Integration of ecological monitoring protocols for ...

Integration of ecological monitoring protocols for ponds in the Brussels-Capital Region Streamlining of methodologies for Water Framework Directive, Habitats Directive and Cyanobacterial surveillance

Stijn Van Onsem Ludwig Triest October 2015

Integration of ecological monitoring protocols for ponds in the Brussels-Capital Region Streamlining of methodologies for Water Framework Directive, Habitats Directive and Cyanobacterial surveillance

Van Onsem S. & Prof. Dr. Triest L. Vrije Universiteit Brussel/Leefmilieu Brussel October 2015 Acknowledgements: We would sincerely like to thank all those who helped with monitoring, identification of samples, discussion and correction of texts: Tebkew Shibabaw Achenef, Renaud Bocquet, Natacha Brion, Pierluigi Colangeli, Sofie de Volder, Sandrine Dutrieux, Mathias Engelbeen, Olivier Schmit, Tim Sierens and Adinew Gizeyatu Zengye

SUMMARY ............................................................................................................................................... 5 SAMENVATTING ...................................................................................................................................... 7 RÉSUMÉ ................................................................................................................................................... 9 ABBREVIATIONS..................................................................................................................................... 11 1 INTRODUCTION ............................................................................................................................. 13 1.1 Biomonitoring and the European ecology-based directives ................................................. 13 1.2 Nature in the city ................................................................................................................... 13 1.3 Ecological objectives for ponds in Brussels ........................................................................... 14 1.4 Biomanipulation, bloom control and the functioning of shallow aquatic ecosystems ......... 16 1.4.1 Fish removal and water drawdown............................................................................... 17 1.4.2 Establishment of a clear-water phase ........................................................................... 18 1.4.3 Submerged macrophyte colonization ........................................................................... 19 1.4.4 Bottlenecks of fish removal ........................................................................................... 19 1.4.4.1 Fish – scale of reduction, in-lake recruitment and recolonization ............................ 20 1.4.4.2 Macrophytes – extent of cover and stability............................................................. 20 1.4.4.3 Dynamics of nutrient status and pH .......................................................................... 21 2 VARIABLE SELECTION & ECOLOGICAL GRADIENTS ........................................................................ 23 2.1 Objectives and study area ..................................................................................................... 23 2.2 Variable selection .................................................................................................................. 24 2.3 Pond dynamics in 2013-2014 ................................................................................................ 26 2.3.1 Physical-chemical conditions and nutrients .................................................................. 26 2.3.2 Phytoplankton ............................................................................................................... 26 2.3.2.1 Collection ................................................................................................................... 26 2.3.2.2 Cell density ................................................................................................................ 27 2.3.2.3 Biovolume.................................................................................................................. 27 2.3.2.4 Cyanobacteria............................................................................................................ 27 2.3.2.5 Results ....................................................................................................................... 29 2.3.2.6 Cell density versus biovolume: consequences for toxic bloom surveillance ............ 32 2.3.3 Trophic state of ponds................................................................................................... 33 2.3.4 Periphyton ..................................................................................................................... 34 2.3.5 Macrophytes.................................................................................................................. 37 2.3.5.1 Methodology ............................................................................................................. 37 2.3.5.2 Results ....................................................................................................................... 38 2.3.6 Zooplankton .................................................................................................................. 39 2.3.6.1 Collection and processing.......................................................................................... 39 2.3.6.2 Filtration capacity ...................................................................................................... 40 2.3.6.3 Results ....................................................................................................................... 41 2.4 Correlation between variables from different protocols ...................................................... 45 3 SURVEILLANCE/OPERATIONAL WFD MONITORING & ECOFRAME ............................................... 49 3.1 Integration of ECOFRAME ..................................................................................................... 49 3.2 Proposed adjustments and additional variables ................................................................... 49 3.2.1 Phytoplankton ............................................................................................................... 49 3.2.1.1 Conductivity............................................................................................................... 49 3.2.1.2 Total Phosphorus....................................................................................................... 50 3.2.1.3 Phytoplankton abundance (cell density) ................................................................... 51

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3.2.1.4 Phytoplankton abundance (Chl a + phaeophytin concentration) ............................. 51 3.2.1.5 Results ....................................................................................................................... 51 3.2.2 Macrophytes.................................................................................................................. 52 3.2.2.1 SM seasonal evolution............................................................................................... 54 3.2.2.2 FA+periphyton nuisance............................................................................................ 57 3.2.2.3 SM+FLM species richness .......................................................................................... 58 3.2.2.4 Results ....................................................................................................................... 60 3.2.3 Supplementary variables ............................................................................................... 61 3.2.3.1 Selection of variables ................................................................................................ 61 3.2.3.2 Assessment principle ................................................................................................. 62 3.2.3.3 Results ....................................................................................................................... 63 3.2.4 Phytobenthos (benthic diatoms) ................................................................................... 63 3.3 Overview of WFD status ........................................................................................................ 64 HABITATS DIRECTIVE: ASSESSMENT OF HABITAT TYPES ............................................................... 69 4.1 Defining habitat types in the Brussels-Capital Region .......................................................... 69 4.1.1 H3140 ............................................................................................................................ 69 4.1.2 H3150 ............................................................................................................................ 72 4.1.2.1 Historical presence and potential in Brussels-Capital Region ................................... 73 SPATIAL ASPECTS OF MONITORING: SHORE VERSUS BOAT SAMPLING ....................................... 77 5.1 Sampling and monitoring from shore: a valid approach? ..................................................... 77 5.2 Methods ................................................................................................................................ 77 5.3 Results and discussion ........................................................................................................... 79 5.4 Effect of pond size ................................................................................................................. 85 5.5 Vegetation analysis................................................................................................................ 87 5.6 Does spatial sampling strategy affect WFD quality assessment? ......................................... 87 5.7 Conclusion ............................................................................................................................. 88 FREQUENCY OF MONITORING ...................................................................................................... 91 6.1 Temporal evolution in ponds ................................................................................................ 91 6.2 Specifics of the urban context ............................................................................................... 91 6.3 Cyanobacteria........................................................................................................................ 92 6.4 Seasonal evolution ................................................................................................................ 92 6.4.1 Data treatment .............................................................................................................. 92 6.4.2 Results and discussion ................................................................................................... 93 6.4.2.1 All ponds combined ................................................................................................... 93 6.4.2.2 Focus on vegetated ponds ........................................................................................ 94 6.4.3 Implications for monitoring ........................................................................................... 94 6.5 Evolution of quality classes: validity of single terrain visits .................................................. 99 6.5.1 Results and discussion ................................................................................................... 99 HARMONIZATION OF ASSESSMENT METHODS FOR WFD, HD & CYANOBACTERIAL SURVEILLANCE 101 7.1 Status assessment based on different protocols ................................................................ 101 7.2 Overview of adjustments of the monitoring strategies ...................................................... 102 7.3 Overview of variables for integrated protocol .................................................................... 102 7.4 Time table and validity of monitoring schedule .................................................................. 103 7.5 Management strategy for aquatic vegetations in the Brussels-Capital Region .................. 105

