considering protected aquatic non-target species in the environmental risk assessment of plant protection products

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1 protected species helmholtz centre for environmental research ufz Permoserstraße 15 D Leipzig Germany Department of System-Ecotoxicology and Department of Conservation Biology considering protected aquatic non-target species in the environmental risk assessment of plant protection products matthias liess mira kattwinkel oliver kaske mikhail beketov henning steinicke mathias scholz klaus henle

2 impressum Funded by: Federal Environment Agency (UBA) Section IV 1.3 Plant Protection Products Wörlitzer Platz 1 D Dessau-Roßlau Germany Förderkenzeichen Kurztitel: Schutz der Biodiversität: Berücksichtigung gesetzlich geschützter aquatischer Organismen in Risikobewertung und -management von Pflanzenschutzmittel Das Schutzgut Biodiversität in der Umweltbewertung von Stoffen: Aktueller Kenntnisstand und Anpassungbedarf in der Risikobewertung und im Risikomanagement zum Schutz gesetzlich geschützer aquatischer Organismen vor den Auswirkungen von Pflanzenschutzmittel-Einträgen in Oberflächengewässer 2

3 table of content 1 Summary 4 2 Background 5 3 Legal status of protected species Definition of protected species Federal Nature Conservation Act (BNatSchG) Federal Ordinance on the Conservation of Species (BArtSchV) Council Directive 92/43/EEC Habitats Directive CITES (Convention in International Trade in Endangered Species of Wild Fauna and Flora Washingtoner Artenschutzabkommen ) Council Regulation (EC) No. 338/97 EU Wildlife Trade Regulation Provisions for specially protected fauna and flora species Species of community interest Specially and strictly protected species Exceptions for agriculture Authorisation of plant protection products Conflicts between different bodies of legislation 10 4 Ecology and distribution of protected species Definition of relevant water bodies Protected species relevant for agricultural landscape Red List status of protected species Habitats of protected species Monitoring data on current distribution of protected species Geographical distribution of relevant protected species 18 5 Assessing ecological vulnerability of protected species Toxicological sensitivity Context sensitivity Ecological sensitivity and recovery 27 6 Risk assessment considering protected species Regionally differentiated risk assessment considering protected species Considering protected species and risk management 29 References 31 Annex 36 3

4 summary 1 Summary The EU Uniform Principles for the assessment of plant protection products (PPPs) require that if preliminary risk characterisation indicates potential concerns, registration cannot be granted unless it can be demonstrated that under field conditions no unacceptable impact on the viability of exposed organisms occurs (Annex VI, Directive 91/414/EEC). In addition, the aim of maintaining biodiversity is stated in the new regulation for the placing of PPPs on the market: A plant protection product shall have no unacceptable effects on biodiversity (Regulation (EC) No 1107/2009). Hence, in order to implement the aim of protecting non-target organisms and biodiversity, it is necessary to identify whether the current risk assessment framework protects all relevant species, including protected species. Such species as stated in the Habitats Directive (Council Directive 92/43/ EEC, 1992) are to be protected from being removed from nature, injured, or killed on the level of a single individual wherever they exist. This can only be derogated to the population level if (1) no reasonable alternatives are applicable and (2) the local population is maintained at a favourable conservation status. In contrast, the level of protection in the legislation that concerns the authorisation of PPPs can be interpreted as the population level in general, which indicates a discrepancy between these two bodies of legislation in terms of the legal requirements for protected species. The aim of this investigation is to identify whether the current risk assessment procedure for PPPs is also adequate for the specific demands of aquatic protected species, that is, whether it is sufficiently protective for protected species if performed in the same way as for other species. After reviewing information on the distribution of protected species, we conclude that protected species are present in scattered but widespread distributions in agricultural habitats. Therefore, they need to be considered within the risk assessment framework of PPPs. With regard to their toxicological sensitivity, protected species seem to be comparable to non-protected species. However, available information raises the concern that protected species need careful evaluation concerning effects and recovery compared with non-protected species. This is because their (1) toxicological sensitivity towards PPPs may be increased in the ecological context (context sensitivity) to a higher degree than that of non-protected species and (2) recovery is slower than that for many non-protected species as protected species often have long generation times (ecological sensitivity). (1) Increased context sensitivity: We argue that, in most cases, protected species gain their protection status because they exist under unfavourable environmental conditions due to considerable (human) pressure. Several investigations show that biological constraints (e.g. food deficiency, predatory stress) and environmental stressors (e.g. unfavourable temperature, low oxygen, high UV radiation) increase toxicological (physiological) sensitivity. Therefore, context sensitivity that reflects the ecosystem context may be considerably higher than expected for non-stressed species. (2) Increased ecological sensitivity: Protected species often have a relatively long generation time (e.g. more than one year in invertebrates). This relatively long generation time results in a reduced ability for recovery compared with that of species with a shorter generation time. From these considerations, we derive the following proposal for future risk assessment and risk management of PPPs: 1) The majority of protected species are present in large areas of Germany. Therefore, risk assessment should generally account for the specific vulnerability of protected species, and so should the general risk mitigation obligations associated with the authorisation of PPPs. 2) The recovery of populations should generally not be considered in environmental risk assessment for aquatic environments as many protected species are characterised by a reduced ability to recover from pesticide stress and may also face a higher risk of extinction due to stochastic processes. 4

