Monday, 16 July 2018

Mapping Portuguese Natura 2000 sites in risk of biodiversity change caused by atmospheric nitrogen pollution

PLoS One. 2018; 13(6): e0198955. Published online 2018 Jun 21. doi: 10.1371/journal.pone.0198955 PMCID: PMC6013174 PMID: 29927996 Pedro Pinho, Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing,1,2,☯* Teresa Dias, Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing,1,☯ Cláudia M. d. S. Cordovil, Funding acquisition, Project administration, Writing – review & editing,3 Ulrike Dragosits, Conceptualization, Funding acquisition, Project administration, Supervision, Writing – review & editing,4 Nancy B. Dise, Writing – review & editing,4 Mark A. Sutton, Conceptualization, Supervision, Validation, Writing – review & editing,4 and Cristina Branquinho, Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Validation, Writing – review & editing1 Julian Aherne, Editor 1 cE3c, Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Portugal 2 CERENA, Centro de Recursos Naturais e Ambiente, Instituto Superior Técnico, Universidade de Lisboa, Portugal 3 LEAF, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, Lisboa, Portugal 4 NERC Centre for Ecology & Hydrology (CEH), Edinburgh Research Station, Bush Estate, Penicuik, Midlothian, United Kingdom Trent University, CANADA Competing Interests: The authors have declared that no competing interests exist. * E-mail: Author information ▼ Article notes ► Copyright and License information ► Disclaimer Go to: Abstract In this paper, we assess and map the risk that atmospheric nitrogen (atN) pollution poses to biodiversity in Natura 2000 sites in mainland Portugal. We first review the ecological impacts of atN pollution on terrestrial ecosystems, focusing on the biodiversity of Natura 2000 sites. These nature protection sites, especially those located within the Mediterranean Basin, are under-characterized regarding the risk posed by atN pollution. We focus on ammonia (NH3) because this N form is mostly associated with agriculture, which co-occurs at or in the immediate vicinity of most areas of conservation interest in Portugal. We produce a risk map integrating NH3 emissions and the susceptibility of Natura 2000 sites to atN pollution, ranking habitat sensitivity to atN pollution using expert knowledge from a panel of Portuguese ecological and habitat experts. Peats, mires, bogs, and similar acidic and oligotrophic habitats within Natura 2000 sites (most located in the northern mountains) were assessed to have the highest relative risk of biodiversity change due to atN pollution, whereas Natura 2000 sites in the Atlantic and Mediterranean climate zone (coastal, tidal, and scrubland habitats) were deemed the least sensitive. Overall, results allowed us to rank all Natura 2000 sites in mainland Portugal in order of evaluated risk posed by atN pollution. The approach is of great relevance for stakeholders in different countries to help prioritize site protection and to define research priorities. This is especially relevant in countries with a lack of expertise to assess the impacts of nitrogen on biodiversity and can represent an important step up from current knowledge in such countries. Go to: Introduction Atmospheric N pollution Nitrogen (N) pollution is a major environmental challenge [1, 2]. Without the use of N-containing fertilizers, the human population would have been approximately half of its current size [1], but 50–75% of the N applied in agriculture is not taken up by crops. This excess is lost to the environment, affecting human health, air, water, soil, climate, and ecosystems’ stability and biodiversity. In Europe alone, this represents an estimated societal cost of 70–320 billion Euros per year [3]. Humankind’s intervention in the N cycle is considered to have already crossed the Earth’s ecological safety boundary, thus threatening our own security [2]. However, the demand for more food and energy due to increasing population and changing consumption patterns hampers the efforts of reducing N emissions [1]. Most of the observed increase in deposited N take two main forms: reduced N (NHy: NH3 and NH4+), primarily from volatilized agricultural emissions, and oxidized N (NOx: nitric acid, particulate nitrate, etc.), primarily from fossil fuel combustion. These different N forms can be deposited by both dry and wet deposition, in proportions that depend on their relative concentrations, precipitation patterns, and environmental drivers of biosphere-atmosphere exchange [4, 5]. Although an approximately 50% decrease in European NOx deposition has been achieved since the 1980s, progress in reducing NHy deposition has been much slower. This is especially true for the Iberian Peninsula, which has become a significant meat-exporting region [6, 7], an activity that releases high levels of reduced nitrogen through excrement and fertilizer used to produce animal feed. The ongoing revision of the EU National Emissions Ceilings Directive [8] proposes a 69% reduction in NOx emissions and 27% reduction in NH3 emissions by 2030 compared with a 2005 baseline. In the case of Portugal, a 71% reduction in NOx emissions is proposed, but only a 16% reduction in NH3 [8]. Thus, NH3 is expected to make a proportionately larger contribution