the impacts of random species loss on ecosystem functioning as well as evaluating the relative contribution of each species to ecosystem production. We used three measures of ecosystem production, either total cell abundance, total biomass, or total chlorophyll a content. Such measures have been used in similar experiments (22, 48, 49), and measures of biomass production have been widely used in plants (11). However, it is to note that ecosystem functioning can be also measured as a flux, such as C fixation, O₂ production, or nutrient recycling, that we were unfortunately unable to measure here. Including such fluxes could lead to different expectations of the BEF slope and is beyond the scope of our study. We further explored the relative importance of the three different mechanisms outlined above (tolerance differences, species interactions, and temporal asynchrony) as drivers of our experimental results. We did so by means of our experimental data and a simple theoretical model of species competition. In particular, we tested whether potential changes in BEF slope were linked to a change in species interactions or a greater spread in thermal tolerances and explored the impact of temporal asynchrony in the model, using cell abundance as a measure for ecosystem function.Open in a separate windowFig. 1.Flowchart of the experimental design and its comparison with the theoretical model.     

From the Cover: Navigating transformations in governance of Chilean marine coastal resources

Marine ecosystems are in decline. New transformational changes in governance are urgently required to cope with overfishing, pollution, global changes, and other drivers of degradation. Here we explore social, political, and ecological aspects of a transformation in governance of Chile''s coastal marine resources, from 1980 to today. Critical elements in the initial preparatory phase of the transformation were (i) recognition of the depletion of resource stocks, (ii) scientific knowledge on the ecology and resilience of targeted species and their role in ecosystem dynamics, and (iii) demonstration-scale experimental trials, building on smaller-scale scientific experiments, which identified new management pathways. The trials improved cooperation among scientists and fishers, integrating knowledge and establishing trust. Political turbulence and resource stock collapse provided a window of opportunity that triggered the transformation, supported by new enabling legislation. Essential elements to navigate this transformation were the ability to network knowledge from the local level to influence the decision-making processes at the national level, and a preexisting social network of fishers that provided political leverage through a national confederation of artisanal fishing collectives. The resultant governance scheme includes a revolutionary national system of marine tenure that allocates user rights and responsibilities to fisher collectives. Although fine tuning is necessary to build resilience of this new regime, this transformation has improved the sustainability of the interconnected social–ecological system. Our analysis of how this transformation unfolded provides insights into how the Chilean system could be further developed and identifies generalized pathways for improved governance of marine resources around the world.     

Natural enemy interactions constrain pest control in complex agricultural landscapes

Biological control of pests by natural enemies is a major ecosystem service delivered to agriculture worldwide. Quantifying and predicting its effectiveness at large spatial scales is critical for increased sustainability of agricultural production. Landscape complexity is known to benefit natural enemies, but its effects on interactions between natural enemies and the consequences for crop damage and yield are unclear. Here, we show that pest control at the landscape scale is driven by differences in natural enemy interactions across landscapes, rather than by the effectiveness of individual natural enemy guilds. In a field exclusion experiment, pest control by flying insect enemies increased with landscape complexity. However, so did antagonistic interactions between flying insects and birds, which were neutral in simple landscapes and increasingly negative in complex landscapes. Negative natural enemy interactions thus constrained pest control in complex landscapes. These results show that, by altering natural enemy interactions, landscape complexity can provide ecosystem services as well as disservices. Careful handling of the tradeoffs among multiple ecosystem services, biodiversity, and societal concerns is thus crucial and depends on our ability to predict the functional consequences of landscape-scale changes in trophic interactions.     

From the Cover: Global meta-analysis reveals no net change in local-scale plant biodiversity over time

Global biodiversity is in decline. This is of concern for aesthetic and ethical reasons, but possibly also for practical reasons, as suggested by experimental studies, mostly with plants, showing that biodiversity reductions in small study plots can lead to compromised ecosystem function. However, inferring that ecosystem functions will decline due to biodiversity loss in the real world rests on the untested assumption that such loss is actually occurring at these small scales in nature. Using a global database of 168 published studies and >16,000 nonexperimental, local-scale vegetation plots, we show that mean temporal change in species diversity over periods of 5–261 y is not different from zero, with increases at least as likely as declines over time. Sites influenced primarily by plant species’ invasions showed a tendency for declines in species richness, whereas sites undergoing postdisturbance succession showed increases in richness over time. Other distinctions among studies had little influence on temporal richness trends. Although maximizing diversity is likely important for maintaining ecosystem function in intensely managed systems such as restored grasslands or tree plantations, the clear lack of any general tendency for plant biodiversity to decline at small scales in nature directly contradicts the key assumption linking experimental results to ecosystem function as a motivation for biodiversity conservation in nature. How often real world changes in the diversity and composition of plant communities at the local scale cause ecosystem function to deteriorate, or actually to improve, remains unknown and is in critical need of further study.A huge number of experiments has investigated the effects of species diversity (typically the number of species) on ecosystem function in small study plots (≤400 m²), with a general consensus emerging that processes such as primary productivity and nutrient uptake increase as a function of the number of species in a community (1–6). These experiments thus appear to provide a powerful motivation for biodiversity conservation, given that ecosystem functions underpin many ecosystem services from which people benefit, such as forage production and carbon sequestration (1). However, the link between diversity-function experiments and the widespread argument that ecosystem function should motivate biodiversity conservation (7–11) hinges on the untested assumption that global biodiversity declines apply to the small scale (2). Experimental studies typically focus on small spatial scales not only for practical reasons, but also because organisms, plants in particular, typically interact over short distances (12), and so it is at the small scale that biodiversity is most likely to have an important impact on the functioning of ecosystems (13–15).Habitat loss, invasive species, and overexploitation, among other factors, have accelerated global species’ extinction well beyond the background rate (16–18), and it is tempting to assume that a global decline in biodiversity is necessarily accompanied by declines at smaller spatial scales. However, this is not a logical inevitability because, unlike other key variables involved in global environmental change, biodiversity at large scales (often termed gamma diversity) is not an additive function of biodiversity at smaller scales (alpha diversity). If global temperature or atmospheric CO₂ concentrations, for example, are increasing at the global scale, the net change over time within local areas must, on average, be positive. However, because local species losses may be accompanied by immigration of species from elsewhere, decreases in biodiversity at the global scale do not necessarily result in any biodiversity change at smaller scales (16, 19, 20). Here we present a global synthesis testing for directional changes in local-scale biodiversity of terrestrial plants, which have been the focus of most well-replicated biodiversity-ecosystem function (BDEF) experiments. We focus on the most commonly studied component of biodiversity—species diversity—estimated by metrics that reflect the number of species (richness) and/or the equitability of their abundances (indices of diversity or evenness).     

