5. Impact of the Quagga Mussel

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Key factors for spread, impact and management of Quagga mussels in the Netherlands

J. Matthews G. van der Velde A. bij de Vaate R.S.E.W. Leuven Key factors for spread, impact and management of Quagga mussels in the Netherlands

J. Matthews G. van der Velde A. bij de Vaate R.S.E.W. Leuven

Final report 24 February 2012

Radboud University Nijmegen, Institute for Water and Wetland Research Department of Environmental Sciences & Department of Animal Ecology and Ecophysiology & Waterfauna Hydrobiologisch Adviesbureau, Lelystad

Commissioned by Invasive Alien Species Team Netherlands Food and Consumer Product Safety Authority Ministry of Economic Affairs, Agriculture and Innovation

Series of Reports on Environmental Science

The series of reports on Environmental Science are edited and published by the Department of Environmental Science, Institute for Water and Wetland Research, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands (tel. secretariat: + 31 (0)24 365 32 81).

Reports Environmental Science nr. 404

Title: Key factors for spread, impact and management of Quagga mussels in the Netherlands

Authors: J. Matthews, G. van der Velde, A. bij de Vaate and R.S.E.W. Leuven

Project manager: Dr. R.S.E.W. Leuven, Department of Environmental Science, Institute for Water and Wetland Research, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ Nijmegen, the Netherlands, e-mail: [email protected]

Project number: 62001209

Client: Netherlands Food and Consumer Product Safety Authority, Invasive Alien Species Team, P.O. Box 9102 HC Wageningen

Reference client: TRCPD/2010/3092

Orders: Secretariat of the Department of Environmental Science, Faculty of Science, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ Nijmegen, the Netherlands, e-mail: [email protected], mentioning Reports Environmental Science nr. 404

Key words: dispersal; dreissenids, ecological effects; invasive species; non-indigenous species

Printed on environmentally friendly paper

2012. Department of Environmental Science, Faculty of Science, Institute for Water and Wetland Research, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands

All rights reserved. No part of this report may be translated or reproduced in any form of print, photoprint, microfilm, or any other means without prior written permission of the publisher. Contents Summary ...... 4 1. Introduction ...... 7 1.1. Background and problem statement ...... 7 1.2. Research goals ...... 8 1.3. Outline of the report and coherence of research ...... 8 2. Materials and methods ...... 10 2.1. Literature survey ...... 10 2.2. Current distribution and relative abundance ...... 10 2.3. Detailed sampling ...... 12 2.4. Analysis of presence and abundance in relation to environmental factors ...... 14 2.5. Influence of temperature and salinity on attachment ...... 14 2.6. Condition analyses in relation to water depth ...... 15 2.7. Bioaccumulation of metals and implications for the food web ...... 15 2.8. Effects of mussel fouling on native unionids ...... 16 2.9. Statistical analysis ...... 18 3. Current distribution ...... 19 3.1. Life cycle and biology ...... 19 3.2. Current distribution of the Quagga mussel ...... 20 3.3. Dispersal rate ...... 24 3.4. The influence of connectivity on distribution ...... 24 3.5. Vectors of colonization ...... 25 3.6. Direction of colonization ...... 28 4. Potential distribution ...... 30 4.1. Physiological tolerance and presence in relation to environmental factors ...... 30 4.2. Effect of temperature and salinity on basal thread development ...... 33 4.3. Influence of substratum on colonization ...... 33 4.4. The effects of shipping on flow velocity ...... 36 4.5. Depth condition relationships ...... 37 4.6. Potential distribution map ...... 38 4.7. Explanations for low mussel densities in the rivers Rhine and IJssel ...... 40 5. Impact of the Quagga mussel ...... 47 5.1. Macro-invertebrate composition in relation to mussel abundance ...... 47 5.2. Implications of metal accumulation in mussels for food chains ...... 48 5.3. Fouling of native unionid mussels ...... 49

5.4. Species replacement ...... 52 5.5. Changes in food webs and energy flow ...... 54 5.6. Effects on fish ...... 57 5.7. Effects on macrophytes ...... 58 5.8. Effects on birds ...... 59 5.9 Parasites of dreissenid species ...... 60 5.10. Predators of dreissenid mussels ...... 61 5.11. Competition by other sessile species ...... 62 5.12. Economic consequences of dreissenid invasions ...... 62 6. Scope of management measures ...... 64 6.1. Preventive and management measures currently applied ...... 64 6.2. Water system approach ...... 64 6.3. Management of colonization vectors ...... 66 6.4. Management strategies for biofouling of infrastructure ...... 70 7. Discussion ...... 76 7.1. Hydrological connectivity and vectors of colonization...... 76 7.2. Direction of colonization ...... 77 7.3. Presence and abundance in relation to environmental factors ...... 77 7.4. Effect of temperature and salinity on byssal thread development ...... 78 7.5. The effects of shipping on flow velocity ...... 78 7.6. Metal accumulation in Quagga mussels and implications for food chains ...... 78 7.7. Fouling of native unionid mussels ...... 79 7.8. Species replacement ...... 80 7.9. Effects on macroinvertebrates ...... 80 8. Conclusions and recommendations ...... 82 8.1. Conclusions ...... 82 8.2. Effective management options ...... 83 8.3. Recommendations for further research ...... 84 Acknowledgements ...... 86 References ...... 87 Appendices ...... 103 Appendix 1. Literature study search terms ...... 103 Appendix 2. Literature study search tools, information and data sources ...... 104 Appendix 3. Sampling locations ...... 106 Appendix 4. Overview of equipment used during field sampling ...... 109 Appendix 5. Sizes of sampled dreissenids in the river Meuse ...... 110

Appendix 6. Mean tissue metal concentrations of dreissenid species ...... 112 Appendix 7. Average current velocity of the Rhine river branches ...... 113 Appendix 8. Macroinvertebrate species composition at detailed sampling sites ...... 114 Appendix 9. Fluid detachment parameter of Quagga mussels ...... 115 Appendix 10. Treatments methods for controlling dreissenid fouling ...... 116 Appendix 11. Example of a protocol for watercraft decontamination...... 118

Summary

The Quagga mussel (Dreissena rostriformis bugensis) is an invasive exotic species that was first identified in the Netherlands in 2006 in the Hollandsch Diep (near Willemstad), a part of former estuary of the rivers Rhine and Meuse. The Quagga mussel is a close relative of the Zebra mussel (Dreissena polymorpha) which invaded the Netherlands two centuries ago.

Quagga mussels have been shown to reach very high densities in other regions outside their natural geographical range (e.g. in North America). High mussel densities can lead to ecological and socioeconomic effects (e.g. changes in food webs and water clarity, effects on indigenous species and biofouling of industrial installations). The Invasive Alien Species Team of the Netherlands Food and Consumer Product Safety Authority (Ministry of Economic Affairs, Agriculture and Innovation) has asked the Radboud University Nijmegen (in cooperation with Waterfauna Hydrobiologisch Adviesbureau) to conduct an investigation to assess the current spread, potential impact and possible options for managing the Quagga mussel in Dutch freshwaters.

A review of previous monitoring records found in the literature and new sampling data collected in 2011 revealed that the Quagga mussel has established itself in the Dutch network of waterways, including many sections of the rivers Rhine and Meuse, their former estuaries Haringvliet, Hollandsch Diep, Volkerak-Zoommeer, the canals connecting these rivers and large inland lakes (Ketelmeer, Markermeer, IJsselmeer, Zwartemeer, southern border lakes and Volkerak-Zoommeer).

Estimations of colonization direction demonstrate that the Quagga mussel has followed routes of colonization from Hollandsch Diep in an easterly and southerly, upstream direction of the rivers Meuse and Rhine, and to the North where it was found in the Princes Margriet Canal in Friesland. Recently, there is also evidence to suggest that dispersal has occurred in a western direction in the rivers Rhine and Meuse originating from recent populations beyond the Dutch border. Speed of spread was estimated to be 54 km yr-1 which corresponds to the estimations of other authors. The Quagga mussel was not found in hydrologically isolated water bodies, such as isolated lakes and tributaries of large rivers where vectors of colonization such as watercraft were absent. In situations where no passive colonization via water current could occur, the most likely colonization vector was the attachment of mussels to the hulls of watercraft (e.g. shipping, yachts, motorboats, barges, canoes) which may contribute to upstream as well as downstream dispersal. Outside of the main commercial shipping routes, pleasure boats would be most likely to be responsible for Quagga mussel spread. Pleasure boats transported overland on trailers that are exposed to air for only a limited period can act as vectors for water-bodies totally isolated by land. Other, colonization vectors may be drift wood are possibly species such as the brown rat, the muskrat and aquatic birds.

