Michael Werner

Don’t edit the human germ line

use of genome-editing tools to modify the DNA of human embryos will be published shortly. There are grave concerns regarding the ethical and safety implications of this research. There is also fear of the negative impact it could have on important work involving the use of genome-editing techniques in somatic (non-reproductive) cells. We are all involved in this latter area of work. One of us (F.U.) helped to develop the first genome-editing technology, zinc-finger nucleases (ZFNs), and is now senior scientist at the company developing them, Sangamo BioSciences of Richmond, California. The Alliance for Regenerative Medicine (ARM; in which E.L., M.W. and S.E.H. are involved), is an international organization that represents more than 200 life-sciences companies, research institutions, non-profit organizations, patient-advocacy groups and investors focused on developing and commercializing therapeutics, including those involving genome editing. Genome-editing technologies may offer a powerful approach to treat many human diseases, including HIV/AIDS, haemophilia, sickle-cell anaemia and several forms of cancer. All techniques currently in various stages of clinical development focus on modifying the genetic material of somatic cells, such as T cells (a type of white blood cell). These are not designed to affect sperm or eggs. In our view, genome editing in human embryos using current technologies could have unpredictable effects on future generations. This makes it dangerous and ethically unacceptable. Such research could be exploited for non-therapeutic modifications. We are concerned that a public outcry about such an ethical breach could hinder a promising area of therapeutic development, namely making genetic changes that cannot be inherited. At this early stage, scientists should agree not to modify the DNA of human reproductive cells. Should a truly compelling case ever arise for the therapeutic benefit of germ line modification, we encourage an open discussion around the appropriate course of action.

Specialization of mutualistic interaction networks decreases toward tropical latitudes.

Species-rich tropical communities are expected to be more specialized than their temperate counterparts. Several studies have reported increasing biotic specialization toward the tropics, whereas others have not found latitudinal trends once accounting for sampling bias or differences in plant diversity. Thus, the direction of the latitudinal specialization gradient remains contentious. With an unprecedented global data set, we investigated how biotic specialization between plants and animal pollinators or seed dispersers is associated with latitude, past and contemporary climate, and plant diversity. We show that in contrast to expectation, biotic specialization of mutualistic networks is significantly lower at tropical than at temperate latitudes. Specialization was more closely related to contemporary climate than to past climate stability, suggesting that current conditions have a stronger effect on biotic specialization than historical community stability. Biotic specialization decreased with increasing local and regional plant diversity. This suggests that high specialization of mutualistic interactions is a response of pollinators and seed dispersers to low plant diversity. This could explain why the latitudinal specialization gradient is reversed relative to the latitudinal diversity gradient. Low mutualistic network specialization in the tropics suggests higher tolerance against extinctions in tropical than in temperate communities.

Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality

Many experiments have shown that loss of biodiversity reduces the capacity of ecosystems to provide the multiple services on which humans depend. However, experiments necessarily simplify the complexity of natural ecosystems and will normally control for other important drivers of ecosystem functioning, such as the environment or land use. In addition, existing studies typically focus on the diversity of single trophic groups, neglecting the fact that biodiversity loss occurs across many taxa and that the functional effects of any trophic group may depend on the abundance and diversity of others. Here we report analysis of the relationships between the species richness and abundance of nine trophic groups, including 4,600 above- and below-ground taxa, and 14 ecosystem services and functions and with their simultaneous provision (or multifunctionality) in 150 grasslands. We show that high species richness in multiple trophic groups (multitrophic richness) had stronger positive effects on ecosystem services than richness in any individual trophic group; this includes plant species richness, the most widely used measure of biodiversity. On average, three trophic groups influenced each ecosystem service, with each trophic group influencing at least one service. Multitrophic richness was particularly beneficial for ‘regulating’ and ‘cultural’ services, and for multifunctionality, whereas a change in the total abundance of species or biomass in multiple trophic groups (the multitrophic abundance) positively affected supporting services. Multitrophic richness and abundance drove ecosystem functioning as strongly as abiotic conditions and land-use intensity, extending previous experimental results to real-world ecosystems. Primary producers, herbivorous insects and microbial decomposers seem to be particularly important drivers of ecosystem functioning, as shown by the strong and frequent positive associations of their richness or abundance with multiple ecosystem services. Our results show that multitrophic richness and abundance support ecosystem functioning, and demonstrate that a focus on single groups has led to researchers to greatly underestimate the functional importance of biodiversity.

Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition

Abstract Global change, especially land‐use intensification, affects human well‐being by impacting the delivery of multiple ecosystem services (multifunctionality). However, whether biodiversity loss is a major component of global change effects on multifunctionality in real‐world ecosystems, as in experimental ones, remains unclear. Therefore, we assessed biodiversity, functional composition and 14 ecosystem services on 150 agricultural grasslands differing in land‐use intensity. We also introduce five multifunctionality measures in which ecosystem services were weighted according to realistic land‐use objectives. We found that indirect land‐use effects, i.e. those mediated by biodiversity loss and by changes to functional composition, were as strong as direct effects on average. Their strength varied with land‐use objectives and regional context. Biodiversity loss explained indirect effects in a region of intermediate productivity and was most damaging when land‐use objectives favoured supporting and cultural services. In contrast, functional composition shifts, towards fast‐growing plant species, strongly increased provisioning services in more inherently unproductive grasslands.