5 background 3) If the current practice of accounting for population recovery in higher tier risk assessment is maintained, then it should be mandatory to exhaust all options of established risk mitigation measures prior to lowering the protection goal to the population level by considering population recovery in the risk assessment. From a scientific point of view it appears reasonable to already apply this principle to the present environmental risk assessment of PPPs. However, this principle cannot be directly derived from the current PPPrelated EU legislation. Thus, we suggest resolving the existing conflict between the Habitats Directive and Directive 91/414 EEC (recently replaced by the new Regulation 1107/2009) by adding a corresponding text passage to the decisionmaking criteria in Annex VI of Directive 91/414 EEC. 4) Protected species are likely to be characterised by an increased sensitivity to pesticides within the environmental context. Therefore, to extrapolate effects from laboratory standard test systems, we suggest exploring whether another safety factor in addition to the existing ones should be introduced. 2 Background Plant protection products (PPPs) pose a high risk to non-target organisms living in the vicinity of treated areas. Therefore, risk assessment frameworks have been established for appropriate risk management. Within the EU, for example, the respective framework is outlined in Directive 91/414/EEC, which has been replaced by Directive 1107/2009. The EU Uniform Principles for the assessment of plant protection products require that if preliminary risk characterisation indicates potential concerns, registration cannot be granted unless it can be demonstrated that under field conditions no unacceptable impact on the viability of exposed organisms occurs (Annex VI, Directive 91/414/EEC). These Uniform Principles have also been adopted by the new Regulation for the placement of PPPs (Regulation (EC) No 1107/2009, European Parliament and European Council 2009). In addition, Regulation (EC) 1107/2009 states the aim of maintaining biodiversity: A plant protection product shall have no unacceptable effects on biodiversity. Therefore, in order to implement the aim of protecting non-target organisms and biodiversity, it is necessary to identify whether the current risk assessment framework protects all relevant species, including protected species. This exercise seems necessary as a review on the effects of pesticides in the field performed by 75 scientists from academia, industry, and regulatory authorities edited by Liess et al. (2005) showed that, in several field investigations, long-term effects of pesticides were observed (for details see Liess et al. 2005; EPiF/Download.html). Likewise, the use of pesticides has been shown to have negative effects on biodiversity in general (Geiger et al. 2010). Nevertheless, it has often been difficult to assign a specific level of exposure to the observed effects. The risk assessment framework of PPPs is based on investigation of the effects on a few species or communities and subsequent extrapolation of the effects to natural communities within the context of ecosystems. The assessment of the acceptability of the impact of a PPP is based on the extent of this effect, where applicable, together with the anticipated recovery at the population level. Uncertainties within this process of prospective risk assessment are compensated for by safety factors. As listed in the OECD Technical Guidance Document (European Commission, 2003) the four main constituent parts of safety factors that are currently recognised are: Intra- and inter-laboratory variation of toxicity data. Intra- and inter-species variation of toxicity data. Short-term to long-term/chronic toxicity extrapolation. Extrapolation of mono-species laboratory data to field impact on ecosystems. The aim of this investigation is to identify whether the current risk assessment 5

6 legal status of protected species procedure is adequate for protected aquatic species, that is, whether it is sufficiently protective if performed in the same way as for other non-target autochthonous species. The study is restricted to macrophytes, (semi-) aquatic macroinvertebrates, fish, and aquatic stages of amphibians. In particular, we want to identify the following aspects that are relevant to the performance of a risk assessment for protected species: Does the legal status of protected species require a special protection level? Are populations of protected species present in agricultural landscapes such that concern over PPP exposure is justified? Do the distribution patterns of protected species at the landscape level require a locally adapted management concept? Are the sensitivity towards PPPs and the ability for recovery of protected species comparable to those of other non-protected species? 3 Legal status of protected species The Federal Nature Conservation Act (BNatSchG, revised version effective as of (Deutscher Bundestag 2009)) defines which species are protected at which level by the implementation of several international and EU bodies of legislation including the Habitats Directive (Council Directive 92/43/EEC, European Council 1992). It also defines the measurements and provisions to protect such species, their populations, and their habitats. There are three protection levels: (1) species of community interest (Arten von gemeinschaftlichem Interesse), (2) specially protected species (besonders geschützten Arten), and (3) strictly protected species (streng geschützten Arten). The specific protection status of species of community interest applies only to nature conservation areas. Measures have to be taken to protect populations within such areas, which include the potential to constrain agricultural activities. Specially and strictly protected species are to be protected from being removed from nature, injured, or killed at the level of single individuals wherever they occur. In addition, strictly protected species shall not be disturbed during certain periods of their life cycle. However, BNatSchG provides broad exceptions for agriculture, fishery, and forestry that allow for downgrading of protection to the population level or beyond. Some of these exceptions do not seem to comply with European law (i.e. the Habitats Directive, (European Council 1992)). Furthermore, the BNatSchG has already been revised owing to a judgement of the European Court of Justice that rejected to similar, earlier rules that grant exceptions and is still under debate. In Germany, the authorisation of PPPs is regulated by the Federal Plant Protection Act (Pflanzenschutzgesetz, PflSchG), which brings Council Directive 91/414/EEC into national legislation. Directive 91/414/EEC has recently been replaced by Regulation (EC) No 1107/2009. As regards the environmental risk assessment and the authorisation of active substances and PPPs, protected species are not explicitly considered in the above-mentioned EU and national legislation. The level of protection allotted by these pieces of legislation can generally be interpreted as being the population level of non-target species, whereas the protection of individuals of these species is not intended. For the scope of this study, we suggest the following procedure based on the European Habitats Directive: The prohibitions that apply to the level of the individual should only be derogated to the population level if (1) no reasonable alternative to a certain agricultural practice is possible in order to protect single individuals (such as pesticide application only in regions at a certain distance from water bodies) and (2) the local population is maintained at a favourable conservation status as is stated in the Habitats Directive. If the status of the local population is less than favourable, the protection should be carried out on the individual level. 6