Just as for the Zebra mussel, our literature review and results of field surveys revealed a number of negative and positive ecological and socio-economic impacts of the Quagga mussel. The Quagga mussel has demonstrated an ability to alter nutrient

4 cycling within water bodies, removing plankton from the water column and redistributing nutrients to the sediment (increase of pelagic-benthic coupling). Plankton removal and the competitive exclusion of larger species of macro-invertebrates (e.g. aquatic snails) can have a negative impact on fish species. Quagga mussel populations can encourage the proliferation of blue green algae that is toxic to other species including humans. Quagga mussels have been demonstrated to increase the morbidity and mortality of native unionid mussels by colonising their shells resulting in their extirpation in regions of North America. Moreover, Quagga mussels in the Netherlands were found to colonise the shells of native unionids, leading to a negative effect on growth. Studies carried out in the Netherlands suggest that Quagga mussels bioaccumulate Arsenic (As), Lead (Pb) and Selenium (Se) to a greater degree than Zebra mussels. Selenium may have a particularly negative impact on diving ducks that feed on these mussel species, resulting in impacts on staging, winter body condition and health. A review of the literature reveals that Quagga mussels carry a similar range of parasites to the Zebra mussel. The Quagga mussel may, therefore, carry the human enteric parasites Cryptosporidium parvum and Giardia lamblia. However, dreissenid mussels do not concentrate these parasites over and above that of the surrounding water column. The Quagga mussel may be replacing the Zebra mussel at a number of locations in Dutch freshwaters. Dreissenid mussels colonise the intake pipes of water purification plants and the cooling facilities of power stations. This leads to severely impeded water flows and damage to these facilities. The removal of dreissenid mussels following industrial biofouling is costly. In the United States between 1989 and late 2004, approximately $267 million was spent on prevention and mitigation of dreissenid infestation in total. The total cost of remediation in the Netherlands is unknown.

A number of positive effects have also been reported. The Quagga mussel has been associated with the recovery of native aquatic plant species due to its ability to clarify the water column resulting in increased light penetration. This may also facilitate the colonization of exotic submerged macrophytes. The change in the nature of benthic substrate due to the presence of dreissenid shells may encourage smaller macroinvertebrate species that benefit from the shelter spaces created. Waterfowl and fish use Quagga and Zebra mussels and their faeces and pseudofaeces as a food source and may benefit from increased overall mussel density.

Many of the effects of Quagga mussels are dependent on their abundance and density in any one water-body. In rivers and canals in the Netherlands, the current impacts are still limited due to relatively low abundance of Quagga mussels (1 – 2,268 individuals per m2) in comparison with invaded water bodies abroad (with maximum densities up to 40,000 individuals per m2 for North America). However, in the coming decades in the Netherlands a strong increase in Quagga mussel density is also expected on hard substrata. This particularly holds for water bodies with suitable substrata, low desiccation risk, low flow velocity and low wave stress due to wind and shipping.

Water depth, flow velocity and substratum type were found to have an effect on Quagga mussel establishment in this study. Water depth variation, the maintenance of current velocity over 0.2 m s-1 and the use of substrata less likely to facilitate Quagga

5 mussel attachment (e.g. replacement of metallic materials with PVC / plastic) may reduce the chance of Quagga mussel invasion in water systems.

The early detection of Quagga mussels is important to increase the chances of successful eradication. Water bodies should be risk assessed and a response plan should be developed to ensure a rapid response once the presence of Dreissena has been established. Vulnerable water bodies should be monitored for dreissenid presence. Once the presence of Quagga mussels is confirmed, effect monitoring may be introduced to chart the progress of any mitigation measures brought into action.

Due to the nature of the current spread of the Quagga in the Netherlands and the importance of watercraft as vectors for colonization, the decontamination of watercraft prior to their transfer to un-colonised water bodies can be an effective management strategy in case of proper application and full compliance by boaters. Hot water sprays are recommended as the most effective way of removing mussel contamination, safest for persons carrying out the decontamination procedures and most environmentally friendly. Recommendations for water temperature and exposure time vary depending on the location of the mussels on the ships hull. Publicity campaigns can be helpful in increasing public awareness of the risk that invasive species pose, the mechanisms of transfer and colonization and increase public compliance to (voluntary) management options.

The biofouling of infrastructure is usually prevented using heat treatment and chlorination. Chlorination may have negative impacts on other species, is expensive, hazardous to store and mussels close their shells preventing exposure to the toxicant. Heat treatment costs energy and can cause problems resulting from thermal discharges. Other approaches that may be effective are the use of Bio-Bullets, pellets containing potassium chloride that are selectively taken up by dreissenid mussels, anti-fouling coatings, photo-catalysis and bacterial biocontrol agents.

1. Introduction

1.1. Background and problem statement

The non-indigenous Quagga mussel (Dreissena rostriformis bugensis) began its colonization of Dutch inland waterways in 2004 approximately (Molloy et al., 2007). Since that time, the species has spread rapidly and recent monitoring has proved that it can be classified as an invasive species within the Netherlands. At certain locations (Figure 1.1), the density of the Quagga mussel has recently been found to be higher than that of the earlier invader Zebra mussel (Dreissena polymorpha) (Bonhof et al., 2009; De Rooij et al., 2009; Bij de Vaate, 2010a) and in several other biogeographical regions, the Quagga mussel replaces the Zebra mussel once it becomes established (Stoeckmann, 2003; Zhulidov et al., 2010). Effects of dreissenid establishment on local aquatic ecology are extensive and mussel colonization threatens indigenous unionid mussel populations (Ricciardi et al., 1996; Ward & Ricciardi, 2007). The shell of living and dead unionid mussels is often used by dreissenids as substratum. Large numbers of Zebra and Quagga mussels can attach themselves to the shell part rising above the sediment, competing with the siphon of the unionids for food particles and blocking their valve movements (Parker et al., 1998; Schloesser et al., 1996). Eventually, unionid mussels can die from starvation after dreissenid infestation (Baker & Hornbach, 1997). In addition to this, dreissenids cause economic damage effecting industrial water users and boaters (Oreska & Aldridge, 2011). It is therefore important to assess the characteristics and potential consequences of the establishment of the Quagga mussel in the Netherlands.

Figure 1.1: Dense bed of Quagga mussels in lake Kraaijenbergse Plassen along the river Meuse near Katwijk (Date: October 16, 2011; Photo: Peter Klok).

Before the start of this project, there was a lack of knowledge regarding the (potential) spread and speed of colonization of the Quagga mussel due to its relatively short presence in the Netherlands. Additionally, insight into the controllable factors that

influence its density and distribution is lacking. To support decision making with regard to the design of measures to prevent potential ecological and economical effects and possible health implications for the Dutch population, the Invasive Alien Species Team of the Netherlands Food and Consumer Product Safety Authority (Ministry of Economic Affairs, Agriculture and Innovation) has asked the Radboud University (in cooperation with Waterfauna Hydrobiologisch Adviesbureau) to carry out a study on the current spread of Quagga mussels in the Netherlands and on environmental factors that influence their establishment.

1.2. Research goals

The major goals of this study are:

To assess the present distribution of the Quagga mussel within the Netherlands.

To assess the rate of establishment of the Quagga mussel in various water-types in the Netherlands.

To assess the (potential) ecological, economic and social impacts of the Quagga mussel establishment in the Netherlands, taking into account the effects of this species in other geographical areas.

To assess the effect of key environmental factors determining the presence and abundance of the Quagga mussel (e.g. pH, EGV, salinity, dissolved nutrients, turbidity, substrate, connectivity, various colonization vectors).

To review possible management options for control of spread and biofouling of the Quagga mussel.

1.3. Outline of the report and coherence of research

The present chapter describes the problem statement, goals and research questions in order to identify key factors for the establishment and management of Quagga mussels in the Netherlands. Chapter 2 gives the methodological framework of the project and describes the literature review, data acquisition, field surveys and various experimental studies in order to derive these key factors and to gain insight into current distribution (chapter 3) and potential distribution (chapter 4) of the Quagga mussel in the Netherlands. Chapter 4 analyses the ecological, economic and public health effects of Quagga mussels. Impacts identified in this study are supplemented and discussed using the international body of knowledge on the effects of invasive dreissenids and Quagga mussel in particular. Chapter 6 describes the scope of management measures and focuses on preventive measures, water system management and control of biofouling by Quagga mussels. Available results will be discussed in chapter 7 and conclusions and recommendations for management and further research are presented in chapter 8. Several appendices with raw data and background information complete this report. The coherence between various

8 research activities and outcomes of the study are visualised in a flow chart (Figure 1.2).

Key factors for spread and impacts of Quagga mussels?

Problem statement and research outline (1)

Literature review and data acquisition (2)

Field Experimental surveys (2) studies (2)

Dispersal Current distribution Environmental vectors (3) and densities (3) factors (3 & 4)

Potential Distribution (4)

Ecological and societal Management options impacts (5) and strategies (6)

Discussion (7)

Conclusions and recommendations (8)

Figure 1.2: Flow chart visualising the coherence of literature review, field survey and experimental studies on key factors for establishment and management of Quagga mussels in the Netherlands.

2. Materials and methods

2.1. Literature survey

A literature study was carried out to provide an overview of the current knowledge on the spread of the Quagga mussel in the Netherlands. Moreover, literature data were collected on the physiological tolerances, substrate preference, colonization vectors, ecological and socio-economic impacts and potential measures for management of this species. It was largely internet based with use of university libraries. Various academic and non-academic search engines and websites were used in a systematic search. It was expected that a large amount of data concerning mussel spread would be published from Dutch sources. Search engines and terms were therefore chosen to maximise the chances that these would be found. Search terms used to carry out the literature study are given in appendix 1. Search engines with a Dutch bias such as the Dutch central catalogue (PiCarta) were used in the search for grey literature particularly. In this instance, the term grey literature refers to reports and articles not found in scientific journals (e.g. reports written by and for the Dutch water boards). An overview of all web based resources used is given in appendix 2. Grey material was given the same weighting as academic material as it was expected that a large proportion of data would be found published in this format.