From the Cover: Photic memory for executive brain responses

Light is a powerful stimulant for human alertness and cognition, presumably acting through a photoreception system that heavily relies on the photopigment melanopsin. In humans, evidence for melanopsin involvement in light-driven cognitive stimulation remains indirect, due to the difficulty to selectively isolate its contribution. Therefore, a role for melanopsin in human cognitive regulation remains to be established. Here, sixteen participants underwent consecutive and identical functional MRI recordings, during which they performed a simple auditory detection task and a more difficult auditory working memory task, while continuously exposed to the same test light (515 nm). We show that the impact of test light on executive brain responses depends on the wavelength of the light to which individuals were exposed prior to each recording. Test-light impact on executive responses in widespread prefrontal areas and in the pulvinar increased when the participants had been exposed to longer (589 nm), but not shorter (461 nm), wavelength light, more than 1 h before. This wavelength-dependent impact of prior light exposure is consistent with recent theories of the light-driven melanopsin dual states. Our results emphasize the critical role of light for cognitive brain responses and are, to date, the strongest evidence in favor of a cognitive role for melanopsin, which may confer a form of “photic memory” to human cognitive brain function.One of the major advances in neuroscience in the last decade was the discovery of a novel class of ocular photoreceptors: the intrinsically photosensitive retinal ganglion cells (ipRGCs) that express melanopsin (1), a photopigment maximally sensitive to blue light (2–4). The finding of a new inner retinal photopigment has led to a complete reexamination of the role of the eye, which is now viewed as the site of two distinct photoreceptive systems: one for vision, based mainly on rods and cones, and one for the non–image-forming functions of light, primarily dependent on melanopsin. Animal data have demonstrated that the melanopsin photoreception system directly mediates the impact of light on sleep/wake regulation (5). In humans, light also regulates sleep and wakefulness and constitutes a powerful stimulant for alertness and cognition (6, 7). However, evidence for the involvement of melanopsin in this human light-driven stimulating impact remains indirect (8, 9), due to the difficulty of selectively isolating contributions of ipRGCs, rods, and/or cones. Therefore, the contribution of melanopsin to the impact of light on human alertness and cognition remains to be established.Photon capture by rod and cone photopigments converts the chromophore from a photosensitive to a photoinsensitive state, triggering phototransduction (10). To regain light sensitivity, the enzymatic retinoid cycle within the retinal pigment epithelium is required for regeneration of the chromophore back to the light-sensitive state. In contrast, melanopsin is a dual-state photopigment, in which photons drive both processes of phototransduction and part of chromophore regeneration (10–12). Recent rodent and human data suggest that exposure to longer wavelength light (590–620 nm; orange–red) triggers melanopsin chromophore regeneration and increases overall subsequent intrinsic photosensitivity of ipRGCs (13, 14). Conversely, exposure to shorter wavelength light (∼480 nm; blue) favors phototransduction and decreases overall subsequent ipRGCs intrinsic photosensitivity (13, 14). At the physiological level (12), the existence of two stable photon absorption states allows photoconversion of melanopsin between the 11-cis and all-trans isoforms of the photopigment-bound chromophore to drive both photic responses and restoration of light responsiveness (12, 14), similar to processes of invertebrate rhabdomeric photopigments (15). Melanopsin would thus act as a light-sensitive switch, with the 11-cis isoform maximally sensitive to 480-nm photons, whereas the all-trans isoform is most efficiently transformed by longer wavelengths. Prior short-wavelength light would therefore decrease the overall proportion of “phototransduction units” of ipRGCs, whereas longer-wavelength photons (∼590–620 nm) would increase the overall proportion of phototransduction units. At intermediate wavelengths near 515 nm, the two processes are in equilibrium, with the two effects counterbalancing each other (“isosbestic value”) (15).The present study aimed at determining melanopsin influence on human cognitive brain function based on this photic history hypothesis of its dual states. Based on the spectral sensitivity of the two states of melanopsin, we hypothesized that the impact of a given test light on cognitive brain responses would be increased, decreased, or intermediate after prior exposure to longer, shorter, or intermediate wavelength light, respectively.     

From the Cover: Warm spring reduced carbon cycle impact of the 2012 US summer drought

The global terrestrial carbon sink offsets one-third of the world’s fossil fuel emissions, but the strength of this sink is highly sensitive to large-scale extreme events. In 2012, the contiguous United States experienced exceptionally warm temperatures and the most severe drought since the Dust Bowl era of the 1930s, resulting in substantial economic damage. It is crucial to understand the dynamics of such events because warmer temperatures and a higher prevalence of drought are projected in a changing climate. Here, we combine an extensive network of direct ecosystem flux measurements with satellite remote sensing and atmospheric inverse modeling to quantify the impact of the warmer spring and summer drought on biosphere-atmosphere carbon and water exchange in 2012. We consistently find that earlier vegetation activity increased spring carbon uptake and compensated for the reduced uptake during the summer drought, which mitigated the impact on net annual carbon uptake. The early phenological development in the Eastern Temperate Forests played a major role for the continental-scale carbon balance in 2012. The warm spring also depleted soil water resources earlier, and thus exacerbated water limitations during summer. Our results show that the detrimental effects of severe summer drought on ecosystem carbon storage can be mitigated by warming-induced increases in spring carbon uptake. However, the results also suggest that the positive carbon cycle effect of warm spring enhances water limitations and can increase summer heating through biosphere–atmosphere feedbacks.An increase in the intensity and duration of drought (1, 2), along with warmer temperatures, is projected for the 21st century (3). Warmer and drier summers can substantially reduce photosynthetic activity and net carbon uptake (4). In contrast, warmer temperatures during spring and autumn prolong the period of vegetation activity and increase net carbon uptake in temperate ecosystems (5), sometimes even during spring drought (6). Atmospheric CO₂ concentrations suggest that warm-spring–induced increases in carbon uptake could be cancelled out by the effects of warmer and drier summers (7). However, the extent and variability of potential compensation on net annual uptake using direct observations of ecosystem carbon exchange have not yet been examined for specific climate anomalies.In addition to perturbations of the carbon cycle, warmer spring temperatures can have an impact on the water cycle by increasing evaporation from the soil and plant transpiration (8–10), which reduces soil moisture. Satellite observations suggest that warmer spring and longer nonfrozen periods enhance summer drying via hydrological shifts in soil moisture status (11). Climate model simulations also indicate a soil moisture–temperature feedback between early vegetation green-up in spring and extreme temperatures in summer (12, 13). Soil water deficits during drought impose a reduction in stomatal conductance, thereby reducing evaporative cooling and thus increasing near-surface temperatures (14). Stomatal closure also has a positive (enhancing) feedback with atmospheric water demand by increasing the vapor pressure deficit (VPD) of the atmosphere (15). The vegetation response thus plays a crucial role for temperature feedbacks during drought (16).Given the opposing effects of concurrent warmer spring and summer drought, and an increased frequency of these anomalies projected until the end of this century (SI Appendix, Fig. S1), it is imperative to understand (i) the response of the terrestrial carbon balance and (ii) the interaction of carbon uptake with water and energy fluxes that are associated with these seasonal climate anomalies.The year 2012 was among the warmest on record for the contiguous United States (CONUS), which experienced one of the most severe droughts since the Dust Bowl era of the 1930s (17, 18). The drought caused substantial economic damage, particularly for agricultural production (SI Appendix). Annual mean temperatures were 1.8 °C above average, with the warmest spring (+2.9 °C) and second warmest summer (+1.4 °C) in the period of 1895–2012 (19). Precipitation deficits started to evolve in May across the Great Plains and the Midwest (17), but eventually affected more than half of the United States (20). By July, 62% of the United States experienced moderate to exceptional drought, which was the largest spatial extent of drought for the United States since the Dust Bowl era (19). Severe drought conditions with depleted soil moisture persisted throughout summer, and unprecedented precipitation deficits of 47% below normal for May through August were observed in the central Great Plains (17).Here, we analyze the response of land-atmosphere carbon and water exchange for major ecosystems in the United States during the concurrent warmer spring and summer drought of 2012 at the ecosystem, regional, and continental scales. We combine direct measurements of land-atmosphere CO₂, water vapor, and energy fluxes from 22 eddy-covariance (EC) towers across the United States (SI Appendix, Fig. S2 and Table S1) with large-scale satellite remote-sensing observations of gross primary production (GPP), evapotranspiration (ET), and enhanced vegetation index (EVI) derived from the space-borne Moderate Resolution Imaging Spectroradiometer (MODIS), and estimates of net ecosystem production (NEP; i.e., net carbon uptake) from an atmospheric CO₂ inversion (CarbonTracker, CTE2014). This comprehensive suite of standardized analyses across sites and data streams was crucial to constrain the impact of such a large-scale drought event with bottom-up and top-down approaches (21), and something only a few synthesis studies have achieved so far (4, 22).We test the hypothesis that increased carbon uptake due to warm spring offset the negative impacts of severe summer drought during 2012, and examine the relationship between early-spring–induced soil water depletion and increased summer temperatures. When using the term “drought,” we refer to precipitation deficits that resulted in soil moisture deficiencies (9).     