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REFERENCES ................................................................................................................................ 107 APPENDICES................................................................................................................................. 113

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SUMMARY The ecological status of standing waterbodies in the European Union is the subject of various environmental regulations, with the Habitats Directive (HD; 1992) and Water Framework Directive (WFD; 2000) comprising two important legal instruments to safeguard freshwater natural heritage. Monitoring of ponds in the Brussels-Capital Region can be specifically directed towards addressing both directives and their translation into regional legislation, as well as be tuned for surveillance of cyanobacterial blooms. In order to optimize efficiency and completeness of the scientific protocol for pond monitoring, ecological status of a series of ponds has been assessed in 2013 and 2014, followed by selection of relevant biotic and abiotic variables and occasional adjustment of previously employed thresholds. In total, 15 ponds with ecological status ranging from clear, macrophyte-dominated to intermediately or turbid were sampled. Assessment focused on environmental parameters, phytoplankton, periphyton, aquatic vegetation (macrophytes) and zooplankton. Monitoring of macroinvertebrates and fish was considered to be sufficiently validated during previous campaigns, while inclusion and added value of phytobenthos (benthic diatoms) should be tested as part of future studies. Overall, many of the indicators for good or bad quality correlated significantly, although several variables remain highly informative even if partly redundant. In any case, monitoring in terms of HD and WFD objectives and cyanobacterial containment requires the inclusion of a particular set of parameters. Concerning Cyanobacteria, the current protocol seems fit for toxic bloom surveillance and response. For the purpose of WFD monitoring, a number of changes to the original scheme are proposed based on (a) observed relevance, (b) literature sources on (hyper)eutrophic peri-urban ponds, (c) elements of the ECOFRAME methodology for shallow lakes, (d) mandatory features outlined within the WFD, and finally, (e) on certain aspects equally relevant to (and therefore aiding) HD status assessment. Important alterations of the WFD protocol for ponds in the Brussels-Capital Region are: -

change of thresholds for a number of phytoplankton parameters; increased attention to submerged macrophyte composition, richness and fitness; grouping and addition of a number of supplementary variables (including abiotic factors, variables describing cladoceran grazing potential and impact of invasive alien species) to evaluate the supportive state of the habitat.

Based on a ‘one out, all out’ assessment of phytoplankton, macrophytes and supplementary variables, three ponds attained the WFD objective of Good Ecological Potential: Leybeek-b (2013), Rood Klooster 5 (2014) and Woluwe Park 1 (long pond, 2013 and 2014). Compared to previous methodologies, the proposed protocol tends to increase the appreciation of a seasonally stable, clear-water equilibrium dominated by a diverse submerged macrophyte community. The potential and occurrence of two aquatic habitat types described in the Habitats Directive, H3140 (“Hard oligo-mesotrophic waters with benthic vegetation of Chara spp.”) and H3150 (“Natural eutrophic lakes with Magnopotamion- or Hydrocharition-type vegetation”) was evaluated for Brussels ponds. A dominance of characean species in clear ponds probably corresponds to H3140, and indicates the (often delicate) potential of this habitat type within the Brussels-Capital Region. Assessment of the ecological state of H3140 seems less straightforward, as characean vegetation in 5

Brussels mainly consists of tolerant taxa. Of those ponds studied in 2013 and 2014, Parc Roi Baudouin 1 (2013) and Leybeek-b (2013) contained vegetation similar to H3140, but both have since degraded considerably. For assessment of H3150, we used the methodology developed in Flanders. Although the necessary combination of relic floating-leaved macrophytes and multiple accompanying species has been observed on several occasions in the Brussels-Capital Region (e.g. Woluwe Park 1 in 2013/2014), key diagnostic species of the habitat are lacking and H3150 merely reaches a degraded state. Given the current circumstances characterized by (hyper)eutrophic nutrient conditions, unbalanced fish communities and limited dispersal opportunities, the probability of attaining sufficient or good status for H3150 in Brussels appears rather low on short notice. Apart from harmonizing cyanobacterial, WFD and HD monitoring, we investigated spatial and temporal aspects of pond assessment. In 2013, sampling was performed from shore and repeated using a boat, in order to compare the accuracy of both methods. Sampling location affected a number of parameters, and for several variables the absolute difference between shore and boat measurements positively correlated with pond size. To obtain a complete overview of the macrophyte community the sampling effort should focus on the totality of the waterbody, and therefore vegetation analysis by boat would be the preferred method. For small, turbid ponds monitoring from the edge could be a valid approach. In years of monitoring, tendencies of ecological degradation within the growth season – with loss of macrophytes and increased turbidity – necessitate repeated visits in order to accurately evaluate the ecosystem status. It is advised to at least sample in May/June and again in July/August, to avoid under- or overestimating the ecological value of dynamic ponds. Considering longer-term follow-up, WFD and HD monitoring cycles (three and six years, respectively) most likely exceed the expected life span of a particular ecological state in ponds of the Brussels-Capital Region. To be in line with the intrinsic philosophy of HD and WFD, habitat status of ponds should at least be checked once every three years, ideally every year.