2.2. Current distribution and relative abundance

Sampling methods Sampling was mainly undertaken in the littoral regions at the sampling points identified in tables 2.1 to 2.2. On arrival at the sampling point all the major substrata below the water line were identified. These fell into three main groups soft substratum, stone and vegetation. The majority of sampling was undertaken by hand from stones as this was usually the most abundant and the preferred substrate of dreissenid species. Five stones were removed at random from below the waterline from depths of up to 75 cm from a 10 to 20 m stretch. If groyne stones were sampled then the downstream side of the groyne was selected for stone removal. All mussels were removed from the most densely colonised side of each stone and the surface area of that stone was calculated so that mussel densities could be determined. Other substrates were sampled using a dip net (for vegetation and soft substrates) and sieve (for immovable substrates such as ships hulls or canal bank reinforcements) and the width of both were calculated to estimate the surface area that was sampled. In both cases, five sieve or dip net samples were taken from the substrate and the contents examined. Data and information obtained during the sampling of locations was recorded in a sampling form and later entered into an Excel sheet. Information recorded included water-body type, level of hydrological isolation and the presence of colonization vectors at the site. Additionally, a photo record was made of each sampling site. To ensure that the data generated from the sampling plan is comparable with other surveys, the procedures from a Rijkswaterstaat guidance document (Reeze et al., 2010) were followed as much as possible. Mussels were removed and placed in separate labelled containers to be

10 transported back to the laboratory for analysis. A description of sampling sites is given in appendix 3.

Measurements of mussels Mussels were either analysed immediately or stored in 70% alcohol or frozen until analysis was possible. Mussels were first identified and separated into two species groups. Individuals were counted and measured lengthwise. Sampling locations where the presence of Quagga mussels had not previously been established were added to an overall map indicating all sites where Quagga mussels have been sampled in the Netherlands. Length-frequency graphs were created to allow comparisons of population structure between species and sampling sites. Surface area sampled was used to calculate the density of mussels found at each sampling site. Estimations of age were made using age-length relationships described by Bij de Vaate (2008). Results for population structure were displayed graphically using bar graphs.

Analyses of dispersal pattern Determining the age of individuals gave an estimate of the time of arrival of the sampled population at the sampling location. The age of mussels was estimated using length- frequency distributions of local populations (Bij de Vaate, 2008). This information was then used to determine the direction of colonization. Smaller individuals of mussels were assumed to have originated from older populations of the same species sampled at adjacent sampling locations within the same water body. Due to the low abundance and small size of mussels found, an analysis of direction of colonization was limited to the river Meuse where abundances were higher relative to the rivers Waal and IJssel. The sampling points under consideration are located at Afferden, Milsbeek, Middelaar and Grave (Figure 2.1).

Figure 2.1: Sampling locations used to determine direction of spread in the river Meuse.

Dispersal rates The approximate rate at which the Quagga mussel has dispersed throughout continuous waterways in the Netherlands has been calculated. The distance between the location of the first recorded sighting of the Quagga mussel (Hollandsch Diep near Willemstad) and the farthest known locations of the Quagga mussel from this point was

measured. The shortest possible connected route was measured without taking the direction of water flow into account. This distance was then divided by the difference in the approximate arrival time of the sampled mussels between the two sampling points. The resulting rate was then converted into a dispersal rate (in km y-1).

Analyses of species replacement An assessment of whether the Quagga was replacing the Zebra mussel at individual sampling locations was carried out. Locations were identified where previous sampling had been undertaken and where the presence of Quagga and Zebra mussels had been established. A comparison of relative abundance of Quagga and Zebra mussels within sampled populations in association with calculations of overall mussel density at these sampling sites was performed. Species replacement could only be established at locations where the overall density of mussels could be established for samples. An increase in overall density reflects a population that has not yet reached the carrying capacity of its habitat. Intra-specific competition will therefore play a less important role in determining the relative abundance of different mussel species. Species replacement was said to be occurring if there was an increase of the abundance of the Quagga mussel with respect to the Zebra mussel in combination with an overall mussel density that remained stable or decreased. The results of the analysis for different sampling points were entered into a table to create a summary of the present Dutch situation.

Effects of hydrological isolation on spread Sampling sites were categorised according to their level of hydrological isolation and the presence of watercraft. Sites were defined as hydrologically isolated if the lay upstream from known populations of dreissenid mussels or if a physical barrier such as dry land lay between the sample site and other hydrologically continuous water bodies. Sites were also characterised in terms of level of isolation, defined as water- bodies with a permanent or seasonal connection and permanently disconnected water bodies. Watercraft were defined as all commercial and non-commercial shipping, sailing and motor boats and other vessels such as canoes and rowing boats. The different categories were then compared to each other for the presence and absence of mussels and the average relative abundance for all locations.

2.3. Detailed sampling

Mussel sampling was undertaken in a similar way to the general study of relative abundance. Information on sampling sites is presented in appendix 3 and 8. For the purposes of this part of the study the whole surface area of a stone was sampled.

Macroinvertebrate composition To analyse the effect that mussel density has on macro-invertebrate species composition and abundance, all macroinvertebrates were removed from the stones. Stones were placed in large plastic trays and subsequently brushed. The stones were then removed from the tray and macroinvertebrates were collected using tweezers and placed in alcohol for transport back to the laboratory. Following identification, calculations of species diversity were made. These results were compared to the

12 densities of Quagga and Zebra mussels for each individual stone using regression analysis. The presence of the Quagga mussel is a pre-requisite of the analysis of effects on the macro-invertebrate community therefore sampling sites were chosen where it was most likely that Quagga would be found. Additional data was collected for turbidity, conductivity, temperature, pH, flow velocity and habitat heterogeneity. The equipment used to obtain data together with relevant information on their use is defined in appendix 4.

Flow velocity Data on flow velocity was collected from ten river and side channel locations. Measurements were taken near river banks where dreissenids most likely colonise. Baseline measurements were taken to establish flow velocity characteristics in the absence of watercraft. A second set of measurements was taken when a ship passed. Details of the type (commercial or pleasure boat) and characteristics of the watercraft (loaded/unloaded, direction of travel) were recorded. The data was subsequently analysed to gain an insight into the potential disturbance that watercraft bow wash create for macroinvertebrate communities living along the river banks.

Temperature gradient Additional sampling points have been proposed for the analysis of the effect of temperature gradient on the Quagga mussel. Sampling was undertaken downstream of the Electrobel power station in Nijmegen, a known source of heat pollution. Five artificial substrate samplers were built using house brick placed in perforated plastic boxes. A min – max thermometer was placed in each and attached in an upright position with a rope. The samplers were placed in the water at the sampling locations on July 21, 2011. A rope was attached to the boxes which were subsequently lowered into the water at intervals downstream of the heat source. Four out of five samplers were placed within the boundaries of Rijkswaterstaat land closed to the public to avoid tampering. The last, located farthest away from the heat source, was located on the west side of the mouth of the Meuse-Waal canal. Initial temperature recordings were taken to establish the initial temperature gradient in the river for the five locations. Additional measurements were taken for turbidity and electrical conductivity at each location. Riprap was sampled to determine if mussels were already present on the substrate at each location. Five stones were taken randomly from a maximum depth of 75 cm below the waterline and examined for mussel presence. Mussels found were placed in plastic containers, one for each location, and transported back to the laboratory for determination and demographic analysis. The artificial substrates were left for seven weeks to allow mussels to colonise and removed for examination on September 7, 2011. Any mussels present were collected and taken to the laboratory for identification and measurement of shell sizes. The maximum and minimum water temperatures, measured over the total period that the artificial substrates were in-situ, were recorded for each site. Ambient air temperatures were also measured. The densities of the mussels found at each site were then related to the temperatures measured there. These relationships were then plotted in a scatter plot to determine the effect that water temperature had on the two species under consideration.

2.4. Analysis of presence and abundance in relation to environmental factors

To ascertain if the potential spread of either the Quagga or Zebra mussel is limited due to the physiological requirements of mussels, a comparison was made between the physicochemical conditions at six locations in the Netherlands. The locations were chosen to represent the major water-types present in the Netherlands. A description of the locations is given in table 2.1.

Table 2.1: Locations chosen for the analysis of environmental factors.

Water body, location Amersfoort coordinates Water type

River Waal, Ewijkse plaat 179.3 432.8 Major river

Pannerdensch canal 199.0 433.5 Canal

River IJssel, Ganzendiep 192.2 511.2 Major river

Brielse Meer, Zwartewaal 074.6 433.5 Lake

River Meuse, Linne 193.5 351.5 Major river

Hollandsch Diep 093.0 412.0 Former river estuary

Data on water chemistry was obtained for a number of physicochemical variables from the website waterbase.nl. The type of data considered depended on the results of the literature search of physicochemical limits of dreissenid mussel species. The physicochemical variables that will be considered are pH, salinity, temperature, suspended sediment, chlorophyll a content, and Lead, Cadmium and Zinc concentration.

Data sets obtained were analysed to identify the maximum and minimum values of different variables. If this analysis revealed conditions that could limit dreissenid species due to their physiological tolerances, further analysis was undertaken to establish how long the adverse conditions persisted and if there was a pattern to the conditions that could prove advantageous or deleterious effects to the different mussel species. Various life cycle stages or behaviour may differ in sensitivity to certain variables, for example reproduction and growth. Therefore, attention was paid to the consequences of these variations. A tick indicates that no physiological limitation could be established, a cross indicates a location where a physiological limitation was established. Arrows indicate the level of traffic observed on the water body.