From the Cover: Father's brain is sensitive to childcare experiences

Although contemporary socio-cultural changes dramatically increased fathers'' involvement in childrearing, little is known about the brain basis of human fatherhood, its comparability with the maternal brain, and its sensitivity to caregiving experiences. We measured parental brain response to infant stimuli using functional MRI, oxytocin, and parenting behavior in three groups of parents (n = 89) raising their firstborn infant: heterosexual primary-caregiving mothers (PC-Mothers), heterosexual secondary-caregiving fathers (SC-Fathers), and primary-caregiving homosexual fathers (PC-Fathers) rearing infants without maternal involvement. Results revealed that parenting implemented a global “parental caregiving” neural network, mainly consistent across parents, which integrated functioning of two systems: the emotional processing network including subcortical and paralimbic structures associated with vigilance, salience, reward, and motivation, and mentalizing network involving frontopolar-medial-prefrontal and temporo-parietal circuits implicated in social understanding and cognitive empathy. These networks work in concert to imbue infant care with emotional salience, attune with the infant state, and plan adequate parenting. PC-Mothers showed greater activation in emotion processing structures, correlated with oxytocin and parent-infant synchrony, whereas SC-Fathers displayed greater activation in cortical circuits, associated with oxytocin and parenting. PC-Fathers exhibited high amygdala activation similar to PC-Mothers, alongside high activation of superior temporal sulcus (STS) comparable to SC-Fathers, and functional connectivity between amygdala and STS. Among all fathers, time spent in direct childcare was linked with the degree of amygdala-STS connectivity. Findings underscore the common neural basis of maternal and paternal care, chart brain–hormone–behavior pathways that support parenthood, and specify mechanisms of brain malleability with caregiving experiences in human fathers.Throughout human history and across cultures, women have typically assumed primary caregiving responsibility for infants (1, 2). Although humans are among the few mammalian species where some male parental caregiving is relatively common, father involvement varies considerably within and across cultures, adapting to ecological conditions (1, 3). Involved fathering has been linked with children''s long-term physiological and social development and with increases in mothers'' caregiving-related hormones such as oxytocin and prolactin (3–6). In addition, animal studies demonstrated structural brain alterations in caregiving fathers (7, 8). It has been suggested that, although maternal caregiving is triggered by neurobiological processes related to pregnancy and labor, the human father''s brain, similar to other biparental mammals, adapts to the parental role through active involvement in childcare (1–3). Despite growing childcare involvement of fathers (3, 5, 6), mechanisms for human fathers'' brain adaptation to caregiving experiences remain largely unknown, and no study to our knowledge has examined the brain basis of human fatherhood when fathers assume primary responsibility for infant care.For social species with lengthy periods of dependence, parental caregiving is key to survival and relies on brain structures that maximize survival (2, 9). Animal studies have demonstrated that mammalian mothering is supported by evolutionarily ancient structures implicated in emotional processing, vigilance, motivation, and reward, which are rich in oxytocin receptors, including the amygdala, hypothalamus, nucleus accumbens, and ventral tegmental area (VTA), and that these regions are sensitive to caregiving behavior (9, 10). Imaging studies of human mothers found activation in similar areas, combined with paralimbic insula-cingulate structures that imbue infants with affective salience, ground experience in the present moment and enable maternal simulation of infant states (11–13). These structures implicate a phylogenetically ancient network of emotional processing that rapidly detects motivationally salient and survival-related cues (14) and enables parents to automatically identify and immediately respond to infant distress, thereby maximizing survival. In humans, this emotional processing network is complemented by a cortical mentalizing network of frontopolar-medial-prefrontal-temporo-parietal structures involved in social understanding, theory of mind, and cognitive empathy, including the medial prefrontal cortex (mPFC), frontopolar cortex, superior temporal sulcus (STS), and temporal poles (15). The mentalizing network plays an important role in individuals'' ability to infer mental states from behavior, is already activated during the parents'' first weeks of parenting, and enables parents to cognitively represent infant states, predict infant needs, and plan future caregiving (11–13).The few studies examining the human father''s brain showed activation in similar areas, including the STS, lateral and medial frontal regions, VTA, inferior frontal gyrus (IFG), and orbitofrontal cortex (OFC) (16, 17). Only one study compared maternal and paternal brain response to infant cues, reporting mothers'' greater amygdala activation, fathers'' greater superior-temporal and medial-frontal activation, and maternal and paternal oxytocin''s different associations with amygdala vs. cortical activation (18). Oxytocin, a nine-amino acid neuropeptide that underpins the formation of affiliative bonds (19), supports the development of human parental caregiving (20). Research has shown that maternal and paternal oxytocin levels are associated with parent–infant synchrony, which is the parent''s careful adaptation of caregiving behavior to infant''s social signals (21). However, although oxytocin levels are similar in mothers and fathers, oxytocin is differentially linked with the parent-specific repertoire, for instance, with affectionate contact in mothers and stimulatory play in fathers (5, 20).Ethological perspectives emphasize the importance of studying the neurobiology of parenting in its natural habitat and of using a behavior-based approach to test parents'' brain adaptation to ecological pressures (22). Consistent with findings in other mammals (10), studies on brain–behavior associations in human mothers describe links between mother–infant synchrony and brain activation in the mother''s subcortical regions, including the amygdala, nucleus accumebens, and hippocampus (11, 13). In contrast, the one study testing human fathers'' brain–behavior associations showed correlations with cortical activation (17). Overall, these findings suggest that distinct brain–hormone–behavior pathways may underpin maternal and paternal care; therefore, oxytocin and parenting behavior may be associated with the emotional processing network in mothers but with the socio-cognitive circuit in fathers. Furthermore, animal studies indicate that active caregiving in biparental fathers leads to greater integration of multiple brain networks involved in nurturance, learning, and motivation (7). Hence, active involvement in caregiving may possibly facilitate integration of both parenting-related networks in human fathers, particularly among those who undertake the primary caregiver role.The present study sought to examine the brain basis of human fatherhood by using a “natural experiment,” afforded for the first time in human history, to our knowledge, by contemporary socio-cultural changes. Throughout history, infants without mothers were cared for by other women (2). Current social changes enable the formation of two-father families raising children with no maternal involvement since birth (3). Such a context provides a unique setting to assess changes in the paternal brain on assuming the traditionally maternal role. Moreover, understanding mechanisms of brain adaptation to caregiving experiences in primary-caregiving fathers may shed further light on processes that refine all fathers'' responses to childcare activities.We visited the homes of two-parent families rearing their firstborn child: heterosexual mother-father couples comprising primary-caregiving mothers (PC-Mothers) and secondary-caregiving fathers (SC-Fathers) and homosexual couples comprising two primary-caregiving fathers (PC-Fathers) (SI Materials and Methods). We videotaped parent–infant interaction in the natural habitat, measured parental oxytocin, and used the videotaped parent–child interactions as stimuli for functional MRI (fMRI) to test parental brain response to infant-related cues. Five hypotheses were proposed. First, we expected activation in both subcortical areas involved in vigilance and reward and cortical circuits implicated in social understanding in all parents raising a young infant. Second, we expected greater subcortical activation in mothers, particularly in the amygdala, which has been repeatedly linked with mammalian mothering (23, 24), and greater activation in cortical socio-cognitive circuits in fathers. Third, the brain–hormone–behavior constellation underpinning maternal care was expected to center around the emotional-processing network, whereas the brain–hormone–behavior links in fathers were expected to coalesce with the socio-cognitive network. Fourth, consistent with the context-specific evolution of human fathering (1), we expected greater variability in fathers'' brain response as mediated by actual caregiving experiences. Such variability would be particularly noted among the primary-caregiving fathers raising infants without mothers and may involve functional integration of the subcortical and cortical networks subserving parenting. Finally, we expected that the pathways leading from the parent''s primary caregiving role to greater parent–infant synchrony would be mediated by parental brain activation and oxytocin levels.     