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SAMENVATTING De ecologische toestand van stilstaande waterlichamen in de Europese Unie is het onderwerp van verschillende milieureguleringen, waarbij de Habitatrichtlijn (HR; 1992) en de Kaderrichtlijn Water (KRW; 2000) belangrijke wetgevende instrumenten zijn voor het beschermen van natuurlijk erfgoed van zoetwaterecosystemen. Monitoring van vijvers in het Brussels Hoofdstedelijk Gewest kan specifiek toegespitst worden op beide richtlijnen en hun omzetting in regionale wetgeving, en tegelijkertijd afgestemd worden op opvolging van cyanobacteriële bloei. Om de efficiëntie en volledigheid van de wetenschappelijke procedure voor vijvermonitoring te optimaliseren, werd in 2013 en 2014 de ecologische staat van een reeks vijvers beoordeeld, gevolgd door selectie van relevante biotische en abiotische variabelen en eventuele aanpassing van voorheen geïmplementeerde grenswaarden. In totaal werden 15 vijvers bemonsterd, variërend van helder, macrofytgedomineerd tot intermediair of troebel. Het onderzoek focuste op omgevingsparameters, fytoplankton, perifyton, aquatische vegetatie (macrofyten) en zoöplankton. Monitoring van macroinvertebraten en de visgemeenschap werd reeds afdoende gevalideerd tijdens voorgaande campagnes, terwijl het gebruik en de meerwaarde van fytobenthos (benthische diatomeeën) best getest wordt in toekomstig onderzoek. Over het algemeen correleerden veel indicatoren voor goede en slechte kwaliteit significant met elkaar, hoewel verschillende variabelen een hoge informatieve waarde behouden ondanks de gedeeltelijke redundantie. In elk geval moeten bepaalde parameters opgemeten worden in functie van HR- en KRW-doelstellingen en cyanobacteriële controle. De huidige werkwijze voor toezicht en reactie op problemen met Cyanobacteria lijkt geschikt. In het kader van KRW-monitoring worden een aantal aanpassingen voorgesteld gebaseerd op (a) waargenomen relevantie, (b) literatuurbronnen betreffende (hyper)eutrofe peri-urbane vijvers, (c) elementen van de ECOFRAME-methodologie voor ondiepe meren, (d) verplichte componenten vernoemd in de KRW, en tenslotte (e) op bepaalde aspecten die eveneens relevant (en om die reden nuttig) zijn voor de beoordeling van de staat van instandhouding voor de HR. Belangrijke wijzigingen van de KRW-procedure voor vijvers in het Brussels Hoofdstedelijk Gewest zijn: -

aanpassingen van grenswaarden voor een aantal fytoplanktonparameters; verhoogde nadruk op samenstelling, soortenrijkdom en fitness van submerse macrofyten; groepering en toevoeging van een aantal supplementaire variabelen (inclusief abiotische factoren, variabelen gerelateerd aan het begrazingspotentieel van watervlooien en de impact van invasieve exoten) om de ondersteunende toestand van de habitat te evalueren.

Op basis van een ‘one out, all out’-beoordeling van fytoplankton, macrofyten en supplementaire variabelen bereikten drie vijvers de KRW-doelstelling van Goed Ecologisch Potentieel: Leybeek-b (2013), Rood Klooster 5 (2014) en Woluwepark 1 (lange vijver, 2013 en 2014). Vergeleken met vorige methodologieën vergroot de voorgestelde procedure de appreciatie van een doorheen het groeiseizoen stabiel helderwaterequilibrium gedomineerd door een diverse gemeenschap van submerse macrofyten. Het potentieel en voorkomen van twee habitattypes beschreven in de Habitatrichtlijn, H3140 (“Kalkhoudende oligo-mesotrofe wateren met benthische Chara spp. vegetaties”) en H3150 (“Van 7

nature eutrofe meren met vegetatie van het type Magnopotamion of Hydrocharition”) werd geëvalueerd voor Brusselse vijvers. Dominantie van kranswiersoorten in heldere vijvers komt vermoedelijk overeen met H3140, en duidt op het (vaak delicate) potentieel van dit habitattype in het Brussels Hoofdstedelijk Gewest. De beoordeling van de ecologische staat van H3140 is minder duidelijk, aangezien kranswiervegetaties in Brussel voornamelijk bestaan uit tolerante taxa. Van de vijvers bestudeerd in 2013 en 2014 bevatten Koning Boudewijnpark 1 (2013) en Leybeek-b (2013) vegetatie gelijkaardig aan H3140, maar beide vijvers degradeerden sindsdien aanzienlijk. Voor de beoordeling van H3150 werd de Vlaamse methodologie gebruikt. Hoewel de benodigde combinatie van relictsoorten (drijfbladplanten) en verscheidene begeleidende soorten op verschillende momenten werd waargenomen in het Brussels Hoofdstedelijk Gewest (bvb. Woluwepark 1 in 2013/2014), blijven elementaire kensoorten van de habitat afwezig en haalt H3150 slechts een gedegradeerde staat. Omwille van de huidige omstandigheden, gekenmerkt door een (hyper)eutrofe nutriëntenstatus, ongebalanceerde visgemeenschappen en beperkte dispersiemogelijkheden, lijkt het bereiken van een voldoende of goede staat van H3150 in Brussel op korte termijn eerder onwaarschijnlijk. Naast het harmoniseren van cyanobacteriële, KRW- en HR-monitoring werden enkele ruimtelijke en temporele aspecten van vijverbeoordeling onderzocht. In 2013 werd staalname uitgevoerd vanaf de oever en herhaald vanop een boot, met als doel het vergelijken van de accuraatheid van beide methoden. De staalnamelocatie beïnvloedde een aantal parameters, en voor verschillende variabelen trad correlatie op tussen het absolute verschil tussen oever- en bootwaarden en de grootte van de vijver. Om een compleet overzicht te krijgen van de macrofytgemeenschap bleek het noodzakelijk om het volledige waterlichaam te analyseren, en om die reden is vegetatieopname met behulp van een boot wenselijk. Voor kleine, troebele vijvers zou monitoring vanaf de oever moeten volstaan. In jaren waarin monitoring plaatsvindt, is het voor een correcte beoordeling van de status van het ecosysteem noodzakelijk om meermaals terreinbezoeken uit te voeren, omwille van een tendens voor ecologische degradatie – met verlies van macrofyten en verhoogde troebelheid – binnen een enkel groeiseizoen. Er wordt geadviseerd om ten minste in mei/juni en opnieuw in juli/augustus te monitoren, om onder- of overschatting van de ecologische waarde van dynamische vijvers te vermijden. Wat betreft opvolging op langere termijn, is het waarschijnlijk dat monitoringscycli voor KRW en HR (respectievelijk drie en zes jaar) de verwachte levensduur van een bepaalde ecologische staat overschrijden voor vijvers in het Brussels Hoofdstedelijk Gewest. Om in overeenstemming te blijven met de intrinsieke filosofie van HR en KRW zou de habitattoestand van vijvers minstens eens per drie jaar gecontroleerd moeten worden, en ideaal zelfs jaarlijks.

