Peter A. Henrys

Phenological sensitivity to climate across taxa and trophic levels

Differences in phenological responses to climate change among species can desynchronise ecological interactions and thereby threaten ecosystem function. To assess these threats, we must quantify the relative impact of climate change on species at different trophic levels. Here, we apply a Climate Sensitivity Profile approach to 10,003 terrestrial and aquatic phenological data sets, spatially matched to temperature and precipitation data, to quantify variation in climate sensitivity. The direction, magnitude and timing of climate sensitivity varied markedly among organisms within taxonomic and trophic groups. Despite this variability, we detected systematic variation in the direction and magnitude of phenological climate sensitivity. Secondary consumers showed consistently lower climate sensitivity than other groups. We used mid-century climate change projections to estimate that the timing of phenological events could change more for primary consumers than for species in other trophic levels (6.2 versus 2.5–2.9 days earlier on average), with substantial taxonomic variation (1.1–14.8 days earlier on average).

Warming effects on greenhouse gas fluxes in peatlands are modulated by vegetation composition

Understanding the effects of warming on greenhouse gas feedbacks to climate change represents a major global challenge. Most research has focused on direct effects of warming, without considering how concurrent changes in plant communities may alter such effects. Here, we combined vegetation manipulations with warming to investigate their interactive effects on greenhouse gas emissions from peatland. We found that although warming consistently increased respiration, the effect on net ecosystem CO2 exchange depended on vegetation composition. The greatest increase in CO2 sink strength after warming was when shrubs were present, and the greatest decrease when graminoids were present. CH4 was more strongly controlled by vegetation composition than by warming, with largest emissions from graminoid communities. Our results show that plant community composition is a significant modulator of greenhouse gas emissions and their response to warming, and suggest that vegetation change could alter peatland carbon sink strength under future climate change.

Country-specific effects of neonicotinoid pesticides on honey bees and wild bees

Damage confirmed Early studies of the impacts of neonicotinoid insecticides on insect pollinators indicated considerable harm. However, lingering criticism was that the studies did not represent field-realistic levels of the chemicals or prevailing environmental conditions. Two studies, conducted on different crops and on two continents, now substantiate that neonicotinoids diminish bee health (see the Perspective by Kerr). Tsvetkov et al. find that bees near corn crops are exposed to neonicotinoids for 3 to 4 months via nontarget pollen, resulting in decreased survival and immune responses, especially when coexposed to a commonly used agrochemical fungicide. Woodcock et al., in a multicounty experiment on rapeseed in Europe, find that neonicotinoid exposure from several nontarget sources reduces overwintering success and colony reproduction in both honeybees and wild bees. These field results confirm that neonicotinoids negatively affect pollinator health under realistic agricultural conditions. Science, this issue p. 1395, p. 1393; see also p. 1331 Bee health is affected by neonicotinoids under field-realistic conditions across crops conditions. Neonicotinoid seed dressings have caused concern world-wide. We use large field experiments to assess the effects of neonicotinoid-treated crops on three bee species across three countries (Hungary, Germany, and the United Kingdom). Winter-sown oilseed rape was grown commercially with either seed coatings containing neonicotinoids (clothianidin or thiamethoxam) or no seed treatment (control). For honey bees, we found both negative (Hungary and United Kingdom) and positive (Germany) effects during crop flowering. In Hungary, negative effects on honey bees (associated with clothianidin) persisted over winter and resulted in smaller colonies in the following spring (24% declines). In wild bees (Bombus terrestris and Osmia bicornis), reproduction was negatively correlated with neonicotinoid residues. These findings point to neonicotinoids causing a reduced capacity of bee species to establish new populations in the year following exposure.

Spatial patterns reveal negative density dependence and habitat associations in tropical trees

Understanding how plant species coexist in tropical rainforests is one of the biggest challenges in community ecology. One prominent hypothesis suggests that rare species are at an advantage because trees have lower survival in areas of high conspecific density due to increased attack by natural enemies, a process known as negative density dependence (NDD). A consensus is emerging that NDD is important for plant-species coexistence in tropical forests. Most evidence comes from short-term studies, but testing the prediction that NDD decreases the spatial aggregation of tree populations provides a long-term perspective. While spatial distributions have provided only weak evidence for NDD so far, the opposing effects of environmental heterogeneity might have confounded previous analyses. Here we use a novel statistical technique to control for environmental heterogeneity while testing whether spatial aggregation decreases with tree size in four tropical forests. We provide evidence for NDD in 22% of the 139 tree species analyzed and show that environmental heterogeneity can obscure the spatial signal of NDD. Environmental heterogeneity contributed to aggregation in 84% of species. We conclude that both biotic interactions and environmental heterogeneity play crucial roles in shaping tree dynamics in tropical forests.