2.5. Influence of temperature and salinity on attachment

A number of experiments were carried out in order to assess how temperature, salinity and light affect the attachment of Quagga and Zebra mussels to hard substratum. Byssal thread production was tested at water temperatures within the temperature range experienced in temperate areas (Therriault & Orlova, 2010), viz. 5, 10, 15, 20 and 25 °C. To test byssogenesis at various salinities, water of the desired salinity was

created by adding sea salt (Tropic Marin, Wartenberg, Germany) to freshwater. Salinities of 0.2, 1, 2, 4, 6, 9, and 12 ppt were applied to examine re-attachment of the dreissenid species within a 24 hour period. This represents an extensive part of the gradient from fresh to brackish water. To assess the possible of a combined effect of salinity and temperature on byssogenesis, combinations of water temperature (5, 15 and 25 °C) and salinity (0.2, 2 and 9) were applied in experiments. For analysis, depending on the data, one-way ANOVA or Welch data analysis was performed (statistical significant difference assumed at p < 0.05). A Scheirer-Ray-Hare (SRH) test was carried out for the salinity x temperature experiment.

2.6. Condition analyses in relation to water depth

In order to assess the effects of depth on survival, condition and stable isotope tissue signatures of the Quagga and Zebra mussel, a transplantation experiment with cages was performed in a freshwater lake Groene Heuvels near Bergharen, The Netherlands (51o 50’ 43’’ N, 5o 41’ 33’’ E). The lake Groene Heuvels is a former sand excavation pit with little organic matter at its bottom. The water has a visibility of about 5 m. The lake with an area of 350,000 m3 reaches a depth of 24 m and had already been invaded by Zebra mussels, which could mainly be found at depths of up to 9 m. The main objective of this research was to assess if Quagga and Zebra mussels respond differently to depth in a deep freshwater lake. The mussels were monitored in a field transplantation experiment for four months. The survival and condition of these species was expected to show differences along a depth gradient and both may depend on the availability and quality of food sources along the depth gradient and in time. Stable isotope analysis was performed to assess possible diet shifts after transplantation to a particular depth.

2.7. Bioaccumulation of metals and implications for the food web

Samples of mussels populations found in the river Waal at Ewijkse Plaat were used in an analysis of tissue metal concentration to establish possible differences in bioaccumulation between the Quagga and Zebra mussel. Mussel samples were taken by hand at extreme low water from the stones covering groynes at the sample site and transported in river water back to the laboratory. Mussel flesh was extracted from their shells the same day, and the tissue was separated into homogenous size samples and subsequently dried at 70 oC for 24 h. The dried samples were then weighed accurately to produce replicate samples of 0.2 g dry weight and then prepared for ICP-MS analysis using microwave destruction. Nitric acid and hydrogen peroxide were added to samples and the samples were then destroyed in the microwave in stages using different power levels for different durations. The samples then underwent ICP-MS analysis to establish the metal concentrations contained within mussel tissue. Mussel tissue was analysed for concentrations of Aluminium (27Al), Chromium (52Cr), Manganese (55Mn), Iron (56Fe), Cobalt (59Co), Nickel (60Ni), Copper (63Cu), Zinc (66Zn), Arsenic (75As), Selenium (82Se), Molybdenum (95Mo), Cadmium (111Cd), Tin (118Sn), Mercury (202Hg) and Lead (208Pb). The resulting metal concentrations

were converted from parts per billion (ppb) to milligrams per kilogram tissue dry weight (mg kg-1) for comparison.

The results generated from the above method have been integrated with a similar study carried out in the lakes IJsselmeer and Markermeer (Ransijn, 2011). Zebra and Quagga mussels were sampled from the 20th July to the 9th of November 2009 from Lake IJsselmeer and from the 23th July to the 11th of November 2009 from Lake Markermeer. The mussels were divided into length categories and grouped for location, and date of collection. One way ANOVA tests were used (significance level of P < 0.05) to determine if metal concentration differed between size classes, species, seasons and locations (Ransijn, 2011).

Additional literature data on metal concentrations in both dreissenid species was collected and included in the analysis. All data relating to the situation in the Netherlands was entered into a results table. Tissue concentrations that were found to be higher or lower in Quagga mussels when compared with Zebra mussels, at locations where these species co-occur, are indicated by an upward facing arrow (↑) and downward facing arrow (↓) for individual metals, respectively. The number of upward and downward facing arrows was then counted and a final total was calculated representing the most frequently occurring situation in different water bodies in the Netherlands.

2.8. Effects of mussel fouling on native unionids

The shell characteristics of several unionid species in the rivers Rhine and Meuse were examined to determine whether infestation with dreissenids has an influence on the shell growth and age of mortality of these native freshwater mussels. The sampling locations reflect water systems with varying hydro-connectivity (Table 2.2).

The unionids were identified according to Gittenberger et al. (1998). After identification of the species, the level of dreissenid fouling was established. The mussels were divided into two classes: 1) shells with no traces of byssus threads, and 2) shells with attached dreissenid mussels or with remnants of their byssus threads.

The length, width and height of each unionid shell were measured using standard measurements of the shell (Figure 2.2; Aldridge, 1999). The average length, width and height for each type of shell (clean and overgrown) were calculated for each species. The surface area of the overgrowth with dreissenids was measured. Since the dreissenids can be detached after the death of the unionid mussel, the coverage of byssus threads was the indicator for the total surface area of the coverage. Using the surface area of the unionids (length*height) and the surface area of the overgrowth, the overgrowth percentage was calculated. When dreissenids were present, the number of individuals per unionid shell was counted and their length was measured.

To determine the age of an unionid mussel, the number of growth lines was counted. Unionid growth slows with age. Recent growth lines are closer to each other and

16 sometimes difficult to distinguish. Therefore, the number of growth lines was considered to be the minimum age of a mussel.

Table 2.2: Sampling locations for the analysis of native unionid species fouling by dreissenids.

Water body Location Amersfoort coordinates Water body Connectivity type to upstream dreissenid populations Lexkesveer ferry River River groyne crossing at 156693 398260 Yes Nederrijn fields Wageningen East of confluence Lake of river Meuse 191631 415788 Artificial lake Yes Mookerplas with Meuse-Waal canal Millingerwaard in Disused gravel Lake the river Waal 196313 430054 and sand quarry Yes Kaliwaal floodplain pit lake Upstream of the Het Meer connection with 188506 429151 Stream No the river Waal Ooijpolder, in the Disused gravel Yes, at times Lake river Waal 192763 431017 and sand quarry of high water Bisonbaai floodplain pit lake discharge Nameless In the river Waal Yes, at times floodplain floodplain 198315 430914 Artificial lake of high water lake Millingerwaard discharge Ewijkse plaat, Yes, at times River Waal west of Nijmegen 198315 430914 Side channel of high water discharge

The data set from all water systems was pooled and the data was analysed to see if there was a difference in length, height and width between clean and infested shells. Box plots were produced to allow easy interpretation of the distribution of the data with regards to the length and height relationship for clean and infested Painter’s mussel (Unio pictorum) shells. The box plots visualize the minimum, lower quartile, median, upper quartile and maximum values. The lower quartile and upper quartile were the boundaries of the box (inter-quartile range). When a value exceeded one and a half times that of the inter-quartile range, it was defined as an outlier value and represented by a dot. When a value exceeded three times the inter-quartile range, it was defined as an extreme value represented by an asterisk. Regression analyses were performed for Painter’s mussels by comparing length versus the number of growth lines to test whether infested mussels grow more slowly than clean mussels. An independent t-test was done to see if the mean length was significantly different between the clean and infested mussels. The data had to be tested for normality (One-Sample Kolmogorov- Smirnov Test) and homogeneity of variances (Levene’s test for equality of variances). The data was transformed with a natural log transformation, log transformation or square root transformation if the data did not pass one of the tests. If the transformation did not make the data suitable for an independent t-test, a Mann- Whitney U test was performed.

Figure 2.2: The measurements of the size and growth lines of native unionid mussels (modified from Aldridge, 1999).

2.9. Statistical analysis

All statistical tests were performed using PASW Statistics 18, Release Version 18.0.0 (SPSS, Inc., 2009, Chicago, IL, www.spss.com).

3. Current distribution

3.1. Life cycle and biology

The Zebra mussels (Dreissena polymorpha) and Quagga mussel (Dreissena rostriformis bugensis) are freshwater members of the family Dreissenidae (Phylum Mollusca, Class Bivalvia, Subclass Heterodonta, Order Veneroida, Superfamily Dreissenidea). Both species are indigenous to the Ponto-Caspian area but have spread via ballast water and the network of waterways into Western Europe (Van der Velde et al., 2010; Bij de Vaate, 2010b).

Dreissenid mussels in North America attain a maximum size of approximately 4 cm (Mills et al., 1996). Life spans and growth rates of Zebra mussels are variable and correlated with habitat primary productivity. The maximum age of Quagga mussels in the river Danube, Bulgaria, was 2 - 4 years (Hubenov & Trichkova, 2007) and >2 years in three Russian reservoirs (Lvova, 2004), indicative of life spans similar to that of Zebra mussels. Although limited, the available data suggests that the population dynamics of Quagga mussels, like Zebra mussels, are similar in North America and Europe.