7 legal status of protected species 3.1 Definition of protected species Federal Nature Conservation Act (BNatSchG) The main regulatory law that deals with protected species in Germany is the Federal Nature Conservation Act (Bundesnaturschutzgesetz (Deutscher Bundestag 2009)). It sets up the requirements and rules for the conservation of native species and their habitats. It also implements stipulations of species and habitat conservation of European or international legislation by transferring them into national law. In particular, it implements Council Directive (EC) 92/43/EEC (Council Directive on the conservation of natural habitats and of wild fauna and flora, Habitats Directive) as well as Council Regulation (EC) No. 338/97 (on the protection of species of wild fauna and flora by regulating trade therein), which in turn enforces CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora) within the EU. Figure 1 gives an overview of the involved regulations and their annexes, which contain the list of species to be protected. A short introduction to all relevant laws and regulations is given below. In contrast to laws and ordinances, the Red Lists of threatened species have no legal status. They contain lists of species that are endangered in Germany as determined by scientific expertise (BfN 2009). However, they were considered in this study to evaluate the endangerment of species and the consequences for risk assessment (see Chapter 4.3) Federal Ordinance on the Conservation of Species (BArtSchV) In addition to those species listed in BNatSchG, the Federal Ordinance on the Conservation of Species (Bundesartenschutzverordnung, BartSchV, (Bundesministerium für Umwelt 2005)) defines some species that are endangered in Germany as specially or strictly protected according to 52 Abs. 1 & 2 BNatSchG (see Figure 1) Council Directive 92/43/EEC Habitats Directive The Habitats Directive forms a cornerstone of Europe s nature conservation policy. It is built around two pillars: the Natura 2000 network of protected sites and a strict system of species protection. By these means, all Species of community interest Conservation areas (Natura 2000) Population level Specially protected No removal from nature, injure, kill Individual level Strictly protected Additionally no disturbance during certain periods Individual level BNatSchG 7, Abs 2, Nr. 10 7, Abs. 2, Nr. 13 7, Abs. 2, Nr. 14 CR (EC) No 338/97 Annex A & B Annex A CD (EC) 92/43/EEC (Habitats Directive) Some additional species defined in BArtSchV Annex II, IV, V Annex IV 1) Annex IV European birds 1) All Annex IV species relevant in this study are listed as strictly protected according to BNatSchG BNatSchG 52, Abs. 1 BNatSchG 52, Abs. 2 Figure 1: Definition of protected species in BNatSchG and other contributing directives and regulations protection level, and main prohibitions 7

8 legal status of protected species typical European wildlife species and their habitats should be maintained or improved to a favourable conservation status. For the habitats listed in Annex I and the species listed in Annex II of the Habitats Directive, sites of community interest must be designated as special areas of conservation. Additionally, species and habitats are divided in two categories: priority and not priority. In a case of a planned interference, more strictly protective regulations are effective for the priority category (BfN 2009b). However, some species (listed in Annex IV) cannot be protected efficiently by the sole protection of these sites of community interest. Therefore, they are protected directly, regardless of whether they are present inside or outside of protected sites (Bundesministerium für Umwelt 2008). For species listed in Annex V, national regulations can be enacted to ensure sustainable utilisation CITES (Convention in International Trade in Endangered Species of Wild Fauna and Flora Washingtoner Artenschutzabkommen ) CITES is an international agreement between governments to prevent species extinction caused by international trade (NN 1973). International trade is restricted depending on the status of endangerment (Annex I, II, III). Annex I contains species that are in danger to becoming extinct. Annex II contains species whose populations have reached a conservation status where regulated trade under scientific control is acceptable (BfN, 2008a). Lists of endangered species contained within CITES feed into the EU Wildlife Trade Regulation. However, most species listed in CITES are vertebrates and hence not relevant to this study Council Regulation (EC) No. 338/97 EU Wildlife Trade Regulation Council Regulation (EC) No. 338/97 enforces into EU law (European Council 1996). Its aim is to protect wild species, listed in four annexes, by regulating EU internal trade but also the import, export, and re-export of these species. The German BNatSchG defines protected species according to the EU Wildlife Trade Regulation. Annex A contains all CITES Appendix I species, with the exception of those species for which a Member State of the EU has requested an exemption (European Council 1996), as well as some Appendix II and III and non-cites species for which the EU assumes that any trade will endanger the existence of the species (European Council 1996; BfN 2008a). Annex B covers all other CITES Appendix II species (except where an EU Member State has entered a reservation). 3.2 Provisions for specially protected fauna and flora species Species of community interest For species of community interest, special conservation areas that comprise their habitats shall be declared to maintain or restore a favourable conservation status according to 7, Abs. 9 BNatSchG and Habitats Directive Art. 1 i) and shall be called Natura 2000 sites. The conservation status of a species comprises the sum of the influences acting on the species concerned that may affect the long-term distribution and abundance of its populations (European Council 1992). The conservation status is favourable when (1) the population can be assumed to be viable in the long term, (2) the natural range of the species is unlikely to be reduced in the future, and (3) there is and will be a sufficiently large habitat to maintain populations. Within such conservation areas, all modifications and disturbances that can negatively affect the conservation status are prohibited 8