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RÉSUMÉ L’état écologique des eaux stagnantes dans l’Union européenne fait l’objet de diverses réglementations environnementales, dont la Directive Habitats (DH; 1992) et la Directive Cadre sur l’Eau (DCE; 2000) constituent deux instruments légaux avec des conséquences importantes concernant la protection du patrimoine naturel des masses d’eau douces. La surveillance des étangs en Région de Bruxelles-Capitale peut être spécifiquement orientée vers l’application des deux directives et leur transposition en législation régionale, ainsi qu’être optimalisée pour la surveillance des efflorescences de cyanobactéries. Afin d’optimaliser l’efficacité et l’exhaustivité du protocole scientifique pour la surveillance des étangs, l’état écologique d’une série d’étangs a été évalué en 2013 et 2014, suivi de la sélection des variables biotiques et abiotiques les plus pertinentes et de la modification de certains seuils employés précédemment. Au total, 15 étangs dont l’état écologique varie de clair et dominé par des macrophytes à intermédiaire ou trouble ont été échantillonnés. L’évaluation s’est concentrée sur les paramètres environnementaux, le phytoplancton, le périphyton, la végétation aquatique (les macrophytes) et le zooplancton. La surveillance des macroinvertébrés et des poissons a été considérée comme suffisamment validée pendant les campagnes précédentes, tandis que l'utilisation et la valeur ajoutée du phytobenthos (les diatomées benthiques) doivent être testées dans le cadre d’études futures. En général, beaucoup d’indicateurs – de bonne ou mauvaise qualité – étaient significativement corrélés, mais différentes variables restaient très informatives même si partiellement redondantes. En tout cas, le suivi en fonction des objectifs de la DH et DCE et du contrôle des cyanobactéries exige l’inclusion d’une série de paramètres particuliers. Concernant les cyanobactéries, le protocole actuel semble bien adapté à la surveillance de prolifération toxique et aux mesures appropriées. Dans le but du monitoring dans le cadre de la DCE, quelques changements de la méthode originale sont proposés sur base (a) de la pertinence observée, (b) de la littérature scientifique concernant les étangs péri-urbains (hyper)eutrophisés, (c) des éléments de la méthodologie ECOFRAME développée pour les lacs superficiels, (d) des particularités obligatoires stipulées dans la DCE, et finalement, (e) de certains aspects aussi pertinents pour (et donc aidant à) l’évaluation de l’état dans le cadre de la DH. Des changements importants du protocole DCE pour les étangs situés dans la Région de BruxellesCapitale sont : -

l’ajustement des seuils de certains paramètres du phytoplancton; une attention accrue à la composition, à la richesse et à l’état physique des macrophytes submergés; le regroupement et l’addition d’un nombre de variables supplémentaires (y compris des facteurs abiotiques, des variables décrivant le potentiel de filtrage cladocère et l’impact des espèces exotiques envahissantes) pour évaluer l’état soutenant de l’habitat.

Sur base d’une évaluation ‘one out, all out’ du phytoplancton, des macrophytes et de variables supplémentaires, trois étangs atteignaient l’objectif DCE d’un Bon Potentiel Ecologique: Leybeek-b (2013), Rouge-Cloître 5 (2014) et Parc de Woluwe 1 (étang long) (2013 et 2014). Par rapport aux méthodologies précédentes, le protocole proposé tend à augmenter l’appréciation d’un équilibre