An explanation of the life cycle of dreissenid mussels contributes to an understanding of how these species disperse in the environment (Figure 3.1). Both mussel species are gonochoristic with males and females releasing sperm and eggs into the water column. Female specimens of Zebra mussel exhibit a high fecundity, capable of releasing over one million eggs in a single spawning event (Mackie & Schloesser, 1996; McMahon, 2002; Stoeckmann, 2003; Keller et al., 2007). Female Quagga mussels are less productive than those of the Zebra mussels. When collected from the same site in western Lake Erie (OH), females of Zebra mussel released 3–4 times more eggs than females of the Quagga mussel (Stoeckmann, 2003). Males and females of both species typically reach sexual maturity within one year (Mackie & Schloesser, 1996; McMahon, 2002; Keller et al., 2007). Following external fertilization, zygotes metamorphose through several pre-settlement larval stages (i.e., trochophore and veliger; Figure 3.1) which are planktonic, enabling rapid downstream dispersal into previously uninhabited waters (Ackerman, 1995a). However, neither larval forms nor adult mussels are generally capable of moving against water currents.

A unique feature of dreissenid mussels compared to native North American and European freshwater bivalves (e.g., unionids) is that adults possess a specialized organ for secretion of proteinaceous byssal attachment threads which allow attachment to hard substrata (Bonner & Rockhill, 1994; Clarke & McMahon, 1996). Dreissenids byssally attached to ships and boats, or aquatic vegetation entangled on vessels, can be transported upstream or overland to uninfested bodies that were otherwise unlikely to be invaded through these species’ natural dispersal mechanisms (Johnson & Carlton, 1996).

Figure 3.1: The life cycle of dreissenids (adapted from: Rajagopal, 2011; Rajagopal et al., 2012).

3.2. Current distribution of the Quagga mussel

Until the 1930s, the Quagga mussel only occurred in the mouth of two rivers discharging into the Black Sea, viz. the Southern Bug and Dnieper in the Ukraine (Son, 2007; Van der Velde et al., 2010). The Zebra mussel is native to the Caspian and Black Sea regions (Ponto-Caspian area) and their associated drainages in Eastern Europe and Western Asia (Zhulidov et al., 2004).

The start of range expansion by the Quagga mussel was about two centuries later than that of the Zebra mussel, but once started it was able to extend its range at a higher dispersal rate than Zebra mussels (Bij de Vaate et al., 2002). When the Quagga mussel began its range expansion, all dispersal pathways in the form of the canal network were available. The Zebra mussel’s range expansion occurred earlier and was limited by a lack of connectivity. Range expansion of this species was facilitated in a step wise process following the construction of various canals (Leuven et al., 2009).

The Quagga mussel’s range expansion started in the 1930s (Son, 2007). Till the 1980s the Quagga mussel expansion was restricted to Russian territory (Orlova et al., 2004, 2005; Zhulidov et al., 2005). However, in the 1980s the Quagga mussel, together with the Zebra mussel, made the same jump dispersal towards North America. Both species arrived from multiple sources in the Black Sea region including the mouth of the River Volga (Therriault et al., 2005; Brown and Stepien, 2010). The discovery of the species in North America in 1991, in the Erie Canal (May and Marsden, 1992), marked the start of their range expansion on that continent (Brown and Stepien, 2010). In Eastern Europe the first record of the species was in 2004 in

20 the Romanian section of the River Danube (Micu and Telembici, 2004) and Popa and Popa (2006).

The first observation in Western Europe was made in 2006 in the Hollandsch Diep, a former estuary of the rivers Rhine and Meuse in the Netherlands (Bij de Vaate, 2006; Molloy et al., 2007; Bij de Vaate and Jansen, 2007; Schonenberg and Gittenberger, 2008). According to Bij de Vaate (2010b) the Quagga mussel introduction into Western Europe was not the result of range expansion from its native range through the River Danube and subsequently the Main-Danube canal and River Rhine, as previously suggested by Molloy et al. (2007). Ballast water transport and release in the Hollandsch Diep is thought to have been the most likely dispersal vector (Bij de Vaate, 2010b; Bij de Vaate et al., 2012). Soon other records in the Netherlands were made in the large rivers, such as the rivers Nederrijn, IJssel, Waal, Bovenrijn and Meuse, and the large canals and lakes that are part of the Dutch network of waterways, such as the IJsselmeer, Markermeer, Frisian lakes, Volkerak-Zoommeer, Pannerdensch canal, Amsterdam-Rhine canal, Rhine-Scheldt canal, Wilhelmina canal and Bathse spuikanaal (Bij de Vaate and Jansen, 2009, 2011; Bij de Vaate, 2009, 2010a; Bij de Vaate et al., 2011; Raad, 2010; Soes, 2008). Spatial analysis of available records shows that the Quagga mussel is now present in all the major rivers in the Netherlands and has extended its range to as far north as the Princes Margriet canal near Grou in the province of Friesland and the river Meuse at the Dutch-Belgian border (Figure 3.2). However, more isolated water bodies such as those located in tributaries upstream from present populations and hydrologically disconnected water bodies such as inland lakes have not been colonised so far (see also paragraph 3.3). The Quagga mussel has not yet been able to colonise large parts of the provinces of Groningen, Drente and Zeeland.

In 2007 Van der Velde and Platvoet (2007) discovered Quagga mussels in the river Main (Germany), a tributary of the river Rhine, which was the start for more observations in Germany. Martens et al. (2007) discovered the species in a series of Upper Rhine harbours, while Haybach and Christmann (2009) found them in the Lower Rhine in 2008 between Dormagen and Bimmen. In 2008 Quagga mussels were found in the Main-Danube canal (Bij de Vaate, 2010b). Mayer et al. (2009) found Quagga mussels on ship’s hulls on the slipway of a shipyard at Speyer, along the Upper Rhine. Imo et al. (2010) studied the populations in the rivers Main and Rhine in order to study their current distribution, the time of arrival and population structure. Quagga mussels found in the river Rhine were smaller than in the river Main. Population genetic analysis did reveal not any sign of founder effects. Based on non-continuous distribution and shell size they conclude that range expansion in Germany involved at least two independent settling events. The first event before 2005, probably caused by jump dispersal since they found one Quagga mussel specimen in a sample from the river Main after genetic re-examination of dreissenids collected in 2005, the second event due to continuous range expansion.

Heiler et al. (2012) observed range expansion in Germany in eastern direction through canals of which the Mittelland Canal is most important connecting river basins of the Weser, Elbe and Oder. Bij de Vaate and Beisel (2011) found them in the French section of the River Moselle, another tributary of the River Rhine, being the first

Quagga mussel observation in France. In 2009 Sablon et al. (2010) recorded the Quagga mussel for the first time from Belgium (Albert Canal, in the vicinity of Grobbendonk), while J. Marescaux (unpubl. results, Univ. Namur, Belgium) observed upstream migration of the species in the Belgian section of the River Meuse from 2010. From all these observations it became clear that the Quagga mussel is quickly expanding in Western Europe after its establishment in the Netherlands.

Figure 3.2: Current distribution of the Quagga mussel in the Netherlands.

To further characterise the spread of the Quagga mussel the cumulative number of records for the Quagga mussels is illustrated. Figure 3.3 shows a sharp increase in the cumulative number of records between the Quagga mussels initial discovery in the Netherlands and 2008 in which time a total of 206 separate locations had been identified. Since 2008 the yearly number of records has slightly reduced to 46 - 50 per year. However, this does not reveal the relationship between the number of locations where the Quagga mussel was found and the overall number of samples taken for dreissenid mussels.

300

250

200

150

100

0 CumulativeQuaggamusselrecords 2006 2007 2008 2009 2010 2011

Figure 3.3: Cumulative number of locations where Quagga mussels were identified.

Figure 3.4 expresses the number of locations where Quagga mussel was found as a percentage of the total number of sampling sites where dreissenid mussels were identified for each year. At most sampling sites several samples were taken. Since 2006, the percentage of dreissenid mussel sites wherein Quagga mussels were identified increased from <1% to 61% in 2008. In the period 2009 - 2011 this percentage was 46 - 50% of the number total locations where dreissenid mussels were recorded.

100 90 80

70 60 50 40

% totalsampled % 30 20 10 0 2006 2007 2008 2009 2010 2011

Figure 3.4: Number of locations where Quagga mussels were identified expressed as a percentage of total number of sampling sites with dreissenids.

The results indicate a steady increase in the number of locations where the Quagga mussel has been found since it was first recorded in the Netherlands in 2006. Combined with the data on wide spatial spread of Quagga records in the Dutch network of waterways (i.e. large lakes and rivers that are interconnected by shipping canals; Fig 3.2), this suggests that the Quagga mussel was able to continue its range extension in Dutch freshwaters. Differences in current spread between Quagga and Zebra mussels are mainly related to present day barriers for dispersal.

3.3. Dispersal rate

The Quagga mussel was found to disperse, by passive as well as active means, at a rate of approximately 54 km yr-1 in continuous water courses in the Netherlands. Bij de Vaate et al. (2012) estimated upstream dispersal rate of Quagga mussels in the river Meuse of about 50-70 km yr-1. Upstream dispersal in the river Meuse was probably facilitated by shipping (see paragraph 3.5). The dispersal rates of the Quagga mussel are within the range recorded by Leuven et al. (2009) for dispersal of Zebra mussels in European waterways (range 14 – 199 km yr-1; mean 65 km yr-1).

3.4. The influence of connectivity on distribution

Zebra and Quagga mussel samples were analysed separately to examine the influence of hydrological connectivity on the presence or absence of each species.

100 90 80

50 % locations absent 40

Locations (%) Locations % locations present 30 20 10 0 Permanent Seasonal connection Disconnected (n=17) connection (n=35) (n=5)

Figure 3.5: The influence of the level of hydrological connectivity on Zebra mussel presence.