to Portuguese N deposition in the future. In a global perspective, increased food demands and more fertilizer use may further increase agricultural N use [9] and NH3 emissions, while a combination of increased agricultural production and climate warming may lead to a doubling of global NH3 emissions by 2100 [10]. Nitrogen pollution and biodiversity Impacts of atN pollution on ecosystems and their biodiversity Most natural terrestrial ecosystems have evolved under a specific and often low N availability, and thus can be changed by excessive N (i.e. atN pollution), through both direct and indirect mechanisms [11]. High levels of gaseous or aerosol-borne N (usually NH3) can be directly toxic to higher plants [12, 13] and to organisms that adsorb elements directly from the environment, such as algae, lichens, or bryophytes [14, 15]. Existing atN pollution also acts indirectly on organisms through factors such as nutrient enrichment, soil or water acidification, altered nutrient ratios, or by intensifying the impact of other stressors such as pathogens, herbivory or climate change [11]. Under atN pollution, species composition changes over time and diversity often declines, as characteristic species of oligotrophic, mesotrophic or circumneutral habitats (including species of conservation interest) are out-competed by faster-growing, more nitrophytic or acid-resistant plants, many of which are ruderals or invasive [11, 16]. In general, forbs, bryophytes, lichens and oligotrophic shrubs are the main functional types negatively affected by atN pollution, while grasses, adapted to higher nutrient levels, are the main functional type to benefit. The impacts of atN pollution on biodiversity [15, 17–19] and on species’ physiology [20, 21] are a particular problem immediately downwind of sources such as intensive livestock production. Direct foliar damage is usually due to high local concentrations of NH3[11] while broader ecosystem-scale changes in soil and vegetation often result from chronically-elevated local and regional N deposition, including a combination of wet and dry deposition of NHy and NOx compounds [19, 22]. Within the soil, atN pollution can reduce the allocation of carbon from the vegetation to mycorrhizal fungi [23, 24] and other free-living microorganisms (e.g. other fungi, N-fixing bacteria, phosphorus solubilizers) thus impacting soil microbial communities and the ecosystem functions and services they provide (e.g. decomposition, biological N fixation). The atN pollution also impacts soil fauna [25]. N-driven changes in soil fauna and microbial communities influence the physical properties of soil, such as soil aggregation, water infiltration and organic matter turnover [26]. The impacts of atN pollution on a species or ecosystem depend on several factors [27], including the duration of exposure, total amount and form of N, species sensitivity, intrinsic ecosystem properties (e.g. fertility and acid neutralizing capacity) and climate [11]. Overall, atN pollution threatens biodiversity globally [11, 28], but a global analysis identified northern temperate, boreal, arctic, alpine, grassland, savannah and Mediterranean biomes as being particularly sensitive to atN pollution [28]. Biodiversity loss is of special concern in biodiversity hotspots such as Mediterranean type ecosystems [29, 30], which are thought to be experiencing the greatest proportional biodiversity change [28]. Of the five global Mediterranean regions (California, central Chile, Mediterranean Basin, southern Cape region and southwestern and southern Australia), California and the Mediterranean are considered those most threatened by atN pollution [31]. In contrast to Californian ecosystems, however, those in the Mediterranean Basin are still relatively poorly studied regarding the impacts of atN pollution [11, 31, 32]. Impacts of atN pollution on European habitats, including the Natura 2000 network In this work, we focused on Natura 2000 areas because they host a significant portion of Europe’s biodiversity, including most of its sensitive and unique species. atN pollution constitutes a serious challenge for the conservation of such habitats and species under the Habitats Directive (92/43/EEC). The Habitats Directive, a cornerstone of Europe’s nature conservation policy, promotes the maintenance of biodiversity and requires the Member States to take measures to maintain or restore natural habitats at a favourable conservation status. The Directive established the Natura 2000 network with the aim of assuring the long-term survival of Europe’s most valuable and threatened species and habitats. These sites are afforded the highest degree of protection under European legislation: the provisions of the Directive require strict site protection measures, any avoidance of deterioration and a precautionary approach to permitting “plans or projects” which are likely to have a significant effect on a site. However, the Habitats Directive does not directly address air pollution impacts, of which N deposition and ozone are currently the most important, and until now, there has been no common European approach for determining the impacts of air pollution on individual sites or their conservation status [33]. To protect ecosystems