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avec de l’eau claire, stable pendant toute la saison et dominé par une communauté diversifiée de macrophytes submergés. Le potentiel et l’occurrence de deux types d’habitats aquatiques décrits dans la Directive Habitats, H3140 (“Eaux oligo-mésotrophes calcaires avec végétation benthique à Chara spp.”) et H3150 (“Lacs eutrophes naturels avec végétation du Magnopotamion ou Hydrocharition”) ont été évalués pour les étangs bruxellois. Une dominance des espèces de Characeae dans les étangs clairs correspond probablement à H3140, et indique le potentiel (souvent délicat) de cet habitat dans la Région de Bruxelles-Capitale. L’évaluation de l’état écologique de H3140 semble moins évidente, puisque dans la Région de Bruxelles-Capitale la végétation des characées est principalement constituée des taxa tolérants. Parmi les étangs analysés en 2013 et 2014, Parc Roi Baudouin 1 (2013) et Leybeek-b (2013) ont présenté une végétation similaire à H3140, mais entre-temps, ils se sont tous les deux considérablement dégradés. Pour l’évaluation de H3150, nous avons utilisé la méthodologie développée en Flandre. Bien que la combinaison nécessaire de macrophytes à feuilles flottantes reliques et de multiples espèces accompagnantes a été observée à plusieurs reprises dans la Région de Bruxelles-Capitale (par exemple, dans Parc de Woluwe 1 en 2013/2014), les espèces diagnostiques essentielles de l’habitat sont absentes et H3150 n’atteint qu’un état dégradé. Étant donné les circonstances actuelles caractérisées par des conditions (hyper)eutrophisées, des communautés de poissons déséquilibrées et des opportunités de dispersion limitées, la probabilité d’atteindre pour H3150 un état suffisant ou bon à Bruxelles semble plutôt faible à court terme. En plus de l’harmonisation de la surveillance cyanobactérienne et celles dans le cadre des DCE et DH, nous avons étudié des aspects spatiaux et temporels de l’évaluation des étangs. En 2013, l’échantillonnage a été effectué depuis la rive et répété en utilisant un bateau, afin de comparer la précision des deux méthodes. La position d’échantillonnage affectait un certain nombre de paramètres, et pour plusieurs variables, il existerait une corrélation positive entre la différence absolue entre les mesures effectuées depuis la rive et à partir d’un bateau et la taille des étangs. Afin d’obtenir une vue d’ensemble complète de la communauté de macrophytes, l’échantillonnage doit se concentrer sur la totalité de la masse d’eau, et donc l’analyse de la végétation par bateau serait préférable. Dans le cas de petits étangs troubles, la surveillance à partir du bord pourrait être une approche valable. Dans les années de surveillance, les tendances à la dégradation écologique au cours de la saison de croissance – avec une perte de macrophytes et une augmentation de la turbidité – nécessitent des visites à plusieurs reprises afin d’évaluer précisément l’état de l’écosystème. Il est donc conseillé d’échantillonner au moins en mai/juin et à nouveau en juillet/août, pour éviter la sous- ou surestimation de la valeur écologique des étangs dynamiques. Considérant le suivi à long terme, les cycles de surveillance dans le cadre des DCE et DH (trois et six ans, respectivement) dépassent très probablement la durée de vie prévue d'un état écologique particulier dans les étangs de la Région Bruxelles-Capitale. Pour être en accord avec la philosophie intrinsèque de la DH et de la DCE, le statut de l'habitat des étangs devrait être vérifié au moins une fois tous les trois ans, idéalement chaque année.

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ABBREVIATIONS B: Boat sample BCR: Brussels-Capital Region DIN: Dissolved Inorganic Nitrogen (nitrate, nitrite, ammonium) ECOFRAME: Ecological monitoring methodology for shallow lakes with respect to Water Framework Directive EM: Emergent macrophytes EQR: Ecological Quality Ratio EU: European Union FA: Filamentous algae FFM: Free-floating macrophytes (unrooted) FLM: Floating-leaved macrophytes (rooted) FR: Flemish Region GEP: Good Ecological Potential H3140: Habitat type 3140 H3150: Habitat type 3150 HD: Habitats Directive IFR (Ind. FR): Individual filtering rate of large Cladocera LCD: Large Cladocera Density LCFR: Large Cladocera Filtering Rate (total filtering rate of large Cladocera community) LCL: Large Cladocera Length MEP: Maximal Ecological Potential OoAo: One out, all out-principle PVI: Plant Volume Infested S: Shore sample SAC: Special Area of Conservation SBZ: Speciale Beschermingszone SM: Submerged macrophytes WFD: Water Framework Directive

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INTRODUCTION

Biomonitoring and the European ecology-based directives

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he influence of anthropogenic activities led to a severe disruption of natural processes in many European countries, and therefore an increased importance of biomonitoring as an ecological assessment tool. A profound understanding of the status of aquatic ecosystems should result in more accurate ways of nature management and creates opportunities to fine-tune policy related to restoration and conservation of freshwater habitats. Environmental monitoring, management and policy exist at different temporal and spatial scales. In Belgium, regulations addressing environmental issues are mainly administered at the regional level (i.e. Flemish, Walloon and Brussels-Capital Regions), but incorporate a large set of European legislative documents. Two of the most ambitious ideological programs launched by the European Union relevant to nature conservation in its member states are the Natura 2000 network of protected areas (EEC 1979; EEC 1992; combining goals stipulated in the Birds and Habitats Directives and converted in legislation of the Brussels-Capital Region through the Ordinance on Nature Conservation 2012) and the implementation of the Water Framework Directive (WFD; EC 2000; Ordinance on Water Policy 2006). Both have had, and continue to have, vast implications on the way biomonitoring and management of surface waterbodies and wetlands are being planned and executed. Notwithstanding the far-reaching environmental improvements accomplished in the trail of legal enforcement of the ecology-based directives, the path towards halting biodiversity loss and restoration of biological integrity in the European Union remains tremendously challenging. Efforts at present seem insufficient in many regards and intended landmarks might unavoidably become delayed (EEA 2012; Kati et al. 2015), while coherence between environmental and agricultural visions at EU-level does not appear obvious (Pe’er et al. 2014). As a result, the original water policy and Natura 2000 objectives could risk being hollowed out during evaluation phases (‘fitness checks’; EC 2015a; EC 2015b), and vigilance is called for to avoid the downgrading of ecological ambitions as a means to comply with legal responsibilities (Moss 2008).

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Nature in the city

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rbanization threatens to suppress biodiversity in many ways, and developing strategies to embed a maximum amount of natural richness within an urban context could help minimizing extinction rates of many freshwater species. In Brussels, the network of ponds and streams and surrounding terrestrial habitats carries a lot of weight when it comes to diversity of diurnal butterflies, amphibians, birds and mammals (Leefmilieu Brussel-BIM 2012). Furthermore, natural environments and green spaces function as important recreational zones. The vicinity of green areas in the Brussels-Capital Region is highly appreciated by inhabitants, while a

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relative scarcity, especially in the city center, is generally negatively perceived (Leefmilieu BrusselBIM 2012). Management plans have been adopted to translate existing nature-related legislation and formulate aquatic and terrestrial nature conservation objectives (Waterbeheerplan/Plan de Gestion de l’Eau and Natuurplan/Plan Nature). By designing a network or patchwork of a mix of pools, ponds and marshlands targeted for high status, with a diverse range of size, depth, connectivity, hydrological regime and sufficiently buffered from negative influences, the Brussels-Capital Region could play a role in supporting European ambitions on aquatic ecosystems.