From the Cover: Condensing water vapor to droplets generates hydrogen peroxide

It was previously shown [J. K. Lee et al., Proc. Natl. Acad. Sci. U.S.A., 116, 19294–19298 (2019)] that hydrogen peroxide (H₂O₂) is spontaneously produced in micrometer-sized water droplets (microdroplets), which are generated by atomizing bulk water using nebulization without the application of an external electric field. Here we report that H₂O₂ is spontaneously produced in water microdroplets formed by dropwise condensation of water vapor on low-temperature substrates. Because peroxide formation is induced by a strong electric field formed at the water–air interface of microdroplets, no catalysts or external electrical bias, as well as precursor chemicals, are necessary. Time-course observations of the H₂O₂ production in condensate microdroplets showed that H₂O₂ was generated from microdroplets with sizes typically less than ∼10 µm. The spontaneous production of H₂O₂ was commonly observed on various different substrates, including silicon, plastic, glass, and metal. Studies with substrates with different surface conditions showed that the nucleation and the growth processes of condensate water microdroplets govern H₂O₂ generation. We also found that the H₂O₂ production yield strongly depends on environmental conditions, including relative humidity and substrate temperature. These results show that the production of H₂O₂ occurs in water microdroplets formed by not only atomizing bulk water but also condensing water vapor, suggesting that spontaneous water oxidation to form H₂O₂ from water microdroplets is a general phenomenon. These findings provide innovative opportunities for green chemistry at heterogeneous interfaces, self-cleaning of surfaces, and safe and effective disinfection. They also may have important implications for prebiotic chemistry.

Water molecules in liquid water are considered stable and inert. We and other investigators have reported that water molecules become electrochemically active and catalytic for various reactions when bulk water is formed into micrometer-sized droplets (microdroplets). Reaction rates for various chemical reactions are accelerated in microdroplets by factors of 10² or more compared to bulk solution (1). The microdroplet environment provides conditions for a lowered entropic barrier, which allows thermodynamically unfavorable reactions to proceed in microdroplets at room temperature (2, 3). We also have shown that water microdroplets induce spontaneous charge exchanges between solutes and water molecules to induce the spontaneous reduction of organic molecules and metal ions as well as the formation of nanostructures without any added reducing agent or template (4, 5). Moreover, we have reported that water molecules undergo spontaneous oxidation to form reactive oxygen species, including hydroxyl radicals (OH) and hydrogen peroxide (H₂O₂) (6–8). Recent investigations attributed the origin of these unique physicochemical properties observed in microdroplets to the enrichment of reactants at the interface (9–11), restricted molecular rotations (12), partial solvation at the water surface (1, 13), and a strong interfacial electric field at the surface of the water microdroplet (14).Microdroplets can be formed either by atomizing bulk water (top down) with various methods such as high-pressure gas nebulization (15), ultrasonic nebulization (16), vibrating micromesh nebulization (17), and piezoelectric nebulization (18), or by condensing vapor-phase molecules (bottom up) (19). A question may be asked whether those unique properties of microdroplets arise only in microdroplets formed by atomization of bulk water. In addition, it may be wondered whether the spontaneous oxidation of water to form H₂O₂ in microdroplets (6) was caused by the atomizing process involving friction or vibration. These questions motivated us to investigate whether H₂O₂ becomes spontaneously generated in water microdroplets formed by the condensation of water vapor in air on cold surfaces, and how universal might this process be. We have paid special attention to the influence of different surface properties, including hydrophilicity and surface roughness, as well as environmental factors, including relative humidity and surface temperature.     

From the Cover: S-nitrosoglutathione reductase (GSNOR) enhances vasculogenesis by mesenchymal stem cells

Although nitric oxide (NO) signaling promotes differentiation and maturation of endothelial progenitor cells, its role in the differentiation of mesenchymal stem cells (MSCs) into endothelial cells remains controversial. We tested the role of NO signaling in MSCs derived from WT mice and mice homozygous for a deletion of S-nitrosoglutathione reductase (GSNOR^−/−), a denitrosylase that regulates S-nitrosylation. GSNOR^−/− MSCs exhibited markedly diminished capacity for vasculogenesis in an in vitro Matrigel tube–forming assay and in vivo relative to WT MSCs. This decrease was associated with down-regulation of the PDGF receptorα (PDGFRα) in GSNOR^−/− MSCs, a receptor essential for VEGF-A action in MSCs. Pharmacologic inhibition of NO synthase with L-N^G-nitroarginine methyl ester (L-NAME) and stimulation of growth hormone–releasing hormone receptor (GHRHR) with GHRH agonists augmented VEGF-A production and normalized tube formation in GSNOR^−/− MSCs, whereas NO donors or PDGFR antagonist reduced tube formation ∼50% by murine and human MSCs. The antagonist also blocked the rescue of tube formation in GSNOR^−/− MSCs by L-NAME or the GHRH agonists JI-38, MR-409, and MR-356. Therefore, GSNOR^−/− MSCs have a deficient capacity for endothelial differentiation due to downregulation of PDGFRα related to NO/GSNOR imbalance. These findings unravel important aspects of modulation of MSCs by VEGF-A activation of the PDGFR and illustrate a paradoxical inhibitory role of S-nitrosylation signaling in MSC vasculogenesis. Accordingly, disease states characterized by NO deficiency may trigger MSC-mediated vasculogenesis. These findings have important implications for therapeutic application of GHRH agonists to ischemic disorders.     