Landscape simplification filters species traits and drives biotic homogenization

Biodiversity loss can affect the viability of ecosystems by decreasing the ability of communities to respond to environmental change and disturbances. Agricultural intensification is a major driver of biodiversity loss and has multiple components operating at different spatial scales: from in-field management intensity to landscape-scale simplification. Here we show that landscape-level effects dominate functional community composition and can even buffer the effects of in-field management intensification on functional homogenization, and that animal communities in real-world managed landscapes show a unified response (across orders and guilds) to both landscape-scale simplification and in-field intensification. Adults and larvae with specialized feeding habits, species with shorter activity periods and relatively small body sizes are selected against in simplified landscapes with intense in-field management. Our results demonstrate that the diversity of land cover types at the landscape scale is critical for maintaining communities, which are functionally diverse, even in landscapes where in-field management intensity is high.

Interannual variation in land-use intensity enhances grassland multidiversity

Significance Land-use intensification is a major threat to biodiversity. So far, however, studies on biodiversity impacts of land-use intensity (LUI) have been limited to a single or few groups of organisms and have not considered temporal variation in LUI. Therefore, we examined total ecosystem biodiversity in grasslands varying in LUI with a newly developed index called multidiversity, which integrates the species richness of 49 different organism groups ranging from bacteria to birds. Multidiversity declined strongly with increasing LUI, but changing LUI across years increased multidiversity, particularly of rarer species. We conclude that encouraging farmers to change the intensity of their land use over time could be an important strategy to maintain high biodiversity in grasslands. Although temporal heterogeneity is a well-accepted driver of biodiversity, effects of interannual variation in land-use intensity (LUI) have not been addressed yet. Additionally, responses to land use can differ greatly among different organisms; therefore, overall effects of land-use on total local biodiversity are hardly known. To test for effects of LUI (quantified as the combined intensity of fertilization, grazing, and mowing) and interannual variation in LUI (SD in LUI across time), we introduce a unique measure of whole-ecosystem biodiversity, multidiversity. This synthesizes individual diversity measures across up to 49 taxonomic groups of plants, animals, fungi, and bacteria from 150 grasslands. Multidiversity declined with increasing LUI among grasslands, particularly for rarer species and aboveground organisms, whereas common species and belowground groups were less sensitive. However, a high level of interannual variation in LUI increased overall multidiversity at low LUI and was even more beneficial for rarer species because it slowed the rate at which the multidiversity of rare species declined with increasing LUI. In more intensively managed grasslands, the diversity of rarer species was, on average, 18% of the maximum diversity across all grasslands when LUI was static over time but increased to 31% of the maximum when LUI changed maximally over time. In addition to decreasing overall LUI, we suggest varying LUI across years as a complementary strategy to promote biodiversity conservation.

Land‐use impacts on plant–pollinator networks: interaction strength and specialization predict pollinator declines

Land use is known to reduce the diversity of species and complexity of biotic interactions. In theory, interaction networks can be used to predict the sensitivity of species against co-extinction, but this has rarely been applied to real ecosystems facing variable land-use impacts. We investigated plant-pollinator networks on 119 grasslands that varied quantitatively in management regime, yielding 25401 visits by 741 pollinator species on 166 plant species. Species-specific plant and pollinator responses to land use were significantly predicted by the weighted average land-use response of each species partners. Moreover, more specialized pollinators were more vulnerable than generalists. Both predictions are based on the relative interaction strengths provided by the observed interaction network. Losses in flower and pollinator diversity were linked, and mutual dependence between plants and pollinators accelerates the observed parallel declines in response to land-use intensification. Our findings confirm that ecological networks help to predict natural community responses to disturbance and possible secondary extinctions.

Pollen amino acids and flower specialisation in solitary bees.