Exploring the ecological constraints to multiple ecosystem service delivery and biodiversity

1. Understanding and quantifying constraints to multiple ecosystem service delivery and biodiversity is vital for developing management strategies for current and future human well-being. A particular challenge is to reconcile demand for increased food production with provision of other ecosystem services and biodiversity. 2. Using a spatially extensive data base (covering Great Britain) of co-located biophysical measurements (collected in the Countryside Survey), we explore the relationships between ecosystem service indicators and biodiversity across a temperate ecosystem productivity gradient. 3. Each service indicator has an individual response curve demonstrating that simultaneous analysis of multiple ecosystem services is essential for optimal service management. The shape of the response curve can be used to indicate whether ‘land sharing’ (provision of multiple services from the same land parcel) or ‘land sparing’ (single service prioritization) is the most appropriate option. 4. Soil carbon storage and above-ground net primary production indicators were found to define opposing ends of a primary gradient in service provision. Biodiversity and water quality indicators were highest at intermediate levels of both factors, consistent with a unimodal relationship along a productivity gradient. 5. Positive relationships occurred between multiple components of biodiversity, measured as taxon richness of all plants, bee and butterfly nectar plants, soil invertebrates and freshwater macroinvertebrates, indicating potential for management measures directed at one aspect of biodiversity to deliver wider ecosystem biodiversity. 6. We demonstrate that in temperate, human-dominated landscapes, ecosystem services are highly constrained by a fundamental productivity gradient. There are immediate trade-offs between productivity and soil carbon storage but potential synergies with services with different shaped relationships to production. 7. Synthesis and applications. Using techniques such as response curves to analyse multiple service interactions can inform the development of Spatial Decision Support tools and landscape-scale ecosystem service management options. At intermediate productivity, ‘land-sharing’ would optimize multiple services, however, to deliver significant soil carbon storage ‘land-sparing’ is required, that is, resources focused in low productivity areas with high carbon to maximize investment return. This study emphasizes that targets for services per unit area need to be set within the context of the national gradients reported here to ensure best use of limited resources.

Do early warning indicators consistently predict nonlinear change in long‐term ecological data?

1. Anthropogenic pressures, including climate change, are causing nonlinear changes in ecosystems globally. The development of reliable early warning indicators (EWIs) to predict these changes is vital for the adaptive management of ecosystems and the protection of biodiversity, natural capital and ecosystem services. Increased variance and autocorrelation are potential early warning indicators and can be readily estimated from ecological time series. Here, we undertook a comprehensive test of the consistency between early warning indicators and nonlinear abundance change across species, trophic levels and ecosystem types. 2. We tested whether long-term abundance time series of 55 taxa (126 data sets) across multiple trophic levels in marine and freshwater ecosystems showed (i) significant nonlinear change in abundance ‘turning points’ and (ii) significant increases in variance and autocorrelation (‘early warning indicators’). For each data set, we then quantified the prevalence of three cases: true positives (early warning indicators and associated turning point), false negatives (turning point but no associated early warning indicators) and false positives (early warning indicators but no turning point). 3. True positives were rare, representing only 9% (16 of 170) of cases using variance, and 13% (19 of 152) of cases using autocorrelation. False positives were more prevalent than false negatives (53% vs. 38% for variance; 47% vs. 40% for autocorrelation). False results were found in every decade and across all trophic levels and ecosystems. 4. Time series that contained true positives were uncommon (8% for variance; 6% for autocorrelation), with all but one time series also containing false classifications. Coherence between the types of early warning indicators was generally low with 43% of time series categorized differently based on variance compared to autocorrelation. 5. Synthesis and applications. Conservation management requires effective early warnings of ecosystem change using readily available data, and variance and autocorrelation in abundance data have been suggested as candidates. However, our study shows that they consistently fail to predict nonlinear change. For early warning indicators to be effective tools for preventative management of ecosystem change, we recommend that multivariate approaches of a suite of potential indicators are adopted, incorporating analyses of anthropogenic drivers and process-based understanding.

The stress response of three-spined sticklebacks is modified in proportion to effluent exposure downstream of wastewater treatment works.

This study was conducted to investigate whether exposure to wastewater treatment works (WWTW) effluent affects the adaptive stress axis of fish resident within the receiving water. Three-spined sticklebacks (Gasterosteus aculeatus) were sampled from sites downstream of ten WWTWs in north-west England, selected to represent a range of human population equivalents between 1000 and 125,000. Following capture, indices of stress (whole-body cortisol and glucose concentrations) were measured both prior to, and following, the imposition of a standardised stressor to establish both baseline and stress-induced concentrations of cortisol and glucose. There was considerable between-site variation in size, and to a lesser extent condition, of the fish. Pre- and post-stress cortisol and glucose concentrations also varied significantly between-sites. A large proportion of the variation in both the somatic data and the stress response was explained by variation in the proportion of effluent contributing to total river flow at the study sites. Mass (r(2)=0.35, P<0.001) and length (r(2)=0.37, P<0.001) of the fish, and cortisol (r(2)=0.26, P<0.001) and glucose (r(2)=0.12, P<0.01) concentrations in unstressed sticklebacks, were positively related to the concentration of effluent across the sample sites. However, in stressed fish, cortisol (r(2)=0.32, P<0.001) and glucose (r(2)=0.14, P<0.001) concentrations exhibited a negative trend in relation to the effluent concentrations across sites. Individual variation in fish size did not account for the variation in either cortisol or glucose levels. These data provide the first indication that modulation of the stress axis in fish by anthropogenic factors might be widespread and of greater significance than hitherto assumed.