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Ecological objectives for ponds in Brussels

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hree waterbodies have to be restored and monitored in view of the WFD: the canal CharleroiBrussels-Scheldt, the Senne river and the Woluwe river. On the contrary, none of the ponds present in the region have been designated, although a small number is followed-up together with the three officially registered waterbodies, using an adapted WFD methodology for standing waters (Van Tendeloo et al. 2004; Triest et al. 2008; Van Onsem et al. 2012; Van Onsem et al. 2014). Although theoretically the WFD is intended to be a restoration and preservation tool for all inland surface waters, irrespective of their size, in practice many of the small waterbodies present in the European Union are inadequately embedded in river basin management plans and therefore often poorly represented in the network of sampling stations. The priority for restoration and follow-up of larger rivers and lakes seems understandable given budgetary and logistic limitations. Secondly, the WFD’s apparent emphasis on larger waterbodies might have fed some misconceptions about targeted water systems. Nevertheless, the ecology of ponds in the Brussels-Capital Region has previously been studied to survey the risk of cyanobacterial blooms (Peretyatko et al. 2010; Peretyatko et al. 2012b), to test the efficacy of management actions (especially biomanipulation; De Backer et al. 2012), to model the dynamics of peri-urban ponds (De Backer et al. 2010; Teissier et al. 2012), or as part of WFD water quality assessments (Van Onsem et al. 2012). The acquired knowledge can figure as a starting point to develop and refine evaluation methods for various objectives (Figure 1), which are:  



Toxic cyanobacterial bloom prevention (Figure 2) Surveillance and monitoring of ecological water quality in line with WFD regulations. For this purpose, elements of an adjusted version of ECOFRAME (De Backer 2011, based on Moss et al. 2003) can be integrated in the operational monitoring already applied (Van Onsem et al. 2014). Status assessment of habitats and species to support Natura 2000.

ECOFRAME (Moss et al. 2003) is a scientific scheme developed to assess the status of different types of shallow lakes in the EU, using the obligatory parameters mentioned in the WFD and defining target values for good and high ecological status. It has been conceived as a workable translation of WFD definitions, presented to but without commitment for governmental agencies. De Backer (2011) partly modified ECOFRAME to apply the method to (hyper)eutrophic, peri-urban ponds in the Brussels-Capital Region.

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For Natura 2000, three Special Areas of Conservation (SAC’s) have been designated in Brussels, including networks of forested zones, parks and various ponds and streams. To specify HD objectives for ponds, the availability and potential of habitat types H3140 (Hard oligo-mesotrophic waters with benthic vegetation of Chara spp.) and H3150 (Natural eutrophic lakes with Magnopotamion- or Hydrocharition-type vegetation) can be analyzed using original descriptions provided by the European Commission (EC 2007) and a methodological approach for status assessment developed in Flanders (T’Jollyn et al. 2009).

Figure 1: Biological pond components studied in methodologies used for different objectives. A combination of the monitoring protocols could be conceptualized as a layered structure showing complementarity or redundancy between methods. HD: Habitats Directive; WFD ECOFRAME: monitoring according to ECOFRAME scheme; WFD operational: applied monitoring in the Brussels-Capital Region; Cyano: toxic Cyanobacteria surveillance. Phytobenthos (diatoms) is currently not incorporated as quality element in WFD monitoring of ponds.

The harmonization and streamlining of the different monitoring needs (Figure 1) could maximize the efficiency of field sampling and surveying of aquatic vegetation. A well-integrated procedure for status assessment combined with regular monitoring of ponds will allow to couple specific management actions with observed dynamics and to estimate deviations from the main goals. Objectives concerning WFD, HD and cyanobacterial bloom reduction are largely complementary, since all rely on reduction of nutrients, balanced fish communities and the stabilization of a macrophyte-dominated clear-water equilibrium (Scheffer et al. 1993). However, the three main objectives possibly represent three gradations in terms of difficulty of achievement. Environmental changes necessary for cyanobacterial bloom abatement might be partially (but delicately) successful even without a shift from turbid to clear water, while a Good Ecological Potential (GEP) pivotal for WFD might be achieved sooner than the conditions indispensible for relative stable growth of key macrophyte species characteristic of H3140 and H3150 (Heutz & Paelinckx 2005). A theoretical

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framework for a stepwise increase in ecological quality and concomitant macrophyte communities is provided in Section 7.5.

Figure 2: Two contrasting sights in Brussels ponds: cyanobacterial scum washed ashore in Leyb-b (August 2014) versus vegetated clear water in Silx (August 2014).

A potential conflict between habitat and species conservation could arise when ponds are managed for habitats less suitable as feeding grounds for protected bat species (Chiroptera). A number of bat populations in the Brussels-Capital Region depend on open areas above or in proximity of ponds to hunt for insects (Leefmilieu Brussel-BIM 2012), but a shift in turbidity state could lower the abundance of Chironomidae and other Diptera as potential food source. Nevertheless, the dietary flexibility of for instance Daubenton's bat (Myotis daubentonii), which feeds predominantly on dipteran prey (Flavin et al. 2001; Vesterinen et al. 2013) but perfectly incorporates more sensitive taxa (Trichoptera; Nissen et al. 2013), demonstrates a generalistic behavior possibly unaffected by the ecological status of ponds.

1.4

Biomanipulation, bloom control and the functioning of shallow aquatic ecosystems

I

n Brussels ponds a frequently employed, efficient intervention to restore clear-water conditions and control phytoplankton is the combination of water drawdown and subsequent fish removal, a type of biomanipulation. The addition of pike to control juvenile fish has been attempted as well, but proved to be much less successful (De Backer et al. 2011).