Pollen nutrient composition could be important in host-plant selection of oligolectic bees. In this study, pollen samples from 142 plant species were analysed separately for water-soluble and protein-bound amino acids. The composition of amino acids varied strongly among plant species, but taxonomically related species had similar compositions. All plant species contained the entire set of essential amino acids, although some in small quantities. Total concentration of freeand protein-bound amino acids was significantly lower in pollen sources used by oligoleges than in other pollen sources. Pollen sources of oligoleges showed a lower concentration of essential amino acids and deviated more strongly from the ideal composition of essential amino acids as determined for honey bees than plants not hosting oligoleges. However, this trend was not confirmed on a cruder phylogenetic plant family level, where pollen chosen by oligolectic bees was similar to other pollen.ZusammenfassungDie meisten Bienen ernähren sich ausschließlich von Pollen und Nektar, wobei Pollen die primäre Proteinquelle ihrer Larven darstellt. Während oligolektische Bienen auf den Pollen einer oder mehrerer nah verwandter Pflanzenarten spezialisiert sind, ist das Blütenspektrum polylektischer Bienen breiter. Der Vorteil der Oligolektie ist bisher weitgehend unbekannt, wobei eine Vielzahl von Hypothesen diskutiert wird. Dazu gehören eine höhere Effizienz der Pollenspezialisten beim Sammeln und bei der Verdauung des Pollens, sowie eine Spezialisierung auf Pollen mit höherem Stickstoffgehalt. Unser Ziel war, herauszufinden, ob die Pollenqualität, insbesondere der Anteil der essentiellen Aminosäuren (Abb. 1), für die Wahl bestimmter Pflanzenarten durch oligolektische Bienen verantwortlich sein könnte. Die Aminosäurezusammensetzung der Pollen von 142 Pflanzenarten (Tab. I) zeigte signifikante Unterschiede zwischen Pflanzenfamilien (Abb. 2). Von oligolektischen Bienen genutzter Pollen unterschied sich jedoch in der Komposition nicht signifikant von anderen Pollenarten. Allerdings enthielt der von oligolektischen Bienen genutzte Pollen eine signifikant geringere Konzentration an Aminosäuren (Abb. 3). Zudem zeigte sich eine verminderte Nahrungsqualität bei Pollenquellen oligolektischer Bienen: Die Komposition essentieller Aminosäuren zeigte eine signifikant größere Diskrepanz zu der für Honigbienen als ideal beschriebenen Komposition als die übrigen Pollenarten. Daher könnte spekuliert werden, dass oligolektische Bienen nährstoffärmeren Pollen nutzen, um interspezifische Konkurrenz mit anderen Pollenkonsumenten zu verringern. Hinweise auf tatsächlich verminderte Konkurrenz gibt es jedoch bislang nicht. Der Befund, dass oligolektische Bienen auf qualitativ minderwertigen Pollen spezialisiert sind, ist zudem stark geprägt durch die in der Analyse überrepräsentierten Asteraceen und Lamiaceen. Diese weisen ähnlich geringe Aminosäurekonzentrationen auf. Auf Familienniveau zeigte der von oligolektischen Bienen genutzte Pollen keine signifikant geringere Qualität.

Land-use intensification causes multitrophic homogenization of grassland communities.

Land-use intensification is a major driver of biodiversity loss. Alongside reductions in local species diversity, biotic homogenization at larger spatial scales is of great concern for conservation. Biotic homogenization means a decrease in β-diversity (the compositional dissimilarity between sites). Most studies have investigated losses in local (α)-diversity and neglected biodiversity loss at larger spatial scales. Studies addressing β-diversity have focused on single or a few organism groups (for example, ref. 4), and it is thus unknown whether land-use intensification homogenizes communities at different trophic levels, above- and belowground. Here we show that even moderate increases in local land-use intensity (LUI) cause biotic homogenization across microbial, plant and animal groups, both above- and belowground, and that this is largely independent of changes in α-diversity. We analysed a unique grassland biodiversity dataset, with abundances of more than 4,000 species belonging to 12 trophic groups. LUI, and, in particular, high mowing intensity, had consistent effects on β-diversity across groups, causing a homogenization of soil microbial, fungal pathogen, plant and arthropod communities. These effects were nonlinear and the strongest declines in β-diversity occurred in the transition from extensively managed to intermediate intensity grassland. LUI tended to reduce local α-diversity in aboveground groups, whereas the α-diversity increased in belowground groups. Correlations between the β-diversity of different groups, particularly between plants and their consumers, became weaker at high LUI. This suggests a loss of specialist species and is further evidence for biotic homogenization. The consistently negative effects of LUI on landscape-scale biodiversity underscore the high value of extensively managed grasslands for conserving multitrophic biodiversity and ecosystem service provision. Indeed, biotic homogenization rather than local diversity loss could prove to be the most substantial consequence of land-use intensification.

Locally rare species influence grassland ecosystem multifunctionality

Species diversity promotes the delivery of multiple ecosystem functions (multifunctionality). However, the relative functional importance of rare and common species in driving the biodiversity–multifunctionality relationship remains unknown. We studied the relationship between the diversity of rare and common species (according to their local abundances and across nine different trophic groups), and multifunctionality indices derived from 14 ecosystem functions on 150 grasslands across a land-use intensity (LUI) gradient. The diversity of above- and below-ground rare species had opposite effects, with rare above-ground species being associated with high levels of multifunctionality, probably because their effects on different functions did not trade off against each other. Conversely, common species were only related to average, not high, levels of multifunctionality, and their functional effects declined with LUI. Apart from the community-level effects of diversity, we found significant positive associations between the abundance of individual species and multifunctionality in 6% of the species tested. Species-specific functional effects were best predicted by their response to LUI: species that declined in abundance with land use intensification were those associated with higher levels of multifunctionality. Our results highlight the importance of rare species for ecosystem multifunctionality and help guiding future conservation priorities.