The Zebra mussel was present at 60 to 70% of locations sampled where there was some degree of connectivity to upstream mussel populations allowing for the passive dispersal of the planktonic mussel larvae (veligers; Figure 3.5) or mussels attached to floating substrata (paragraph 3.5).

The Quagga mussel is present at a little over 60% of locations with a permanent hydrological connection, at approximately 20% of locations where the connection occurs during seasonal high water flow and is totally absent at disconnected locations (Figure 3.6). Until now, the Quagga mussel has only been able to colonise water courses and lakes that are included in the Dutch network of waterways and are connected to other populations of mussels allowing colonization to occur via passive dispersal of veligers in the water flow or via transport of mussels by watercraft. The

permanence of that connection is relevant in determining the chance that the Quagga mussel will be present at a particular location. The absence of mussels at permanently disconnected locations, such as inland lakes and small tributaries, suggests that upstream dispersal by watercraft and connection to upstream populations of mussels has, up to now, determined whether Quagga mussels establish within water-bodies in the Netherlands. Upstream dispersal facilitated by attachment to watercraft has been identified as an important mode of dispersal for the Quagga mussel in the Dutch parts of the rivers Rhine and Meuse (Bij de Vaate et al., 2012).

100 90 80

50 % locations absent 40

Locations (%) Locations % locations present 30 20 10 0 permanent Seasonal connection disconnected (n=17) connection (n=35) (n=5)

Figure 3.6: The influence of the degree of hydrological connectivity on Quagga mussel presence.

3.5. Vectors of colonization

The degree of hydrological connectivity together with the presence of vectors of colonization influences the ability of Quagga mussels to colonise water courses and lakes that are included in the Dutch network of waterways. The Quagga mussel has been able to colonise and is present in generally higher abundances in water bodies that are hydrologically connected to upstream mussel populations allowing passive dispersal of mussel veligers to occur and where colonization vectors are present (Figure 3.7). In water bodies where hydrological connectivity is maintained but no watercraft are present, Zebra mussel abundance represents the greater percentage of the total dreissenid population on average.

Samples taken from rivers where no upstream Quagga mussel populations exist such as the rivers Overijsselse Vecht, Berkel, Oude IJssel, Schipbeek and Niers contained no Quagga mussels. The sampling location in the river Overijsselse Vecht lies upstream of weirs that heavily reduces the possibility that mussels may disperse by passive means or by the use of vectors such as shipping sailing from point to point.

100 90

80 70 60 50 % Quagga mussel 40 30 % Zebra mussel

Average abundanceAverage (%) 20 10 0 Hydrologically Hydrologically Hydrologically connected + connected, no isolated (n=16) watercraft (n=29) watercraft (n=12)

Figure 3.7: The effect of hydrological isolation and the presence of watercraft on average relative abundance of Quagga and Zebra mussels for all sampling locations.

Figure 3.8: Vectors for dispersal of dreissenid mussels. a and b) Examples of Zebra mussels attached to floats at lake Rijkerswoerdse plassen; c and d) Temporary metal pontoon and location where Zebra mussels were attached (Photos: J. Matthews).

The definition of watercraft in this figure omits watercraft and other structures present due to overland transfer on trailers. This suggests that this vector type has not yet

26 been exploited by the Quagga mussel as a mechanism for colonization of hydrologically isolated water bodies. Inland isolated water bodies such as the lakes Rijkerswoerdse plassen and Aamsche plas, were found to be colonised by Zebra mussels only. The local use of pleasure craft, metal pontoons and floats, transported overland (Figure 3.8a-d, Rijkerswoerdse plassen) provide a route for dispersal and explain why Zebra mussels are able to colonise such locations. In spite of an extensive survey of suitable substrates, mussels were not found at any other location in Rijkerswoerdse plassen. It is possible that the mussels were already attached when these structures were positioned in the water. Quagga mussels were found attached to metal substrates at other sampling locations (metal bank reinforcement in the Wilhelmina canal at Tilburg). Therefore there remains a potential for Quagga mussels to use these types of vectors. Other possible mechanisms by which mussels could enter isolated water bodies are via waterfowl that prey on dreissenids or introduction as a measure for combating eutrophication.

The Zebra mussel arrived in the Netherlands long before the Quagga mussel and has therefore been able to exploit these vectors and colonise more isolated water bodies. It is expected that the Quagga mussel will, in time, colonise more isolated water bodies utilising the same vectors of overland transfer.

a b

c d

Figure 3.9: Vectors for dispersal of Quagga mussels: a) tire in floodplain lake; b) twig in a watercourse; c) and d) drift wood at river bank (Photo a, c and d: Rob Leuven; b: Peter Klok).

Quagga mussels were observed on rubber and were present in very high densities on the inside of a discarded tire in the Kaliwaal, a floodplain lake with a permanent

connection to the river Waal (Figure 3.9a). Mussels were observed to colonise only the sheltered inside section of the tire. Quagga and Zebra mussels were also found attached to drift wood (Figures 3.9b-d), Wood is an effective vector of colonization as it can transport adult mussels to previously un-colonised areas with the river current or flood pulse.

Table 3.1 gives an overview of colonization vectors that were identified during the literature review and field study. The material from which the vector is constructed is also relevant to mussel attachment and will be addressed in a separate section dedicated to substrates.

Table 3.1: Overview of colonization vectors relevant to the spread of dreissenids from literature and observed during field work.

Vector Mode of transport Examples and relevant information

water-flow Passive downstream In the presence of upstream populations

commercial shipping Active up / down stream Barges

watercraft Active up / down stream Large sailing boats, motor boats

Canoes, sailing / rowing / motor boats. watercraft overland Active overland dependant on resistance to desiccation

other overland Active overland Metal pontoon, floats

vegetation, wood, branches Passive downstream / active up With water-flow or attached to other and twings / down stream + overland vectors e.g. watercraft

Predatory animals such as aquatic birds, Active up / down stream + muskrats and brown rats, and attached Several animal species overland to Chinese mitten crabs, crayfish and turtles

3.6. Direction of colonization

In general, the population structure of Quagga mussels at various sampling points in the river Meuse between Afferden and Grave indicates that the proportion of mussels aged more than a year decreases the further up- and downstream of Middelaar (Figure 3.10). This indicates that in this section of the river Meuse, colonization has taken place in a southerly direction possibly via watercraft. However, the presence of a younger population in the river Meuse at Grave also provides some evidence of downstream colonization. This suggests the existence of several mechanisms determining Quagga dispersal in the river Meuse, such as up- and downstream dispersal via watercraft and downstream passive dispersal via water flow.

100

50 0-1yrs 1-2yrs 40

% total abundance total % >2yrs 30

0 Afferden (n = 232) Milsbeek (n = 123) Middelaar (n = 419) Grave (n = 169) Sampling location

Figure 3.10. The relative contribution of age classes to the total abundance of Quagga mussels found at sampling locations in the river Meuse.

4. Potential distribution

4.1. Physiological tolerance and presence in relation to environmental factors

Table 4.1 outlines the physiological tolerances of the Quagga and Zebra mussels. These factors are important for current and future establishment of dreissenid populations. Table 4.2 gives an overview of potential limitations related to past and current habitat conditions in the Netherlands. The potential effects of future trends in environmental conditions on Quagga mussel establishment will be analysed in paragraph 4.6.

Optimal pH is the same for both species. Differences between species relate to maximum pH, just as minimum calcium concentration, maximum temperature and minimum temperature for reproduction. These factors are expected to influence species replacement dependent on habitat conditions. Habitat conditions that would influence the colonization of sites by both species were related to pH and to restricted connectivity. While pH was never low enough to eliminate the possibility of dreissenid colonization at any site, there were periods at every sampling site where the pH dropped below the value that is considered ideal for both reproduction and growth. This is particularly relevant for the river Meuse at Linne where ideal pH conditions only occurred in two measurements and at a time where temperatures were unsuitable for Zebra mussel reproduction. The presence of mussels in samples taken at sites where pH dropped to between 7.5 and 8 at various times of the year supports authors who argue that while pHs below 8 are not ideal for dreissenids, pHs within this range do not rule out mussel invasion (Mackie, 2005). In a recent study by Claudi et al. (2012) adult Quagga and Zebra mussels showed 40% mortality after 11 weeks of exposure to a pH of 6.9. In the same study both dreissenid species were prevented from settling at pH 7.1. The authors commented that the pH effects, such as mortality and reduced settlement, may have been visible at less acidic values if the background calcium concentration in the water was lower than the 41 mg l-1 used in their experiments. Acidified bogs and moorland pools in the southern, central and eastern parts of the

Netherlands and locations with seepage of CO2-rich groundwater are unsuitable for colonization by Quagga and Zebra mussel.

Salinity was elevated to a level that would limit reproduction in both species for one observation at in the river Meuse at Zwartewaal. However, the singular nature of this observation makes it impossible to conclude that salinity would have a negative effect on the reproductive capacity at this location.

At locations where data was available, the main channel velocity was observed to be above values that could be tolerated by both dreissenid species.

The concentrations of Lead, Cadmium and Zinc at the locations specified in table 4.2 would not limit the Zebra mussel at any location. Due to the absence of toxicity data in relation to Quagga mussels, no conclusions can be drawn relating to the effect metal

30 toxicity on colonization of this species or on the potential replacement of the Zebra mussel by the Quagga mussel.

Table 4.1: Physiological tolerances and toxic effect concentrations of metals for the Zebra mussel and the Quagga mussel.