from atN pollution, thresholds for N have been set as critical levels (atmospheric concentration) and critical loads (deposition in ecosystems) [34]. Exceedance of critical loads for N deposition is often associated with a reduction in plant species richness in a broad range of ecosystems. Critical loads of 5–10 kg N ha-1 yr-1 have been defined for sensitive ecosystems [24, 35], although there is evidence that individual sensitive species may decline at levels below the critical load [36], and effects may occur over the longer-term at lower loads [11]. Combining global modelled N deposition with the spatial distribution of protected areas under the UN Convention on Biological Diversity showed that 40% of all protected areas (or 11% of all ecosystems, by area) are projected to receive N deposition higher than 10 kg N ha-1 yr-1 by 2030 [37]. The Portuguese case The Natura 2000 network together with the national network of protected areas covers approximately 22% of the mainland Portuguese terrestrial territory. Portuguese nature conservation areas are created and managed by the national authority for nature conservation ICNF ( Emissions of NH3 are distributed unevenly throughout Portugal due to the patchy location of intensive livestock farming and agriculture, which comprise 85% of the total NH3 emissions. Some municipalities have relatively high emission densities due to the presence of point source emissions associated with industrial activities such as intensive pig and poultry rearing (6%). Overall, there has been a downward trend in NH3 emissions since 1990 (-22.7%), mainly due to decreasing numbers of cattle and energy production from renewable sources [38]. Only a few studies deal with the impact of atN pollution on Portuguese ecosystems. In a Mediterranean Basin matorral habitat (, the form and dose of available N are being manipulated in an ongoing field experiment running since 2007. The study site, located south of Lisbon (Natura 2000 site PTCON0010 Arrábida/Espichel), has low ambient N deposition (<4 kg N ha-1 yr-1) and low soil N content (0.1%). N availability is increased in three N-treatments through additions of 40 kg N ha-1 yr-1 as a 1:1 NH4Cl to (NH4)2SO4 mixture, and 40 and 80 kg N ha-1 yr-1 as NH4NO3. The impacts on plant composition and diversity (richness and evenness) [16, 39] and ecosystem characteristics (soil extractable N and organic matter, aboveground biomass and % of bare soil) [16, 40] and functions (decomposition, nitrification, biological N fixation) [41] are assessed. In contrast to most similar studies, plant species richness increased with enhanced N input and was more related to ammonium than to nitrate. Data suggest that enhanced NH4+ availability affects the structure of the matorral, which may promote soil erosion and N leakage, whereas enhanced NOx availability leads to biomass accumulation, which may increase fire risk [16]. Based on this experiment, the first empirical critical load of N for this European habitat was set at between 20–30 kg N ha-1 yr-1 [35]. Sclerophyllous grazed forests (dehesas in Spain and montados in Portugal - have been characterized regarding their NH3 critical levels and N critical loads [19], including for situations in which other pollution sources co-occur with N [22]. This was done using the changes in functional diversity of one of the most sensitive components of the ecosystem, epiphytic lichens [15]. Under atN pollution, the total plant species richness of these ecosystems did not change, but their functional diversity has undergone a complete shift from a community dominated by oligotrophic species to one dominated by nitrophytic ones [42]. This led to the establishment of a critical level for ammonia at 0.6 μgm−3 and a critical load for N at 26 kg ha−1 yr−1 [19], which is within the upper range established for other semi-natural ecosystems [19]. Aim Taking into consideration the risk posed by N to biodiversity [43, 44], and the knowledge gaps identified for Portugal, the main objective of this work was to map the risk that atN pollution poses to changing biodiversity at Natura 2000 sites located in mainland Portugal. Because most areas with a conservation interest in Portugal occur within or in the immediate vicinity of agriculture fields, which emit mostly NHx, we have focused on NH3 emissions and used it as a proxy for overall atN pollution. We used the most recent spatially distributed NH3 emission inventory available for Portugal at the municipality level together with the location of the Natura 2000 sites. Then we ranked the sensitivity of the habitats within the Habitats Directive (92) to atN pollution using expert knowledge and produced a risk map integrating both NH3 emissions and Natura 2000 sites’ susceptibility to atN pollution. The risk map enables prioritisation of conservation strategies within the Natura 2000 network and identification of research gaps in evaluating the impacts of atN pollution on habitat conservation. In the following section, we review the ecological impacts of N deposition within the context of the EU Natura 2000 network and in relation to Portuguese conditions. Afterwards, we describe the assessment and mapping methodologies applied, and then present and discuss the results.