9 legal status of protected species ( 33, BNatSchG). Measures have to be taken to achieve a favourable conservation status. Additionally, species of community interest that are not specially or strictly protected are covered by 39 BNatSchG like all other wild animals and plants. This paragraph describes the same prohibitions as are mentioned for specially protected species (see below), but with the constraint that a disturbance must be wilful or without good cause. As a result, species of community interest are only protected within nature conservation areas and only on the population level. Thus, the disturbance and even killing of a single individual of such species is allowed inside or outside of conservation areas as long as it is not intentional or without good cause Specially and strictly protected species 44 BNatSchG declares the prohibitions in dealing with protected species beyond the general protection of wild fauna and flora given in 39. Within the scope of this study, the relevant provisions are 44, Abs. 1: (1) It is prohibited: 1) to pursue, capture, injure, or kill any wild specimen of specially protected fauna species, or to remove from the wild, damage, or destroy any forms of their life cycle, 2) to considerably disturb (erheblich stören) any wild specimen of strictly protected fauna or European bird species during the breeding, upbringing, molting, migration, or hibernation seasons; a considerable disturbance is given if the conservation status of the local population is degraded by the disturbance, 3) to remove, damage, or destroy breeding or resting sites of a wild specimen of specially protected fauna, 4) to remove any wild specimen of specially protected flora, or morphological forms of development thereof, and to damage or destroy them or their sites. Contrary to the Habitats Directive, these prohibitions are not restricted to deliberate actions. In summary, according to the BNatSchG, to kill or harm a single individual of a protected species or to destroy certain sites that are important in their life cycle are not allowed. Moreover, strictly protected fauna species may not be disturbed during certain life cycle stages. This protection of the single individual is in line with Article 12 Clause 1, Habitats Directive. However, the protection against the disturbance of strictly protected species (BNatSchG, 44, Abs. 1, Nr. 2) is diluted compared with that of the Habitats Directive (Article 12, Abs., 2b). In the latter, not only considerable disturbances are forbidden but also the timing of such prohibited disturbances is not strictly restricted to certain periods. In detail, the Habitats Directive prohibits the disturbance of these species, particularly during the period of breeding, rearing, hibernation, and migration, which is similar to the phrasing of the European Directive on the conservation of birds (Council Directive 79/409/EEC on the conservation of wild birds). In addition to BNatSchG, BArtSchV 4, Abs. 1, Nr. 6 prohibits the luring, catching, or killing of specially protected species using toxicants. Additionally, the Federal States can enact general dispositions or ordinances for the management of protected species ( 44, Abs. 4 BNatSchG) Exceptions for agriculture The Federal State authorities may grant exceptions to the prohibitions listed above in individual cases or in general ordinances to prevent extensive economic loss in agriculture, forestry, fishery, or water management according to 45, Abs. 7, BNatSchG, and 4, Abs. 3 BArtSchV. Such exceptions are only allowed if no reasonable alternatives (zumutbare Alternativen) are possible and if the conservation status of the population will not be degraded. In comparison, Article 16, Habitats Directive, allows derogations from the individual level of protection only in those cases where a favourable conservation status is present and maintained (not only the current one on whatever level that is). Nevertheless, 45, 9

10 legal status of protected species Abs. 7 BNatSchG additionally refers directly to Article 16, Habitats Directive, and restricts the allowed derogations to terms therein. In contrast to the aforementioned restricted exceptions and in contradiction to Habitats Directive, Art. 16, 44, Abs. 4 BNatSchG defines broad general exceptions from the prohibitions mentioned above ( 44, Abs. 1) for agriculture, forestry, and fishery. It declares that the prohibitions of harming or killing are not violated as long as the regulatory requirements of good professional practice 1 are applied ( Einhaltung der guten fachlichen Praxis ) and if the conservation status of the local population is not degraded. Additionally, if other measures like territory protection or wildlife conservation programs can ensure the preservation of the protection status, it is not necessary to consider it in agricultural management. Thus, no reasonable alternatives have to be taken into account, no exception permission is necessary, and the level of protection is in general derogated to the population level. In opposition to this, Art. 16, Habitats Directive, only allows exceptions from the provisions if there is no satisfactory alternative and the derogation is not detrimental to the maintenance of the populations of the species concerned at a favourable conservation status in their natural range. Thus, it is questionable if these exceptions comply with European legislation (Möckel 2008). 3.3 Authorisation of plant protection products In Germany, the authorisation of plant protection products is regulated by the Federal Plant Protection Act (Pflanzenschutzgesetz, PflSchG), which brings Council Directive 91/414/EEC into national legislation. Directive 91/414/EEC has recently been 1) In the case of pesticide application, for example, good professional practice means that the WHG (Wasserhaushaltsgesetz) and PflSchG (Pflanzenschutzgesetz), especially 6 Abs. 2, 15 Abs. 2 PflSchG (e.g. amount of pesticides applied, distance to water bodies etc. as specified by the BVL Bundesamt für Verbraucherschutz und Lebensmittelsicherheit) and PflSchAnwV (Pflanzenschutzanwendungs-Verordnung), have to be considered. replaced by Regulation (EC) No 1107/2009. These two bodies of EU legislation (and accordingly the PflSchG, which refers to Directive 91/414 EEC) do not explicitly mention protected species in connection with the procedures for environmental risk assessment and decision-making, respectively. For the approval of active ingredients it must be shown that PPPs that contain the active ingredient as well as their residues have no unacceptable effects on the environment under particular consideration of non-target organisms, biodiversity, and ecosystems (1107/2009/EC, Art. 4, para. 2b & 3e ii, iii). In addition, the authorisation of PPPs shall follow the requirements of Annex VI to Directive 91/414/EEC (1107/2009/EC, Art. 29, para. 6), which is also applied in the German national authorisation process (Ordinance on Plant Protection Products, Pflanzenschutzmittelverordnung, PflSchMV 1a, Abs. 6, 1). In Annex VI, it is stated that a PPP must not have any long-term repercussions for the abundance and diversity of nontarget species (91/414/EEC, Annex VI, part I C 1, para. 5). Hence, the level of protection allotted by these bodies of legislation can be interpreted as being the population level of non-target species (including protected species) in general, whereas categorical protection of individuals of these species is not intended. The PfSchG, which regulates the authorisation of PPPs as well as the conditions of their use, accounts for protected species only in the provisions for the use of PPPs ( 6, Abs 1). Here, the wording of the BNatSchG (and accordingly, the wording of the Habitats Directive, see Chapter 3.2.2) is in part quoted directly. This places the responsibility for individuals or populations of protected species exclusively on the single applicant of PPPs. 3.4 Conflicts between different bodies of legislation As mentioned in Chapter 3.2.4, BNatSchG allows for broader exceptions from the prohibitions for protected species than the Habitats Directive and it appears questionable whether these deviations from the 10