Relationship between the Concentrations of Dissolved Organic Matter and Polycyclic Aromatic Hydrocarbons in a Typical U.K. Upland Stream

Concentrations of total and freely dissolved polycyclic aromatic hydrocarbons (PAHs) and dissolved organic carbon (DOC) were measured in water collected during four sampling events at five sites from the River Wyre. The sites are typical of streams draining upland organically rich soils in northwest U.K. Freely dissolved PAHs were separated from those associated with DOC using a flocculation method. The sum of concentrations of the total and freely dissolved PAHs analyzed ranged from 2.71 to 18.9 ng/L and 2.61 to 16.8 ng/L, respectively. PAH concentrations and PAH fluxes derived from concentrations and water flow rates generally increased downstream, the trend in the latter being more pronounced. The concentration of individual PAHs containing five or more aromatic rings was found to be strongly correlated to the DOC concentration (p < 0.0001), suggesting common terrestrial sources and hydrological pathways. In contrast, no significant relationships were observed between concentrations of PAHs with four or fewer rings and DOC. Concentrations of PAHs with more than four rings showed similar seasonal variation as DOC concentration (peaking in the late summer), while variation in two or three ring PAHs was out of phase with DOC (peaking in the winter). As the PAH-DOC relationship appeared partly dependent on the molecular weight of the PAHs, a linear regression function that included an interaction between this variable and DOC concentration was used to model PAH concentrations over a 2 year period to estimate annual fluxes. The relationship identified between PAH concentrations and DOC should help to enhance interpretation of PAH monitoring data that are currently sparse both spatially and temporally and, thus, enable more robust assessments of the potential risks of these environmental pollutants to sensitive aquatic organisms and human water supplies.

Mycobacterium avium subspecies paratuberculosis is widely distributed in British soils and waters: implications for animal and human health

In the first comprehensive geographical survey of distribution in Great Britain, Mycobacterium avium ssp. paratuberculosis (MAP) was detected in 115 of 1092 (10.5%) soil cores, in the range of 5 × 10(2) to 3 × 10(6) MAP cell equivalents (CE) g(-1) wet weight soil with the majority of the positive PCR reactions (n = 75; 65%) occurring around the limit of detection (500-5000 CE g(-1) wet weight soil). The distribution of MAP significantly increased from North to South and was significantly correlated with increasing cattle numbers over the same longitudinal axis. Similarly MAP occurrence significantly increased towards easterly latitudes although none of the parameters measured were associated. Comparisons of land use indicated that MAP was widely distributed in both farming and non-farming areas. Soil core samples taken from the rivers Wyre and Douglas catchments (Lancashire, UK) and river Tywi (South Wales) were negative for MAP. However, river monitoring showed a consistent presence of MAPs throughout those catchments over a 6-month period. We concluded that MAP is widely distributed within and outside the confines of the farming environment; its geographical distribution is wider than originally anticipated and; monitoring rivers describes the MAP status of catchment better than individual soil samples.

Field surveys reveal the presence of anti-androgens in an effluent-receiving river using stickleback-specific biomarkers

This study was designed to assess whether the removal of endocrine disrupting chemicals (EDCs) and other substances from a Waste Water Treatment Works (WWTW) effluent (receiving water: R. Ray, Swindon, UK) by granular activated carbon (GAC) affected biomarkers of exposure to EDCs [vitellogenin (VTG) and spiggin] in male and female three-spined sticklebacks in the receiving water. A nearby river (R. Ock), with a negligible effluent loading, was used as a control. On each river fish were sampled from four sites on five occasions both before and after remediation of the WWTW effluent. The results show for the first time in a UK field study a clear seasonality of blood VTG concentrations in wild male fish, following closely the VTG profile in female fish from both rivers. VTG levels in male fish from the R. Ray were significantly reduced after the GAC installation. However, VTG levels in males from the control sites also varied significantly across the same period, reducing the significance of this finding. A laboratory exposure to oestradiol (using site-specific lower and upper levels of oestrogenic activity) failed to elevate VTG concentrations in male sticklebacks suggesting that concentrations in the effluent, even prior to remediation, may not have exceeded a critical sensitivity threshold. Most importantly, a significant increase in female kidney spiggin content (a highly specific biomarker of xeno-androgen exposure) occurred in fish in the R. Ray after the GAC installation to levels comparable with those in fish from the control river. The significance of this finding is strengthened by the fact that during the pre-remediation period in the R. Ray, female spiggin levels increased with increasing distance from the WWTW. Our results provide the first in vivo evidence of the presence of anti-androgens in a UK WWTW effluent. To our knowledge this is the first UK-based comprehensive field study on the effects of a WWTW upgrade on biomarkers of EDC exposure using a sentinel fish species and our findings confirm the value of the stickleback as a model species for studying EDCs both in the laboratory and in the wild.