From the Cover: Species fluctuations sustained by a cyclic succession at the edge of chaos

Although mathematical models and laboratory experiments have shown that species interactions can generate chaos, field evidence of chaos in natural ecosystems is rare. We report on a pristine rocky intertidal community located in one of the world’s oldest marine reserves that has displayed a complex cyclic succession for more than 20 y. Bare rock was colonized by barnacles and crustose algae, they were overgrown by mussels, and the subsequent detachment of the mussels returned bare rock again. These processes generated irregular species fluctuations, such that the species coexisted over many generations without ever approaching a stable equilibrium state. Analysis of the species fluctuations revealed a dominant periodicity of about 2 y, a global Lyapunov exponent statistically indistinguishable from zero, and local Lyapunov exponents that alternated systematically between negative and positive values. This pattern indicates that the community moved back and forth between stabilizing and chaotic dynamics during the cyclic succession. The results are supported by a patch-occupancy model predicting similar patterns when the species interactions were exposed to seasonal variation. Our findings show that natural ecosystems can sustain continued changes in species abundances and that seasonal forcing may push these nonequilibrium dynamics to the edge of chaos.Since ancient times, it is often argued that undisturbed ecosystems will approach some form of stable equilibrium, at which the populations of the species are maintained at relatively constant numbers (1, 2). However, ecological studies have criticized this idea of “the balance of nature” by pointing out that species abundances in natural ecosystems may remain in a perpetual state of change (3–5). For instance, intransitive competition can lead to a cyclic succession, supporting continued changes in community composition as the dominance is passed on from one species to another in an eternal loop (6–10). Recent theory predicts that seasonal forcing of a cyclic succession can produce quasiperiodic and chaotic species fluctuations (11, 12). Chaos has attracted ecologists’ attention, because it limits the long-term predictability of species abundances (13) and because these nonequilibrium dynamics can potentially sustain a high biodiversity (9). Chaos is predicted by various mathematical models (9, 14–16) and has been found in laboratory experiments with insect populations (17), microbial food webs (18), and plankton communities (5). However, field evidence of chaos in natural ecosystems is rare (19–21) and has never been documented in relation to cyclic succession.Chaos is commonly described as bounded aperiodic dynamics of a deterministic system that exhibits sensitive dependence on initial conditions (22). Sensitivity to initial conditions implies that small initial differences will grow exponentially in time, such that long-term prediction becomes impossible. In practice, however, a clear distinction between deterministic and stochastic fluctuations is often impossible, because the intrinsic dynamics of natural systems are influenced by exogenous stochastic variation. For instance, species fluctuations are not only caused by competition and predation but also affected by “environmental noise” generated by stochastic variation in weather conditions. During recent decades, considerable advances have been made in the analysis of chaos in the presence of noise (23–25). In particular, sensitive dependence on initial conditions can be estimated for noisy systems using Lyapunov exponents that quantify the extent to which environmental perturbations are amplified (or damped) by the intrinsic dynamics of the system.Here, we investigate the species dynamics of a rocky intertidal community in the Cape Rodney-Okakari Point Marine Reserve on the North Island of New Zealand (Fig. 1A). This reserve was established in 1975 as the first marine reserve in New Zealand. It offers ideal conditions for long-term studies of species interactions, because anthropogenic impacts have been kept to a minimum for several decades (26, 27). The rocky intertidal community is dominated by three sessile species: the honeycomb barnacle Chamaesipho columna (Spengler, 1790), the crustose brown alga Ralfsia cf confusa (described as Pseudolithoderma sp. in ref. 28), and the little black mussel Xenostrobus pulex (Lamarck, 1819). Interactions between these species have been described in previous studies (28–30). Barnacles colonize bare rock by gregarious settlement, developing extensive sheets that cover the rocky surface (29). Crustose algae settle on top of the barnacles but do not harm them. Rather, the crustose algae leave space for the barnacles’ waving cirri and benefit from nutrients released by barnacles (28). Xenostrobus mussel larvae cannot settle on smooth bare rock, but they settle gregariously on top of barnacles and crustose algae (29, 30). Xenostrobus mussels subsequently develop a dense carpet, killing the barnacles underneath. After the dead barnacles detach from the underlying rock, the mussel carpet is no longer anchored to any solid surface, and it is washed away by the daily tides (29). Hence, bare rock becomes available again, and the species succession starts anew (Fig. 1B).Open in a separate windowFig. 1.The rocky intertidal community. (A) Aerial view of the study site at Goat Island Bay. (B) Cyclic succession at the rocky intertidal site. First, barnacles settle on bare rock, and second, crustose algae invade. Third, mussels settle on top of the barnacles and crustose algae, forming a dense carpet that smothers the barnacles and algae underneath. Fourth, the mussels detach, bare rock becomes available again, and the cycle restarts. Drawn by Jan van Arkel (University of Amsterdam, Amsterdam, The Netherlands). (C) Time series were obtained from a permanent grid consisting of 20 plots and five nodes (A–E). The percentages of cover of barnacles, crustose algae, and bare rock were monitored in the plots, whereas mussel cover was estimated from photographs of the nodes. Ten plots and five nodes within the red line were used for the time series analysis.This paper analyzes the species fluctuations resulting from this hypothesized cyclic succession. Species abundances (expressed as percentage of cover) were monitored on a monthly basis for more than 20 y using a permanent grid (Fig. 1C and SI Appendix, Figs. S1–S5). We use the time series to determine common periodicities in the species fluctuations indicative of a cyclic succession and estimate local and global Lyapunov exponents as indicators of the potential presence of chaos. Finally, we compare the obtained results against a simple patch-occupancy model to assess whether the species interactions described above can, indeed, produce a cyclic succession characterized by chaotic species fluctuations.     

From the Cover: Outsourcing CO2 within China

Recent studies have shown that the high standard of living enjoyed by people in the richest countries often comes at the expense of CO₂ emissions produced with technologies of low efficiency in less affluent, developing countries. Less apparent is that this relationship between developed and developing can exist within a single country’s borders, with rich regions consuming and exporting high-value goods and services that depend upon production of low-cost and emission-intensive goods and services from poorer regions in the same country. As the world’s largest emitter of CO₂, China is a prominent and important example, struggling to balance rapid economic growth and environmental sustainability across provinces that are in very different stages of development. In this study, we track CO₂ emissions embodied in products traded among Chinese provinces and internationally. We find that 57% of China’s emissions are related to goods that are consumed outside of the province where they are produced. For instance, up to 80% of the emissions related to goods consumed in the highly developed coastal provinces are imported from less developed provinces in central and western China where many low–value-added but high–carbon-intensive goods are produced. Without policy attention to this sort of interprovincial carbon leakage, the less developed provinces will struggle to meet their emissions intensity targets, whereas the more developed provinces might achieve their own targets by further outsourcing. Consumption-based accounting of emissions can thus inform effective and equitable climate policy within China.     