11 ecology and distribution of protected species European legislation are acceptable (Möckel 2008). In particular, this applies to not considering the actual conservation status of the population of the protected species as well as to the categorical statement that farming in accordance with good professional practice does not violate the prohibitions of harming or killing protected species. Furthermore, a contradiction between the EU PPP-related legislation and the Habitats Directive is clear as the level of protection is set at the level of the population (91/414/ EEC, Annex VI, Decision Making). As regards protected species, this is clearly less strict than the Habitats Directive as the latter only allows for lowering the protection level from individuals to populations under certain circumstances (see Chapter 3.2.3) that include the exceptional case that no reasonable alternatives to protect individuals are applicable. Regarding these alternatives, the Habitats Directive does not provide criteria to evaluate whether a certain alternative is reasonable or not. However, we assume that the established risk mitigation measures for the application of PPPs that include no-spray buffer zones and the use of drift-reducing spraying devices can generally be considered as reasonable as these measures are also established as risk management obligations in the authorisation procedures of PPPs. 4 Ecology and distribution of protected species In this chapter, the ecology and distribution of protected semiaquatic and aquatic species within the taxa evaluated in this study that are relevant for agricultural landscapes are summarised. On the basis of habitat requrements, 166 protected species were identified that are present in agricultural landscapes and thus potentially impacted by agrochemicals (PPPs). Animals comprise 123 species; plants comprise 38 species and seven families. Most of the animals are dragonflies and damselflies (Odonata) followed by amphibians and fish. Linking the lists of protected species to the current Red List data (BfN 2009) has shown that the majority of the protected species (according to their legislative status) are rare and endangered as indicated by their Red List status (according to scientific expertise). Reasons for the endangerment of the protected species include habitat degradation, habitat loss, and toxicants. Further investigations are required for a better understanding of the causes of endangerment (LfULG 2003; LfULG 2004; Schütz 2006; LfULG 2007; Freyhof 2008a; IUCN 2009). An analysis of the distribution of the protected species showed that these species occupy both flowing and standing water bodies, and many of these species are widely distributed all over Germany. To reveal whether the protected species are currently present in the water bodies within German agricultural landscapes, the actual distribution of the protected species was analysed using several monitoring datasets. This analysis showed that (i) the majority of the sites in which the protected species are present are located in agricultural landscapes, and (ii) that a considerable number of protected species are present at those sites. In addition, these sites were scattered evenly over the investigated territories. Furthermore, the available data on pesticide contamination has shown that several protected species were recorded at sites contaminated by pesticides. All these analyses unequivocally show that protected species actually inhabit water bodies within agricultural landscapes and can therefore be affected by PPPs. 4.1 Definition of relevant water bodies The water bodies under consideration were those that are present in agricultural landscapes and potentially impacted by agrochemicals. These habitat types were defined as follows: running water bodies with a maximum width of 3 m and a maximum depth of 0.3 m; standing water bodies with a maximum diameter of 20 m and a maximum depth of 0.3 m. 11

12 ecology and distribution of protected species These thresholds were fixed upon expert agreement to define the water bodies that are (i) actually present in the agricultural landscape (Liess and von der Ohe 2005, Schäfer et al. 2007), and (ii) subject to direct input of pesticides from agricultural land owing to surface runoff and spray drift (e.g. Kreuger 1998; Liess, Schulz et al. 1999; Liess and von der Ohe 2005; Schäfer, Caquet et al. 2007). In larger water bodies, the relevance of pesticide stress is generally lower because of dilution processes. Such larger water bodies are also subject to more complex impacts that include a variety of non-agricultural pressures (e.g. dredging, complex contamination (Tockner et al., 2008)). In the analyses of the available data sets, the selection of habitats, however, was based on the habitat type rather than the habitat size as this variable was rarely reported. However, information on size was indirectly available as a certain habitat type generally implies a certain size. Specifically, we considered species in cases where their habitat was described as (i) rill, streamlet, brook, and ditch for flowing water bodies, and as (ii) puddle, pool, and small pond for standing water bodies. Species that were only present in mountainous regions where agriculture is not performed were excluded. 4.2 Protected species relevant for agricultural landscape For the taxonomic groups considered in the present study (periphyton, macrophytes, aquatic macroinvertebrates, fish, and amphibians), we identified 166 species that matched the habitat parameters described above (for a detailed list of species, see Report Annex, Tables 1 and 2). Animals comprise 123 species; plants comprise only 38 species and seven families. Most of the animals were dragonflies and damselflies (Odonata) followed in prevalence by amphibians and fish. Table 1 shows the number of protected species that in habit in small water bodies, which are specially protected by the Federal Nature Conservation Act (BNatSchG) (Deutscher Bundestag 2009), the Federal Species Conservation Directive (BArtSchV) (Bundesministerium für Umwelt 2005), and the Habitats Directive, Annex IV (European Council 1992). In addition, species mentioned in Annexes II and V of the Habitats Directive (species of community interest) are also listed. For some of the macrophytes, clear classification of their habitat is difficult as they can be found in the transition section between water bodies and wet terrestrial habitats. However, in cases where a species could not be clearly assigned to one habitat it was nonetheless included in the analyses Table 1: Number of protected species per species group that can be found in small flowing and standing water bodies. Taxonomic group Number of protected species (except family level or sp./indet.) Amphibia 21 Pisces & 4 (9) Crustacea 7 (1) Odonata 62 Mollusca 9 (3) Coleoptera 4 Annelida 1 Arachnida 2 Sum 110 (13) Macrophytes 45 * Numbers of species of community interest (Habitats Directive, Annex II & V) are given in parentheses; * among these 45 species, of seven families all species are listed. 4.3 Red List status of protected species While the definition of protected species is legislative (see Chapter 3), the Red Lists include those species that are endangered according to scientific expertise. These Red Lists have no legislative status. We analysed relationships between the list of protected species and the Red Lists to reveal whether the protected species are also endangered and to what degree. The analysis showed 12