Quagga mussel Zebra mussel Notes

Min no data 7.49

Max no data 9.3-9.68 40% mortality after >pH8 both pH 18 18 2 11 weeks 6.9 6.9 optimal Settlement 18 18 prevented 7.1 7.1 >8-102 (growth) >910 >12-152 15-18 for life cycle Min (reproduction) Temp (oC) (reproduction) to complete (21- 30 days)2 Max 25-346, 13, 15, 16 30-343,7, 14, 15, 16 Current Min Not applicable Not applicable -1 Velocity 0.09 m s both -1 4 (m s ) Max 0.09-0.24,5 0.09-0.24,5 optimal

Min 121 81 -1 >25 no limit to Ca (mg l ) 2 Max not applicable not applicable infestation Zebra mussel: Max 53, 15 4-18.43, 15 no reproduction loss <2‰ Salinity (‰) No byssal thread Quagga mussel: 17 17 production >4 >4 reproduction occurs <2-3‰11

12 Pb µg l-1 48hr exposure no data 370 * (EC50 filt ) 10wk exposure no data 9112

12 Zn µg l-1 48hr exposure no data 560 * (EC50 filt ) 10wk exposure no data 13112

12 Cd µg l-1 48hr exposure no data 388 * (EC50 filt ) 10wk exposure no data 2712

12 Cu µg l-1 48hr exposure no data 41 * (EC50 filt ) 10wk exposure no data 4312 *50% Effect concentration (filtration); 1Jones & Ricciardi (2005); 2Mackie (2005); 3Spidle et al. (1995); 4Ackerman (1999); 5Eckman et al. (1989); 6Dom et al. (1993), McMahon et al. (1994), Spidle et al. (1995); 7Iwanyzki & McCauley (1993); 8Bowman & Bailey (1998); 9Ramcharan et al. (1992); Neary & Leach (1992); 10Bij de Vaate (2008); 11Rosenberg & Ludyanskiy (1994); 12Kraak et al. (1994); 13Mills et al. (1996); 14Ussery & McMahon (1995); 15Karatayev et al. (1998); 16Verbrugge et al. (2012); 17Grutters et al. (2012); 18Claudi et al. (2012).

Table 4.2: Suitability of water bodies for colonization of dreissenid species in the Netherlands.

Location River Panner- River River River Former Lake Lake Waal at densch IJssel at Meuse Meuse river IJsselmeer# Markermeer# Parameter Ewijkse canal Ganzen- at at Linne estuary plaat diep Zwarte Hollandsch waal Diep pH within √ √ √ √ √ √ Not done Not done physiological limits pH × × × × × × Not done Not done optimal Temperature completion of √ √ √ √ √ √ Not done Not done lifecycle Temperature √ √ √ √ √ √ Not done Not done growth Temperature √ √ √ √ √ √ Not done Not done reproduction Calcium no limit to √ √ √ √ √ √ Not done Not done infestation Salinity within √ √ √ √ √ √ Not done Not done physiological limits Salinity √ √ √ × √ √ Not done Not done reproduction Lead (Pb) EC 50filt √ √ √ √ √ √ √ √ 10wks* Cadmium (Cd) EC 50filt √ √ √ √ √ √ √ √ 10wks* Zinc (Zn) EC 50filt √ √ √ √ √ √ √ √ 10wks* Connectivity Weirs √ √ √ √ × √ √ √ absent? Connectivity Downstream of √ √ √ √ √ √ √ √ colonization source? Shipping ↑ ↑ ↓ ↑ ↓ ↑ ↑ ↑ traffic Main channel × × × no data no data no data √ √ flow velocity†

√: condition fulfils criteria for colonization; ×: condition reduces the likelihood of colonization; ↑: over 80,000 passages per year; ↔: passages between 40,000 and 80,000 per year; ↓: passages below 40,000 per year (Ministerie van Verkeer en Waterstaat & Centraal Bureau voor de Statistiek, 2003); *: Laboratory derived effect concentration for filtration where 50% of individuals were affected over a 10 week period; †: See appendix 7 for actual flow velocities; #: Adapted from Ransijn (2011).

4.2. Effect of temperature and salinity on basal thread development

Temperature and salinity are important factors limiting the local species pools of native and exotic molluscs in the river Rhine basin (Verbrugge et al., 2012). To further expand on the physiological tolerance analysis, the effect of salinity and temperature on byssal thread development of dreissenids was examined (Figure 4.1; Grutters et al., 2012).

50 0.2 ppt A B

45 2 ppt

40 9 ppt 35 30 25 20 15 10

Mean Mean numberofthreads 5 0 5 15 25 5 15 25 Temperature oC Temperature oC

Figure 4.1:The effect of varying levels of temperature and salinity on the number of byssal threads in Quagga mussel (A) and Zebra mussel (B) within 24 h of reattachment (adapted from Grutters et al., 2012).

At a water temperature of 25 °C and a salinity of 0.2 ppt the byssogenesis of the Zebra mussels was significantly higher than that of Quagga mussels, of which the byssal thread production levelled out between 15 °C and 25 °C. Byssogenesis at temperatures lower than 25 °C was similar for both species. Both species did not produce any byssus threads at salinities of 4 ppt or higher. Zebra mussels performed slightly better than Quagga mussels at almost all conditions in the 24 hour reattachment experiments. This difference is particularly pronounced at the most extreme temperatures tested. Additionally, the Zebra mussels produced nearly double the amount of byssal threads of Quagga mussels at 5 oC when combined with the lowest salinity level (0.2 ppt).

4.3. Influence of substratum on colonization

During the sampling of mussel populations it was observed that Quagga mussels are able to attach to a variety of natural and human made materials. These range from natural stone and wood to plastics, rubber and metals. While mussels were able to attach to all these materials, the level of attachment strength between different materials has been show to vary and may influence mussel colonization and the effectiveness of decontamination. Ackerman et al. (1996) found that Quagga mussel’s

33 attachment varied significantly with substrate type (natural ≥ metallic > polymeric), material composition and with the roughness of the substrates (Appendix 9). The detachment parameter (DP) is a function of current velocity and mussel length which is proportional to the actual fluid force required to detach a mussel (Ackerman et al., 1995b). Rock and steel exhibited the strongest attachment strength while the lowest attachment strength was measured on smooth polymeric substrates (Teflon, Plexiglas and acrylic) (Ackerman et al., 1996). There were exceptions to this however. PVC, for example was similar in attachment strength to natural and metallic substrates. Aluminium displayed lower attachment strengths than that of other metallic substrates. The influence of surface roughness was also examined for the different materials. The average initial surface roughness did not provide a consistent relationship with the measured attachment strength for all materials examined apart from Teflon and stainless steel (Ackerman et al., 1996). Kobak (2010) found attachment decreasing in order for resocart (phenoplast), aluminium, PVC, rubber and zinc. Lowest attachment was recorded on Penaten® cream-coated resocart. A limitation of this research is that only adult mussels have been considered. Other authors have observed a variation in mussel veliger settlement rates for the Zebra mussel between different substrates dependent on texture, chemical composition and orientation of the substrate (Marden & Lansky, 2000; Czarnoleski et al., 2004; Kobak, 2005). Chen et al. (2011) observed that Quagga mussels veligers exhibited no settlement preference between fibreglass, acrylonitrile butadiene styrene (ABS) plastic, high density polyethylene (HDPE) plastic, aluminium, stainless steel or concrete underlayment board (CUB). However, these authors considered that the disagreement between their results and others was related to sampling interval and experimental setup. It should be noted at this point that, during flood pulses, the buoyancy of drift wood will assist in the further dispersion of mussels if they become attached and that wood may be an important vector of colonization where other vectors and Quagga planktonic larvae are absent (e.g. floodplain lakes and disconnected side channels).

Dreissenids are classified as ecosystem engineers and increase the surface area of hard substratum increasing suitability for further mussel colonization by their living and empty shells (Wilson et al., 2006).

The most common substrata observed during field work were groyne stones, riprap and sand on river and lake bottoms. Only one of the core samples taken from soft substrates revealed live mussels. However, there is evidence in the literature to suggest that Quagga mussels can survive on soft substrates in lakes. In Lake Ontario, Canada, Zebra mussels were generally more abundant on hard substrate (Mellina & Rasmussen, 1994; Nalepa et al., 1995), while Quagga mussels were often found at greater proportions on deeper soft substrates (Mills et al., 1993). Wilson et al. (2006) found dreissenids at a density of 12,111 individuals per m2 on silt. However, mussel densities remained highest on hard substrata (boulder and cobble) and lower numbers on unconsolidated substrates (sand and silt). Mellina & Rasmussen (1994) suggested that higher densities present on consolidated substrates may reflect ease of attachment and substrate stability. The lack of mussels found on soft substrata in our investigation may be related to the fact that most of our sampling points were located in the littoral zone rivers (mainly groyne fields). Water velocity in rivers may limit the settling of veligers and colonization of soft substrates. Observations in the lakes

IJsselmeer, Markermeer and Volkerakmeer showed that the presence of solid substratum in the top layer of soft bottoms (e.g. old shells of marine mussels) is a facilitating factor for the presence of Quagga and Zebra mussels (Bij de Vaate & Jansen, 2011; Bij de Vaate et al., 2011). Small clumps of Quagga mussels can also expand to large mussel beds, as recently observed in lake Markermeer (Bij de Vaate & Jansen, 2011) and in a lake connected to the river Meuse near Katwijk (Figure 4.2; personal communication Peter Klok). Carpets of mussels are usually found in deeper water. In shallow lakes, such as lake Markermeer, anaerobic sediments and turbulence caused by shipping and wind resulting in regular suspension and sedimentation of fine and course particulate matter can limit colonization.