From the Cover: Defense mutualisms enhance plant diversification

The ability of plants to form mutualistic relationships with animal defenders has long been suspected to influence their evolutionary success, both by decreasing extinction risk and by increasing opportunity for speciation through an expanded realized niche. Nonetheless, the hypothesis that defense mutualisms consistently enhance plant diversification across lineages has not been well tested due to a lack of phenotypic and phylogenetic information. Using a global analysis, we show that the >100 vascular plant families in which species have evolved extrafloral nectaries (EFNs), sugar-secreting organs that recruit arthropod mutualists, have twofold higher diversification rates than families that lack species with EFNs. Zooming in on six distantly related plant clades, trait-dependent diversification models confirmed the tendency for lineages with EFNs to display increased rates of diversification. These results were consistent across methodological approaches. Inference using reversible-jump Markov chain Monte Carlo (MCMC) to model the placement and number of rate shifts revealed that high net diversification rates in EFN clades were driven by an increased number of positive rate shifts following EFN evolution compared with sister clades, suggesting that EFNs may be indirect facilitators of diversification. Our replicated analysis indicates that defense mutualisms put lineages on a path toward increased diversification rates within and between clades, and is concordant with the hypothesis that mutualistic interactions with animals can have an impact on deep macroevolutionary patterns and enhance plant diversity.Ever since the key innovation hypothesis was first proposed in the 1940s (1, 2), the origination of novel traits has been a popular yet controversial explanation for the exceptional disparity in species richness observed across clades in the tree of life. Despite decades of research linking traits to diversification, we have remarkably few examples of traits that have been convincingly demonstrated to spur diversification repeatedly across independent, distantly related groups. Notable exceptions include a number of ecologically important traits mediating interactions between plants and animals (3–6), suggesting that these interactions may be particularly important drivers of macroevolutionary patterns. Here, we test the hypothesis that plant defense mutualisms, a widespread and classically studied ecological interaction whereby plants provide food rewards to arthropod bodyguards in return for protection against natural enemies (7), increase the evolutionary diversification rate of the plant lineages that participate in them. The morphological traits that mediate defense mutualisms represent well-studied examples of characters hypothesized to expand a plant’s niche via interactions with mutualists and influence species success in various environmental contexts (8). Although the costs and benefits of participating in defense mutualisms are well studied (9), the hypothesis that the ecological impact of defense mutualisms leaves a predictable macroevolutionary signature, increasing lineage diversification within and among clades of plants, has only been examined in a single genus (10).Defense mutualisms may have an impact on plant speciation and extinction rates via several mechanisms. Unlike the evolution of traits related to reproduction, which, more intuitively, could have an impact on lineage diversification (e.g., refs. 5, 11), the direct mechanism by which defense mutualisms are hypothesized to influence diversification is less obvious. One direct mechanism is a decreased incidence of damage and disease due to an enhanced defensive repertoire, which may allow for increased population sizes and, in turn, lower extinction rates (6). Additionally, by expanding the realized niche of a plant (12), defense mutualisms may broaden the range of habitats a plant can occupy (10), thereby increasing instances of allopatric speciation.However, in addition to these direct mechanisms, the evolution of mutualistic traits may facilitate diversification indirectly. First, if niche expansion results in the successful occupation of more environments, mutualistic traits may increase the probability a lineage will encounter conditions ripe with ecological opportunity (e.g., new adaptive zones), which, in turn, will drive increases in diversification. In other words, the evolution of a trait may enable subsequent diversification via increasing exposure to new environments, some of which will harbor external drivers of radiation, such as the uplift of a mountain range or unoccupied niches. Second, the evolution of defense mutualisms may free up resources for the plant, and thereby facilitate the evolution of other innovative traits that subsequently enhance diversification. These indirect effects need not be contingent on the existence of the direct effects mentioned above, and represent a largely overlooked hypothesis concerning how traits can affect diversification (13–15).We suggest that indirect impacts of trait evolution on diversification should be reflected in a phylogenetic pattern in which the origination of a trait is followed by an increased probability of subsequent, downstream rate shifts relative to clades that lack the trait (Fig. 1). Because the indirect effect of the trait is contingent upon additional conditions (e.g., ecological opportunity, the evolution of another trait), there may be a substantial lag between the origin of the trait and rate shifts. Alternatively, a direct effect of the trait on the diversification rate is consistent with a pattern whereby a sustained rate shift occurs concomitantly with, or on the same branch as, the origin of the trait on the phylogeny (Fig. 1). Direct and indirect patterns are not mutually exclusive, and both patterns may be detectable on a single phylogeny (Fig. 1).Open in a separate windowFig. 1.A conceptualization of phylogenetic patterns consistent with direct or indirect effects of EFNs (or any trait) on lineage diversification. A net change in diversification may be due to direct or indirect mechanisms. In the Upper Right, a rate shift occurs concomitantly with the origin of EFNs, consistent with a direct effect. If one or more shifts occur with some delay (Lower), this is consistent with a hypothesis that a trait has an indirect or context-dependent effect on diversification rates.We focus on the macroevolutionary consequences of the repeated origination of extrafloral nectaries (EFNs), nectar-secreting glands found on nonfloral plant tissues that provide food for a wide array of beneficial arthropod bodyguards (16). EFNs are well studied ecologically, and their only known function is defense against herbivores and microbial pathogens by attracting natural enemies (17). Such features have evolved hundreds of times and occur in about a quarter of all vascular plant families (18). Here, we first ask whether, across all vascular plants, families containing species with EFNs are associated with higher diversification rates than families without EFNs. We then focus in on the phylogenetic history and evolution of EFNs in six distantly related plant clades to evaluate whether EFNs are linked, directly or indirectly, to increased lineage diversification rates. As such, this study represents a replicated, multiscale test of the macroevolutionary consequences of a convergently evolved and ecologically important mutualistic trait.     