13 ecology and distribution of protected species Table 2: Summary of Red List categories of relevant animal species. *: invulnerable, 0: extinct or lost, 1: critically endangered, 2: endangered, 3: vulnerable, D: data insufficient, G: vulnerable, but unknown degree, R: extremely rare, V: near threatened, advance warning list. RL status 2009 * D G R V Amphibia Pisces & RL status Amphibia Pisces & Coleoptera 2 2 Crustacea Odonata Annelida 1 Arachnida 1 1 Mollusca Macrophytes that most of the protected species are also rare and endangered as indicated by their Red List status (for a summary see Table 2; the full table can be found in the Report Annex, Tables 3 and 4). For Amphibia, Pisces, and, the Red Lists were established in 1998 and revised in 2009 (BfN 2009). The specially protected Amphibia were sometimes listed in the Red List as least concern, invulnerable, but the strictly protected ones were often listed as vulnerable (3) to endangered (2) (Table 2). For Pisces and, no clear relationship between protection status and endangerment was found. Only one critically endangered (1) species (Eudontomyzon vladykovi) was specially protected. The other vulnerable to critically endangered ones are listed as protected (Habitats Directive Annex II) or covered by regulations of trading (Habitats Directive Annex V). For the Coleoptera, the Red List endangerment category corresponded to the protection status (critically endangered strictly protected, endangered specially protected). In the group of Crustacea, all species were critically endangered to extinct (1 to 0) and most of them were strictly protected. The strictly protected Odonata were all critically vulnerable to extinct (1 to 0), while many of the specially protected ones were also at least near threatened (V). Additionally, the Red Lists from several Federal States showed that several species were endangered because their populations were decreasing. For the two Arachnida species, the Red List endangerment category corresponded to the protection status as follows: vulnerable specially protected, and critically endangered strictly protected. Likewise, the four strictly protected molluscs were extinct (0), whereas the specially protected ones were at least vulnerable (3). Likewise, the protection status of plants corresponds to their level of endangerment: extinct and critically endangered species (0 to 1) are strictly protected and the other species are specially protected. The endangerment of species is often due to a combination of factors. Anthropogenic disturbances like water regulation, exposure to toxicants and nutrients, siltation, and sedimentation are the main factors that affect the species either directly or indirectly via their habitats (for references see below). A detailed list of the species habitat requirements and major factors that can cause the 13

14 ecology and distribution of protected species Table 3: Habitat preference of specially and strictly protected animal species for small flowing and standing water bodies (species of community interest (FFH, Annex II, V) in brackets) Taxonomic group flowing water body standing water body floating and standing water body Amphibia Pisces & 3 (6) 0 1 (3) Crustacea (1) Odonata Mollusca (3) Coleoptera Annelida Arachnida Sum 22 (6) (7) Macrophytes Table 4: Presence of Amphibia in agricultural land (data from Günther 1996). (scientific) (German) Occurence in agricultural used lands Bombina bombina Rotbauchunke Usually, breeding ponds can be found in submerged cultivated pastures and in depressions in fields (e.g. Sölle). Agricultural landscapes are therefore a main breeding habitat. Bombina variegata Gelbbauchunke Originally distributed in floodplains. Today not typically in ponds of agriculturally used lands, but can be found sporadically in breedings sites within vineyards and fields. Bufo bufo Erdkröte The most common toad in Germany which can be found in almost any kind of habitat, including ponds and terrestrial habitats in agricultural lands. However, preferred breeding sites are water bodies larger than the size limit used in this study. Alytes obstetricans Geburtshelferkröte Has very broad habitat requirements and can be found in a large variety of ponds. Can be found in all kinds of agriculturally used lands. Bufo calamita Kreuzkröte Can be found mainly in temporary ponds on fallow lands and on agricultural lands, incl. wheel tracks. Bufo viridis Wechselkröte Is common on fallow land as well as in agricultural lands, especially vineyards, which are a preferred habitat. Hyla arborea Laubfrosch Can sporadically be found in presswater areas in pasture land and meadows but also frequently also at field margins if structurally rich hedges are present Pelobates fuscus Knoblauchkröte Agricultural used lands of any kind (intensively and extensively) are a main habitat with >60% of all ponds where P. fuscus is found. Rana arvalis Moorfrosch Uses as breeding habitat presswater and rain water fed depressions and small water filled ditches in pastures, meadows, and forests. Usually, it does not occur on intensively used agricultural fields but its grassland habitats may be use intensively. 14

15 ecology and distribution of protected species endangerment of the protected animal species is given in Table 5 of the Report Annex. The fish species are mainly endangered owing to stressors such as water pollution and regulation of water like damming (Table 5) (LfULG 2003; LfULG 2004; LfULG 2007; Freyhof 2008a; IUCN 2009). Sedimentation of fine particles and sludge due to erosion is a critical stressor for the species that inhabit clear rivulets or brooks with running water (e.g. Thymallus thymallus, Cottus gobio, Salmo salar) (LfULG 2003; LfULG 2007). The native crayfish species (Astacus astacus, Austropotamobius torrentium, Austropotamobius pallipes) are considerably impacted by a crayfish plague, which was introduced in 1860 in Germany along with (scientific) (German) Occurence in agricultural used lands Rana dalmatina Springfrosch Mainly occuring in deciduous and mixed forests. Unlikely on intensively used agricultural lands, but can be found in grasslands near forests. Rana kl. esculenta Teichfrosch Very common green frog that can be found in pastures as well as in intensively used agricultural lands in small and large ponds (temporary or permanent) as well as in ditches. Rana lessonae Kleiner Wasserfrosch Summer and hibernation habitats are not limited to ponds; breeding habitats can be found in forests, meadows, swamps, and adjacent to agricultural fields. Rana ridibunda Seefrosch Has very broad habitat requirements. Can be found in ponds and ditches in agricultural used lands (mainly dispersing, juvenile, and subadult individuals), but these areas are not prime habitats. Breeding occurs preferentially in water bodies much larger than the upper size limit used in this study. Rana temporaria Grasfrosch Very common frog species in Germany that can be found in all types of agriculturally used lands. Absent only in very large intensively used areas, e.g. Querfurter Platte. Salamandra salamandra Feuersalamander Unlikely in intensively used agricultural areas, but can be found in gardens, parks, structurally rich vineyards, and forest strips adjacent to agrarian lands. Rarely in ponds adjacent to agricultural lands. Salamandra atra Alpensalamander Unlikely in intensively used agricultural areas, but distributed in cultivated pasture in the Alpine region. Life-bearing species with no aquatic phase Triturus alpestris Bergmolch Uses primarily forested landscapes but can be found also in landscapes dominated by agriculture. Triturus cristatus Kammmolch Wide distribution and can be found in all kinds of agriculturally used lands. Triturus carnifex Alpen-Kammmolch Very isolated distribution in Southeastern Bavaria. Unlikely in ponds within agriculturally used lands. Triturus helveticus Fadenmolch In contrast to the following species, it is primarily a forest dwelling species and only rarely found on intensively used meadows or fields adjacent to meadows. Triturus vulgaris Teichmolch Most common newt in Germany and distributed in all kinds of agricultural lands (intensively used land and extensive grasslands). 15