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Biomanipulation, described as the intervention in an ecosystem by manipulating key components of the ecological community, has been proposed as a means to restrain freshwater primary production boosted by eutrophication (Figure 3; Shapiro et al. 1975). In productive, shallow waterbodies the nature of alternative stable states may prevent a systematic improvement of water clarity in spite of efforts reducing eutrophication (Scheffer et al. 1993; Scheffer et al. 2001; Ibelings et al. 2007), and therefore a drastic alteration of the food web might be essential. Removal of benthivorous and zooplanktivorous fish probably is the most popular management tool to manipulate the lacustrine food web. The success rate and stabilization of the intended clear-water state depend on a number of key factors, and their evolution after biomanipulation: the fish assemblage, macrophyte cover and nutrient status. As primary production in aquatic systems is strongly nutrient-diven, biomanipulation often can be thought of as a surrogate for a more thorough remediation of excess internal and external nutrient supply (Søndergaard et al. 2008). When nutrient levels are not dealt with, positive results are generally short-lived, and a return of phytoplanktonic blooms often is inevitable. The different processes involved in biomanipulation of shallow lakes and ponds by fish removal are described hereafter.

1.4.1

Fish removal and water drawdown

Firstly, to tip over the existing balance in a lake or pond affected by blooms, a significant removal of fish has to be achieved. The minimal catch effort needed is difficult to define empirically since data on initial fish densities and their impact are hard to obtain, but lies within the order of either a 75 to 80% reduction within a few years (Meijer et al. 1999; Søndergaard et al. 2000), or a removal of >200 kg/ha over a three-year period (Olin et al. 2006; Søndergaard et al. 2008). A mathematical relation for temperate shallow lakes was described by Jeppesen & Sammalkorpi (2002) as: required annual catch (kg/ha) = 16.9 TP0.52 (Total Phosphorus in µg P/L). In deeper lakes, the necessary catch effort could be lower (Jeppesen & Sammalkorpi 2002). Managers might opt for a drastic water drawdown accompanied by a total removal of the fish stock (van de Bund & van Donk 2002; Van Wichelen et al. 2007; Peretyatko et al. 2009). In flow-through systems, the hydrological situation simplifies technical measures to achieve drainage, followed by either partial or complete fish removal. Timing, duration and level of water drawdown are important management aspects to consider. Because of the oxygenation, mineralization and compaction of exposed sediments, the emptying of a waterbody may act in combination with the downsizing of fish populations to control algal and cyanobacterial blooms after refilling (Cooke et al. 2005; Van Wichelen et al. 2007). In most cases, however, the main action determining management success immediately after water level rise seems to be the food web manipulation itself, through enforcement of biotic key-interactions. A possible, but speculative, additional advantage of water drawdown could be the destruction of cyanobacterial resting stages accumulated on the sediment during years of bloom formation. Since massive emergence under favorable conditions can lead to cyanobacterial blooms (Microcystis: Ståhl-Delbanco et al. 2003) and relationships exist between numbers of settled resting stages and ensuing water column concentrations (Anabaena flos-aquae: Kravchuk et al. 2011), the termination of in situ recruitment could decrease the competitive abilities of Cyanobacteria within the plankton community and prolong the positive effect of biomanipulation. However, survival of a small fraction 17

of settled akinetes or colonies might be enough to generate noxious blooms in summer (Cirés et al. 2013).

Figure 3: Biomanipulation tools to control (cyanobacterial) phytoplankton. Biomanipulation-mediated biotic interactions preventing phytoplanktonic growth are given in black. Undesired side-effects of biomanipulation are shown in gray (see box for explanation). Conventional arrows represent facilitating effects, while ––| interactions indicate negative influences. Dotted arrow: nutrient recycling by fish; YOY fish: young-of-the-year fish.

Apart from interacting in the trophic food chain, fish removal might abate toxic blooms when growth of Cyanobacteria is stimulated by gut passage (Figure 3; Kolmakov & Gladyshev 2003; Prokopkin et al. 2006). Especially the mucilaginous colonies of Microcystis are capable of surviving ingestion by some fish species, and following excretion their growth can be facilitated as a result of nutrient uptake in the alimentary canal (Lewin et al. 2003; Zeng et al. 2014).

1.4.2

Establishment of a clear-water phase

Fish removal can increase transparency in a number of ways, including bottom-up and top-down effects. In shallow lakes and ponds, decreased bioturbation by benthivorous fish reduces concentration of suspended particles and nutrient availability in the water column (Figure 3; Søndergaard et al. 2008). The reduced sediment resuspension by large bream, carp, tench or roach to a great extent can be responsible for creating a window of opportunity for submerged macrophyte colonization in spring, and tends to outlive effects of biomanipulation on Chl a concentrations, i.e. phytoplankton turbidity (Beklioglu & Tan 2008; Søndergaard et al. 2008). However, waterbodies lacking an optimal light regime mainly as a result of high phytoplankton biomass might benefit primarily from an increased grazing pressure of large Cladocera, released from predation by 18

zooplanktivorous fish (Figure 3). Large Cladocera, especially Daphnia spp., are able to create periods of clear water, thus stimulating macrophyte growth. Cladoceran size rather than density sometimes is shown to be a better explanatory variable (Peretyatko et al. 2009), and might be a key factor to avoid cyanobacterial development in macrophyte-poor situations. A common view regarding Daphnia filtration states that it could potentially alter the composition of phytoplankton in favor of large, difficult-to-process filamentous Cyanobacteria or Microcystis colonies, thus actually increasing the risk of toxic bloom formation. Although taxon identity as well as respective densities influence the interaction between daphnids and Cyanobacteria (Asselman et al. 2014; Jiang et al. 2014), large-sized Daphnia are able to reduce even theoretically inedible Cyanobacteria and tolerate high toxin concentrations under certain conditions (Sarnelle 2007; Chislock et al. 2013; Ekvall et al. 2014). Furthermore, isotopic analyses have suggested a generalistic feeding behavior of zooplankton towards available food sources, with consumers incorporating more carbon of prokaryotic origin when Cyanobacteria dominate (Bontes et al. 2006).