From the Cover: Spiral precipitation patterns in confined chemical gardens

Chemical gardens are mineral aggregates that grow in three dimensions with plant-like forms and share properties with self-assembled structures like nanoscale tubes, brinicles, or chimneys at hydrothermal vents. The analysis of their shapes remains a challenge, as their growth is influenced by osmosis, buoyancy, and reaction–diffusion processes. Here we show that chemical gardens grown by injection of one reactant into the other in confined conditions feature a wealth of new patterns including spirals, flowers, and filaments. The confinement decreases the influence of buoyancy, reduces the spatial degrees of freedom, and allows analysis of the patterns by tools classically used to analyze 2D patterns. Injection moreover allows the study in controlled conditions of the effects of variable concentrations on the selected morphology. We illustrate these innovative aspects by characterizing quantitatively, with a simple geometrical model, a new class of self-similar logarithmic spirals observed in a large zone of the parameter space.Chemical gardens, discovered more than three centuries ago (1), are attracting nowadays increasing interest in disciplines as varied as chemistry, physics, nonlinear dynamics, and materials science. Indeed, they exhibit rich chemical, magnetic, and electrical properties due to the steep pH and electrochemical gradients established across their walls during their growth process (2). Moreover, they share common properties with structures ranging from nanoscale tubes in cement (3), corrosion filaments (4) to larger-scale brinicles (5), or chimneys at hydrothermal vents (6). This explains their success as prototypes to grow complex compartmentalized or layered self-organized materials, as chemical motors, as fuel cells, in microfluidics, as catalysts, and to study the origin of life (7–18). However, despite numerous experimental studies, understanding the properties of the wide variety of possible spatial structures and developing theoretical models of their growth remains a challenge.In 3D systems, only a qualitative basic picture for the formation of these structures is known. Precipitates are typically produced when a solid metal salt seed dissolves in a solution containing anions such as silicate. Initially, a semipermeable membrane forms, across which water is pumped by osmosis from the outer solution into the metal salt solution, further dissolving the salt. Above some internal pressure, the membrane breaks, and a buoyant jet of the generally less dense inner solution then rises and further precipitates in the outer solution, producing a collection of mineral shapes that resembles a garden. The growth of chemical gardens is thus driven in 3D by a complex coupling between osmotic, buoyancy, and reaction–diffusion processes (19, 20).Studies have attempted to generate reproducible micro- and nanotubes by reducing the erratic nature of the 3D growth of chemical gardens (10, 11, 13, 15, 21). They have for instance been studied in microgravity to suppress buoyancy (22, 23), or by injecting aqueous solutions of metallic salts directly into silicate solutions in 3D to dominate osmotic processes by controlled flows (10, 11). Analysis of their microstructure has also been done for different metallic salts, showing a difference of chemical composition on the inner and the outer tube surfaces (24, 25). The experimental characterization and modeling of the dynamics remains however dauntingly complex in 3D, which explains why progress in quantitative analysis remains so scarce.We show here that growing chemical gardens in a confined quasi-2D geometry by injecting one reagent solution into the other provides an innovative path to discover numerous original patterns, characterize quantitatively their properties, and explain their growth mechanism. A large variety of structures including spirals, filaments, worms, and flowers is obtained in a horizontal confined geometry when varying the reagent concentrations at a fixed flow rate. The patterns differ from those in 3D as the growth methodology decouples the different effects involved in the formation of classical chemical gardens. The buoyancy force is reduced by the vertical confinement, whereas injection decreases the influence of osmotic effects.     

From the Cover: Behavioral assessment of sensitivity to intracortical microstimulation of primate somatosensory cortex

Intracortical microstimulation (ICMS) is a powerful tool to investigate the functional role of neural circuits and may provide a means to restore sensation for patients for whom peripheral stimulation is not an option. In a series of psychophysical experiments with nonhuman primates, we investigate how stimulation parameters affect behavioral sensitivity to ICMS. Specifically, we deliver ICMS to primary somatosensory cortex through chronically implanted electrode arrays across a wide range of stimulation regimes. First, we investigate how the detectability of ICMS depends on stimulation parameters, including pulse width, frequency, amplitude, and pulse train duration. Then, we characterize the degree to which ICMS pulse trains that differ in amplitude lead to discriminable percepts across the range of perceptible and safe amplitudes. We also investigate how discriminability of pulse amplitude is modulated by other stimulation parameters—namely, frequency and duration. Perceptual judgments obtained across these various conditions will inform the design of stimulation regimes for neuroscience and neuroengineering applications.Intracortical microstimulation (ICMS) is an important tool to investigate the functional role of neural circuits (1, 2). In a famous example, microstimulation of neurons in the middle temporal area was found to bias the perceived direction of visual motion stimuli, causally implicating these neurons in the computation of visual motion direction (3). Experiments with ICMS of somatosensory cortex showed that changing the frequency of stimulation elicited discriminable percepts, demonstrating that temporal patterning of cortical responses has perceptual correlates (4). Building on the success of these and other studies, ICMS has been proposed as an approach to restore perception in individuals who have lost it, for example in visual neuroprostheses for the blind (5, 6) or somatosensory neuroprostheses for tetraplegic patients (7–11). In the present study, we sought to characterize the psychometric properties of ICMS delivered to primary somatosensory cortex (S1) across a wide range of stimulation regimes. In psychophysical experiments with Rhesus macaques, we first measured the detectability of ICMS pulse trains and assessed its dependence on a variety of stimulation parameters. We then measured the degree to which animals could discriminate pairs of ICMS pulse trains that differed in amplitude. In both the detection and discrimination experiments, ICMS parameters—amplitude, pulse width, pulse train duration, and pulse train frequency—spanned the range that is detectable and has been typically deemed safe (12–14). Results from the present experiments will inform the design of future studies involving ICMS as well as the development of sensory encoding algorithms for neuroprostheses.     

From the Cover: The skeleton of tropical intraseasonal oscillations

The Madden–Julian oscillation (MJO) is the dominant mode of variability in the tropical atmosphere on intraseasonal timescales and planetary spatial scales. Despite the primary importance of the MJO and the decades of research progress since its original discovery, a generally accepted theory for its essential mechanisms has remained elusive. Here, we present a minimal dynamical model for the MJO that recovers robustly its fundamental features (i.e., its “skeleton”) on intraseasonal/planetary scales: (i) the peculiar dispersion relation of dω/dk ≈ 0, (ii) the slow phase speed of ≈5 m/s, and (iii) the horizontal quadrupole vortex structure. This is accomplished here in a model that is neutrally stable on planetary scales; i.e., it is tacitly assumed that the primary instabilities occur on synoptic scales. The key premise of the model is that modulations of synoptic scale wave activity are induced by low-level moisture preconditioning on planetary scales, and they drive the “skeleton” of the MJO through modulated heating. The “muscle” of the MJO—including tilts, vertical structure, etc.—is contributed by other potential upscale transport effects from the synoptic scales.     