16 ecology and distribution of protected species crayfishes from North America and seriously affected most of the crayfish populations in Germany (Schütz 2006). Currently existing populations of native crayfishes are threatened by non-native species that are resistant to the crayfish plague. All species in the group of small Crustacea such as fairy shrimps inhabit temporary water bodies. The main reason for their endangerment is habitat loss due to drainage (Table 5, Appendix). The major reason for the endangerment of Odonata is habitat loss and degradation due to regulation of water and contamination with agricultural pesticides and fertilisers (Bellmann 1992). Molluscs such as mussels are mainly endangered owing to their specific life cycle that includes parasitism of the mussels larvae on specific fish species. Therefore, mussels are affected by the contaminants directly (e.g. Margaritifera margaritifera and Unio crassus are highly sensitive to water pollution (Baumgärtner 1994)) and also indirectly through the decline of fish populations. The protected snail species are mainly endangered by water regulation and pollution (BfN 2008b; BfN 2008c; BfN 2008d). Representatives of Coleoptera and Arachnida have no special ecological requirements. It is assumed that they are endangered by general factors such as habitat loss, degradation, and contamination (Kreuels 2000; LANUV 2008; BfN 2008e; BfN 2008f) (Report Annex, Table 5). Amphibians are widely represented in agricultural landscapes; therefore, habitat destruction and contamination with pesticides and fertilisers are the major factors that endanger this group (Günther 1996, Steinicke, 2002, Steffens, 2002, Nyström, 2002, Blab, 2002, Nöllert, 1992, Grosse, 1996). Additional factors that affect amphibian populations are road mortality during migrations to and from breeding sites and a new disease called chytridiomycosis (May 2009; Voyles 2009). While chytridiomycosis has been detected in German amphibians, the extent to which it has contributed to amphibian decline in Germany is still unknown. 4.4 Habitats of protected species The protected species relevant for agricultural landscapes were divided into three large groups according to their habitats: small flowing water bodies, small standing water bodies, and both small flowing and standing water bodies (Table 3). Most of the species (48) are found in both small flowing and standing water bodies. Nearly the same number of species (46) inhabit only small standing water bodies, and 28 species prefer only small flowing water bodies (Table 3). Protected plant species occur in both flowing and standing water bodies. Table 4 describes the occurrence of protected amphibian species in agricultural landscapes. Most of the amphibians occur in ponds or other small water bodies in agricultural areas. For some species, these are even distribution hotspots (e.g. Pelobates fuscus) (Günther 1996). Agricultural landscapes are widely distributed all over Germany, including in low mountain ranges. Thus, it is likely that amphibians are present in these areas. Only five out of 21 species are rarely present in areas of intensive agriculture. However, they are found in pastures, meadows, mountainous regions (Hyla arborea, Rana lessonae, and Salamandra atra), in grasslands near forests (Rana dalmatina), or in gardens, parks, and forest strips adjacent to agricultural areas (Salamandra salamandra) (Günther 1996). In additions, spawning ground of Hyla arborea, Rana lessonaecan be present in the vincinity of intensive arable land use. Salamandra salamandra has also been found in structurally rich vineyards and tree plantations (Rimpp 2007). 4.5 Monitoring data on current distribution of protected species The spatial distribution of protected species indicates how they should be treated within the risk assessment framework. If the occurrence of a protected species is restricted to a small area, local risk assessment measures apply. In cases where they are widespread, 16

17 ecology and distribution of protected species general risk assessment measures should be applied. To reveal whether the protected species are currently restricted to small areas or widespread in water bodies, the actual distribution of the protected species within German agricultural landscapes was analysed using several monitoring datasets. By this method, we can identify whether protected species should be assessed by measures on the national level or if local management is sufficient. Specifically, we used monitoring data of Natura 2000 sites (European Environment Agency 2009) with macrophyte, fish, amphibian, and macroinvertebrate data for the whole of Germany. Furthermore, we received datasets from the Sächsisches Landesamt für Umwelt, Landwirtschaft und Geologie (LfULG) (LfULG 2009) on fish, macrophytes, and macroinvertebrates, and datasets from the European MODELKEY Project (von der Ohe 2009) on macroinvertebrates and fish (for Saxony only). Additionally, macroinvertebrate data from Lower Saxony (NLÖ, now NLWKN, (NLWKN 2009)) were available (for visualisation of data see Fig. 2). The proportion of sampling sites at which protected species were present compared with the total number of sampling sites could not be calculated because we only received information on those sites where protected species were found. The datasets were selected because (i) they were available at the time of project implementation and (ii) they were considered as representative. However, a more comprehensive analysis covering all of Germany requires significant data mining and analytical work and calls for a larger research project. In the Natura 2000 dataset, the category N06, Inland water bodies (Standing water, running water) was used to identify the relevant sampling sites. This dataset does not include measurements of stream sizes, and therefore it may include results from streams larger than those defined in the present study. However, as the relevant species from that dataset were determined as species that inhabit small streams (see Chapter 4.2 Protected species relevant for agricultural landscape), it is plausible that they were present in the habitats of interest in the monitored areas. The other three data sets also contained no information on stream size, but typological classification was available. Therefore, we used the data from the water body types that matched the size parameters defined previously (see 4.1 Definition of relevant water bodies). These are 13 out of 25 types of German stream typology (Pottgiesser 2008). The majority of sample sites where protected species were detected are actually located in agricultural lands (42 % to 82 %, Table 5), as revealed by the intersection of the location of sampling points and a land cover map (Corine Land Cover; European Environment Agency). All arable land use classes as well as vineyards, fruit and berry cultures, and cultures with complex cultivation patterns were counted as arable land (Corine class codes 211, 212, 221, 222, 242, and 243). In addition, as shown in Figure 2, these sample sites were scattered across the study regions. Sampling sites outside of arable land and within arable land generally showed the same number of protected species (Wilcoxon-Rank-Sum Test, p < 0.05, measures as species number); only for the NLÖ data set was an increased number of protected species found at sampling sites outside of arable land. All the analysed datasets included low numbers of protected species, as these species are in general rare and have a low abundance. The majority of the species were from the order Odonata followed by the groups Pisces,, and Mollusca (Table 9). However, some of these species were abundant in the data sets considered (Table 10). To summarise the information from Table 9, 13 % of the protected Amphibia were found in one data set, 53 % of the relevant protected Pisces were found in two datasets, 75 % of protected Coleoptera were found in two datasets, 54.5 % of the Odonata and 58 % of the Mollusca were recorded in all datasets, and 12.5 % of Crustacea were in one dataset. It should be taken into account that the records of the amphibians were only obtained from the Natura 2000 dataset; however, this does not imply that these species only live in these areas, as they were 17