1.4.3

Submerged macrophyte colonization

Once a clear-water phase has been established, submerged macrophytes are able to gradually colonize the shallow regions of the waterbody (Figure 3). In shallow lakes and ponds, aquatic vegetation has the potential to occupy the whole surface area, a feature with far-reaching implications for the suppression of planktonic blooms. A suite of macrophyte-mediated interactions enhancing the stability of the clear-water state have been identified, amongst others nutrient competition with phytoplankton, provision of shelter for horizontally migrating zooplankton and allelopathy (Burks et al. 2002; van Donk & van de Bund, 2002). In the end, the complexity of aquatic ecosystems and the scale of biomanipulation often make it unrealistic to pinpoint the exact mechanisms responsible for an observed pattern when large beds of submerged macrophytes have developed. In temperate regions with winter die-off, macrophytes rely on a yearly return of a sufficiently long clear-water phase in spring in order to establish stands large enough to inhibit phytoplankton growth in summer. Unfortunately, in many cases of lake and pond restoration through biomanipulation, the likelihood of an ideal light climate for macrophyte recruitment early in the growing season diminishes year after year, especially because of high nutrient levels or fish replenishment. The longterm stability after biomanipulation thus often becomes compromised by an unfavorable nutrient state or the impossibility to achieve a balanced fish community.

1.4.4

Bottlenecks of fish removal

The shock effect of a sufficiently large reduction of cyprinid fish mostly inhibits phytoplankton abundance on short notice, especially early in the growth season, but tendencies towards increased dominance and reoccurrence of summer blooms appear to be inevitable in many cases (Meijer et al. 1999; van de Bund & van Donk 2002; Beklioglu & Tan 2008; Søndergaard et al. 2008). Because often a principle goal of biomanipulation is to lower the risk of cyanobacterial blooms, a return to turbid

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conditions but without dominance of Cyanobacteria and related health risks could still be considered as a partial success.

1.4.4.1

Fish – scale of reduction, in-lake recruitment and recolonization

A primary cause for biomanipulation failure or lack of prolonged effects is insufficient fish removal, or a quick recovery of zooplanktivorous populations via recruitment or dispersal. Cyanobacterial abundance is not affected when the minimal catch has not been reached (Olin et al. 2006; Søndergaard et al. 2008). A complete removal of fish often results in a trophic cascade powerful enough to allow phytoplankton, including Cyanobacteria, to be controlled, even in the absence of macrophytes (van de Bund & van Donk 2002; Peretyatko et al. 2012a). Efficacy of biomanipulation of ponds in the Brussels-Capital Region has been tested by Peretyatko et al. 2009 and De Backer et al. 2012. Prior to biomanipulation, ponds were overstocked with fish (>500 kg ha-1), contained no aquatic vegetation and frequently endured toxic cyanobacterial blooms. After complete draining, all fish was removed. Large-bodied Cladocera (mainly Daphnia spp.) started to control phytoplankton biomass and turbidity, in most cases enabling extensive growth of submerged macrophytes (Peretyatko et al. 2009). Where submerged vegetation was not restored (either because of a lack of propagules or a high waterfowl herbivory), a clear-water state was maintained by intense grazing by large Cladocera (reaching >3 mm in length). The high filtration rates did not lead to a shift from dominance of edible, eukaryotic phytoplankton towards colonial or filamentous, theoretically grazing-resistant cyanobacteria, suggesting that zooplankton alone could prevent cyanobacterial bloom formation in eutrophic, fishless ponds (Peretyatko et al. 2009; Peretyatko et al. 2012a). In one pond still lacking submerged macrophytes several years after biomanipulation, a bloom of Aphanizomenon occurred as soon as fish reappeared (Peretyatko et al. 2012a). In these peri-urban pond systems, Peretyatko et al. (2012a) found a significant, overall decrease of cyanobacterial biovolume in all encountered scenario’s following biomanipulation (i.e., longer-term success, brief success and failure after brief success). When biomanipulation only briefly restored a clear-water phase, a generally lowered cyanobacterial biovolume was still apparent even after buildup of total phytoplankton biovolume to pre-management conditions (Peretyatko et al. 2012a). However, in these situations cyanobacterial peaks were higher than those observed in successful cases and periods, which indicates that a collapse of the clear-water state increases the risk of blooms of cyanobacteria.

1.4.4.2

Macrophytes – extent of cover and stability

The importance of submerged macrophytes for the stability of a clear-water state has been emphasized by various authors (Scheffer et al. 1993; Søndergaard et al. 2008). Results of fish removal in shallow lakes in the Netherlands showed an increased resilience above 25% surface cover by macrophytes (Meijer et al. 1999), a value similar to the threshold of 30% observed for Danish lakes (Jeppesen et al. 1990) and peri-urban ponds in Belgium (De Backer et al. 2012). In a meta-analysis of Danish shallow lakes, drastic fish removal significantly decreased cyanobacterial biomass until five years (Søndergaard et al. 2008). In many of these lakes, macrophytes quickly colonized large parts.

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Since in biomanipulated peri-urban ponds in Brussels the likelihood of recolonization with small zooplanktivorous cyprinid fish remained high (schools of juvenile fish appeared in 9 out of 12 ponds during the years following biomanipulation), the most essential biotic component stabilizing the clear-water state turned out to be the extent of submerged macrophyte cover. Below 30% surface cover, ponds tended to shift back to turbid conditions in the presence of fish (De Backer et al. 2012). In general, fish recolonization did not significantly increase phytoplankton biovolume if more than 30% of the surface area was covered by submerged macrophytes, although in absence of large Cladocera at TP concentrations exceeding 0.300 mg P/L, submerged macrophytes could maintain a clear-water state only when cover reached at least 82% at some point during the growth season (De Backer et al. 2014).

1.4.4.3

Dynamics of nutrient status and pH

Ultimately, avoidance of blooms and the stability of the clear-water state rely on favorable nutrient dynamics. Positive effects of biomanipulation will be prolonged if nutrient concentrations have been restricted prior to management of the food web. Teissier et al. (2012) found a weakened relationship between TP and Chl a concentrations in the water column of ponds in the Brussels-Capital Region with an extensive submerged macrophyte cover (>30%) and/or efficient zooplankton grazers (mean Large Cladocera Length >1 mm) compared to cyanobacteria-infested ponds before biomanipulation and those having only sparse vegetation (