From the Cover: PNAS Plus: Intrathecal gene therapy rescues a model of demyelinating peripheral neuropathy

Inherited demyelinating peripheral neuropathies are progressive incurable diseases without effective treatment. To develop a gene therapy approach targeting myelinating Schwann cells that can be translatable, we delivered a lentiviral vector using a single lumbar intrathecal injection and a myelin-specific promoter. The human gene of interest, GJB1, which is mutated in X-linked Charcot–Marie–Tooth Disease (CMT1X), was delivered intrathecally into adult Gjb1-null mice, a genetically authentic model of CMT1X that develops a demyelinating peripheral neuropathy. We obtained widespread, stable, and cell-specific expression of connexin32 in up to 50% of Schwann cells in multiple lumbar spinal roots and peripheral nerves. Behavioral and electrophysiological analysis revealed significantly improved motor performance, quadriceps muscle contractility, and sciatic nerve conduction velocities. Furthermore, treated mice exhibited reduced numbers of demyelinated and remyelinated fibers and fewer inflammatory cells in lumbar motor roots, as well as in the femoral motor and sciatic nerves. This study demonstrates that a single intrathecal lentiviral gene delivery can lead to Schwann cell-specific expression in spinal roots extending to multiple peripheral nerves. This clinically relevant approach improves the phenotype of an inherited neuropathy mouse model and provides proof of principle for treating inherited demyelinating neuropathies.Inherited demyelinating neuropathies result from genetic defects in a variety of genes that are expressed by myelinating Schwann cells (1). These mutations are thought to cause demyelination in a cell-autonomous manner. Recessively inherited disorders cause loss of function, and dominantly inherited disorders cause haplotype insufficiency or toxic gain of function (2, 3). Achieving a therapeutic correction of these genetic defects requires either gene replacement or gene silencing approaches, ideally confined to myelinating Schwann cells (4).Various techniques for gene delivery to peripheral nerves have been attempted, including adenoviral (AV) and adeno-associated viral (AAV) vectors and ubiquitous promoters (5). Intramuscular and direct intraneural injections help restrict expression to Schwann cells, but the duration of expression is typically limited. Lentiviral vectors produce sustained expression and have been injected intraneurally in crushed sciatic nerves to achieve retrograde transport and gene expression in motor neurons (6) and locally to transduce Schwann cells (7). None of the approaches published to date has provided a Schwann cell-specific gene delivery method to achieve widespread and stable expression.We recently reported Schwann cell-specific expression driven by the rat myelin protein zero (Mpz) promoter of a neuropathy gene following intraneural lentiviral vector delivery, alleviating pathological changes in a model of X-linked Charcot–Marie–Tooth disease (CMT1X) (8). Expression was restricted to the injected sciatic nerve, however, thus limiting its usefulness for clinical applications.Here we report a gene delivery approach via a single lumbar intrathecal injection leading to stable Schwann cell gene expression in an unexpectedly widespread distribution—the lumbar spinal roots and along the entire length of the femoral and sciatic nerves. Using this approach to treat a mouse model of CMT1X resulted in significant behavioral, functional, and morphological improvement, providing an important advance toward treating inherited neuropathies.     

From the Cover: Using selection bias to explain the observed structure of Internet diffusions

Recently, large datasets stored on the Internet have enabled the analysis of processes, such as large-scale diffusions of information, at new levels of detail. In a recent study, Liben-Nowell and Kleinberg [(2008) Proc Natl Acad Sci USA 105:4633–4638] observed that the flow of information on the Internet exhibits surprising patterns whereby a chain letter reaches its typical recipient through long paths of hundreds of intermediaries. We show that a basic Galton–Watson epidemic model combined with the selection bias of observing only large diffusions suffices to explain these patterns. Thus, selection biases of which data we observe can radically change the estimation of classical diffusion processes.     

From the Cover: Climate shock effects and mediation in fisheries

Climate shocks can reorganize the social–ecological linkages in food-producing communities, leading to a sudden loss of key products in food systems. The extent and persistence of this reorganization are difficult to observe and summarize, but are critical aspects of predicting and rapidly assessing community vulnerability to extreme events. We apply network analysis to evaluate the impact of a climate shock—an unprecedented marine heatwave—on patterns of resource use in California fishing communities, which were severely affected through closures of the Dungeness crab fishery. The climate shock significantly modified flows of users between fishery resources during the closures. These modifications were predicted by pre-shock patterns of resource use and were associated with three strategies used by fishing community member vessels to respond to the closures: temporary exit from the food system, spillover of effort from the Dungeness crab fishery into other fisheries, and spatial shifts in where crab were landed. Regional differences in resource use patterns and vessel-level responses highlighted the Dungeness crab fishery as a seasonal “gilded trap” for northern California fishing communities. We also detected disparities in climate shock response based on vessel size, with larger vessels more likely to display spatial mobility. Our study demonstrates the importance of highly connected and decentralized networks of resource use in reducing the vulnerability of human communities to climate shocks.

Climate shocks threaten food systems around the world and are expected to increase in frequency and intensity under climate change (1–5). Distinct from climate change (e.g., long-term warming), climate shocks rapidly outstrip the capacity of a system to cope by inflicting unexpected and highly concentrated damage (6). Vulnerability of communities to climate shocks varies within and across food systems, depending on the severity of the shock and the sensitivity and adaptive capacity of community members (7). Communities that form the harvesting and processing base of food systems—especially agrarian and fishing communities—are often among the most vulnerable to climate shocks (8), as their resource-based economies operate at the interface of environment and society. Marine heatwaves represent one such climate shock of growing importance, as they impact fishing communities by compromising seafood safety, shifting species distributions, and lowering recruitment and survival of fished species (9–12).Diversifying harvest portfolios is one strategy used by fishers to manage risk (13–16). If marine heatwaves disproportionately affect a subset of species, fishers may respond by shifting participation into less affected fisheries. This response, referred to as “leakage” or “spillover” (17–21), restructures the networks that form as fishers participate in multiple fisheries (19–21). The topology of these fisheries participation networks can reveal the extent to which climate shocks lead to indirect or lasting changes in patterns of resource use within fishing communities and, by drawing on network theory, indicate the sensitivity of these communities to perturbations (18).The 2014–2016 North Pacific marine heatwave (12, 22) was a climate shock that led to a massive harmful algal bloom (HAB), contaminating Dungeness crab with biotoxins and compelling state managers to coordinate fishery closures along the entire US West Coast (23). In California, where the Dungeness crab fishery represents ∼26% of all annual fishery revenue (California Department of Fish and Wildlife; https://wildlife.ca.gov) and supports >25% of all commercial fishing vessels (Pacific Fisheries Information Network; http://pacfin.psmfc.org), the HAB significantly delayed the 2015–16 commercial Dungeness crab fishing season (24). California Dungeness crab landings for the 2015–16 season reached only 52% of the average catch from the previous 5 y, spurring Congress to appropriate >$25 million in federal disaster relief funding (25). Dungeness crab fishers reported shifting participation to alternative fisheries during the 2015–16 season to offset socioeconomic impacts (26, 27); however, to date there has been no quantitative demonstration of spillover from the Dungeness crab fishery, or analysis of how the resulting changes in fisheries participation networks may have varied geographically and persisted after the closures were lifted.Our study examined the impact of the 2015–16 Dungeness crab fishery closures (hereafter 2016 closures) on patterns of resource use in California fishing communities. We considered seven fishing communities representing a total of 2,516 individual fishing vessels (Table 1). We found significant changes in fisheries participation network topology during the 2016 closures, which corresponded with a severe reduction in fishing activity, spillover of fishing effort from the Dungeness crab fishery, and spatial variation in pre-shock network topology. Our analysis captured changing patterns of resource use during a severe climate shock, and demonstrated how this emergent social outcome in fishing communities can be predicted by pre-shock network metrics and related to the adaptive strategies of community member vessels. We discuss the implications of fishery management measures for adaptive decision making and network structure, and provide recommendations for sustainable fishery management during climate shocks.Table 1.Ports of landing and vessel counts for the seven California fishing communities included in this study