18 ecology and distribution of protected species Table 5: Overall numbers of sample sites that include records of protected species in the analysed monitoring datasets and respective numbers of the sites within arable lands (% of all sites are given in parentheses). Dataset Overall number of samples Number of samples in arable lands (% of all sites) Saxony (MODELKEY) (82%) Lower Saxony (NLÖ 1999, 2000) (77%) Saxony (LfULG) (76%) Germany (Natura 2000) (42%) Table 6: Number of relevant protected species contained in monitoring data of small flowing water bodies (NR indicates that the taxonomic group was not recorded). Taxonomic group Saxony (LfULG) Saxony (MODELKEY) Lower Saxony (NLÖ 1999, 2000) Germany (Natura 2000) Amphibia NR NR NR 3 Pisces & 1 (5) NR NR 2 (3) Crustacea (1) Odonata 17* 21* 39* 4 Mollusca (2) Coleoptera 1 2 Annelida Arachnida Plantae 2 3 Species of community intrest like (Habitats Directive, Annex II & V) are given in parentheses. * Genera included. not considered in the other monitoring programmes (Tables 6 and 7). The LfULG dataset for Saxony also contains information on pesticide measurements. Examples of small streams where the protected fish species and pesticides have been detected at the same sampling site are given in Table 8. All detected substances, except disulfoton, are authorised for use in Germany (Henneberg 2006; LLFG 2009). These are herbicides from the classes chloroacetanilide (metolachlor and metazachlor), triazine (terbutylazin), and urea (isoproturon), and the organophosphorous insecticides disulfoton, dimethoate, and mevinphos (the latter of these is not authorised for use according to Council Directive 91/414/EEC concerning the placement of plant protection products on the market (Bundesamt für Verbraucherschutz und Lebensmittelsicherheit 2010)). These monitoring data clearly show that protected species that require good water quality are present in water bodies contaminated with agricultural pesticides, and can therefore be affected by these contaminants. Whether these individuals were only temporarily present in these water bodies or whether the population is sustainable is a question that cannot be answered in this investigation. 4.6 Geographical distribution of relevant protected species Information on the geographical distribution of protected species is necessary for the planning and implementation of conservation measures. Specifically, it is required to decide whether such measures should be taken at the local level or for the whole of 18

19 ecology and distribution of protected species Figure 2: Sample sites where protected species were recorded as being located within arable land (at least one species recorded per site, only the sites in arable land are shown). 19

20 ecology and distribution of protected species Table 7: Number of sample sites in different monitoring databases where protected species have been detected, with percentage of all sample sites in brackets (NR indicates that the taxonomic group was not recorded). (scientific) Bombina bombina Bombina variegata Triturus cristatus Lampetra planeri Eudontomyzon mariae Ukrainisches Bachneunauge (German) Taxonomic group Saxony (LfULG) Saxony (MODEL-KEY) Lower Saxony (NLÖ 99/ 02) Germany (Natura 2000) Rotbauchunke Amphibia NR NR NR 247 Gelbbauch unke Amphibia NR NR NR 163 Kammmolch Amphibia NR NR NR 596 Bach neunauge Pisces & Pisces & Cottus gobio Groppe Pisces & Rhodeus amarus Misgurnus fossilis Bitterling Schlammpeitzger Pisces & Pisces & Cobitis taenia Steinbeißer Pisces & Dytiscus latissimus Graphoderus bilineatus Hydrophilus piceus Austropotamobius pallipes Calopteryx virgo Calopteryx splendens Oxygastra curtisii Ophiogomphus cecilia (O. serpen tinus) Coenagrion mercuriale Cordulegaster spp. 291 (39,7)* NR NR 307 NR NR (62,2)* NR NR (5,0)* NR NR 28 (3,8)* NR NR (3,1)* NR NR 199 Breitrand Coleoptera 6 Schmal bin diger Breit flügel- Tauchkäfer Pechschwarzer Kolbenwasserkäfer Coleoptera 9 Coleoptera 1 (0.1) Dohlenkrebs Crustacea 1 Blauflügel- Prachtlibelle Gebänderte Prachtlibelle Gekielte Smaragdlibelle Grüne Keiljungfer Helm- Azurjungfer Odonata 50 (23.5) 11 (11.2) 25 (2.8) Odonata 108 (50.7) 43 (43.8) 208 (23.5) Odonata 9 (4.2) 1 (1.0) 10 (1.1) 95 Quelljungfern Odonta 5 (2.3) 2 (2.0)

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