Figure 4.2: Two stages in the expansion of small clumps of Quagga mussels to musselbeds at a depth of 4 m in lake Kraaijenbergse Plassen connected to the river Meuse near Katwijk (Date October 16, 2011; Photos: Peter Klok).

In lakes and side channels of large rivers the presence of aquatic macrophytes may provide a refuge for populations of Zebra mussels that may otherwise be replaced by Quagga mussels. Mussel populations were examined in Lake Erie to determine the effects that plant substrates had on Quagga and Zebra mussel partitioning. It was found that even at locations where the proportion of benthic dreissenids had been 92- 100% Quagga mussel, Zebra mussels constituted 30-61% of dreissenids found attached to macrophytes (Diggins et al., 2004). Folino-Rorem et al. (2006) examined the effect of filamentous substratum on Zebra mussel establishment. The results suggest that the heavy settlement of Zebra mussel larvae on macrophytes may simply be a function of the increase in surface area of substratum afforded by macrophytes (Folino-Rorem et al., 2006). The size of mussels growing on filaments was, on average, smaller than those grown on control surfaces. Folino-Rorem et al. (2006) suggested that this could be evidence that when mussels reached a certain size, they migrated from filaments, however, they did not observe secondary settlement. If mussels were to settle on other substrates colonised by Quagga mussels, there may be an increase in inter-specific competition. The potential for macrophytes to provide a refuge for the Zebra mussel would therefore be reduced, also because they die off in winter time and sink to the bottom.

Table 4.3: Summary of flow velocity along banks and groynes during ship passages at various sampling locations.

River Waal, River Nederijjn, River Nederrijn, River Vecht near River IJssel at Electrobel Bakenhof (side Bakenhof, Dalfsen Rheden Ferry Nijmegen channel) Arnhem

A Amersfoort coordinates 185.7 430.3 211.1 503.8 199.7 445.8 192.5 441.8 192.6 441.8

Watercraft type commercial commercial commercial tanker tanker tanker Loaded / unloaded loaded Direction of travel downstream upstream upstream /positioning

Minimum m s-1 0.02 0.02 0.02 Maximum m s-1 0.25 0.21 0.14 Average m s-1 0.12 0.08 0.05

Minimum m s-1 (baseline) 0.03 0.00 0.05 0.00 0.00 Maximum m s-1(baseline) 0.09 0.02 0.22 0.07 0.05 Average m s-1(baseline) 0.06 0.01 0.13 0.03 0.02

River Waal, River River Meuse, River Meuse, River Meuse, Ewijkse plaat Nederrijn, Grave Eckertsedijk Middelaar Randwijk, Wageningen Amersfoort coordinates 179.4 432.8 175.6 441.3 179.7 419.4 198.2 404.7 189.6 415.7 Watercraft type commercial commercial commercial commercial commercial tankers tanker tanker tanker tanker Loaded / unloaded loaded unloaded unloaded direction of travel 1 upstream, 1 downstream, upstream, far downstream /positioning downstream far side side

Minimum m s-1 0.01 0.02 0.03 0.03 0.04 Maximum m s-1 0.42 0.08 0.09 0.23 0.22 Average m s-1 0.11 0.04 0.05 0.08 0.11

Minimum m s-1(baseline) 0.01 Maximum m s-1(baseline) 0.04 Average m s-1(baseline) 0.03

4.4. The effects of shipping on flow velocity

The effects of shipping on the flow velocity fluctuation at areas of suitable habitat may influence the chances of dreissenid establishment and survival. Flow velocity data in association with characteristics of ship passages are summarised for various sampling locations in table 4.3.

At three out of four locations where a baseline measurement was recorded, shipping affected the flow velocity in dreissenid habitat. Baseline flow velocities exceeded maximum tolerances at only one location (the river IJssel at Rheden ferry) whereas flow velocity increase immediately following ship passages exceeded maximum tolerances in five out of eight instances (i.e. the river Waal at Ewijkseplaat and Electrobel, Nijmegen; the river Meuse at Eckertsedijk and Middelaar and the river IJssel at Rheden ferry).

0.30

0.25

D. bugensis & D.

0.20 1 - polymorpha MAX 0.15

0.10 Flow velocity m s mvelocity Flow

0.05 D. bugensis & D. 0.00 polymorpha 1 11 21 31 41 51 61 71 81 91 101 111 121 131 optimum MIN Measurement number

point at which a commercial ship passes in a downstream direction

Figure 4.3: Example of the effect of passing shipping on flow velocities within dreissenid habitat in the river Waal at Nijmegen and optimum flow velocities for Quagga and Zebra mussels. For optimum flow velocities see table 4.1.

A typical example of the effect that a passing ship has on flow velocities in the near shore habitat is shown in figure 4.3. Maximum flow velocity increases from 0.12 m s-1 prior to the ship passage to 0.25 m s-1 in the time immediately following. This exceeds the maximum flow velocity tolerance for dreissenids. It was observed that at locations where maximum flow velocity was exceeded, the densities of mussels were generally low in exposed habitat. Moreover, most individuals were collected from microhabitats that offer shelter from water flow (e.g. underneath groyne stones and riprap).

4.5. Depth condition relationships

When both Quagga and Zebra mussel invade a new freshwater body they will have to use similar food resources (seston) and space (hard substratum). In the great Laurentian lakes of North America, a depth zonation could develop when both species co-occur in a lake with Quagga mussel more abundant in deeper, colder parts of the water bodies than Zebra mussel (Mills et al., 1996). Mitchell et al. (1996) also

observed this difference in abundance of both species along a depth gradient, but added that temperature tends to be correlated with depth in a lake. Although observations showed that the Quagga mussel occupies deeper zones of lakes than the Zebra mussel, no comparative controlled experiments have been conducted thus far. With increasing depth many factors change in a lake, such as water pressure, temperature, flow velocity, oxygen supply and food quantity and quality. All of these factors can influence the species distribution.

Zebra mussels collected from several deep freshwater lakes (Groene Heuvels, Berendonck, Haarsteegse Wiel) showed a decrease in the condition index with increasing depth so it is likely that some factors reduce the condition of the mussels in these lakes over depth. In order to assess the effects of depth on survival, condition and stable isotope tissue signatures of the Quagga and Zebra mussel, a transplantation experiment with cages was performed in a deep freshwater lake Groene Heuvels (24 m) for four months. The lake had already been invaded by Zebra mussels, which could mainly be found at depths of up to 9 m. The main objective of this research was to assess if Quagga and Zebra mussels respond differently to depth in a freshwater lake. The survival and condition of these species was expected to show differences along a depth gradient and both may depend on the availability and quality of food sources along the depth gradient and in time.

In contrast to observations in North America, Quagga mussels hardly survived at large depths (17 m) in a freshwater lake (i.e. a former sandpit) in the Netherlands and showed already after 3.5 weeks a very high mortality compared to Zebra mussels. Both species showed hardly mortality at lower depths (1-10 m). The condition index of the surviving mussels was lowest for both mussel species at 17 m depth. At that depth their condition index did not improve or decreased. In contrast the condition index increased after 16 weeks at lower depths (1-10 m). The condition index after 16 weeks showed a negative relation with depth. Stable isotope values of the transplanted mussels showed a shift after 3.5 and 16 weeks. In all species after 3.5 weeks trophic level (δ15N) decreased except at 17 m depth where it did not change. Furthermore, after 16 weeks in Quagga as well as Zebra mussels the carbon source changed as δ13C became more negative in all mussels transplanted to 2-10 m depth. The Zebra mussels collected outside the cages from this depth gradient showed an even much lower trophic level, but a similar carbon isotope range which correlated with seston, aquatic macrophytes and terrestrial leaf material at these shallower depths. Carbon signatures of both species at 17 m were similar to that of seston at that depth. Temperature became as low as 2 oC at that depth. The outcome of this transplantation experiment showed that larger depths in deep Dutch freshwater lakes are more favourable for Zebra mussels than for Quagga mussels.

4.6. Potential distribution map

A potential distribution map of the Quagga mussel was constructed using information on current distribution, physiological tolerances, characteristics of water bodies and vectors for dispersal (Figure 4.4).

Figure 4.4: Potential distribution map of Quagga mussel in the Netherlands (Dark red: current distribution; transparent red: potential distribution based on present day distribution of the Zebra mussel and connectivity of water bodies).

It is expected that all water bodies of the Dutch network of waterways, such as the freshwater parts of large rivers and lakes and connecting shipping canals, will be soon entirely colonized by the Quagga mussel. Colonization of isolated water bodies in the hinterland of large rivers and river tributaries without shipping or upstream populations will take much more time and change of dispersal will strongly depend on presence of suitable vectors (paragraph 3.4 and 3.5), (future) environmental conditions (paragraphs 4.1-4.5) and management measures (paragraph 6.2 and 6.3). The dispersal rate strongly depends on the hydrological regime (flow direction and velocity) and frequency of shipping passages through these waters. Without the implementation of effective prevention measures, the Quagga mussel is expected to spread to all water bodies where the Zebra mussel now occurs.

Poorly buffered and brackish or salty water bodies are unsuitable for colonization by dreissenids. Examples of these water bodies are acidified bogs and moorland pools (with a low pH and water hardness) in the southern, central and eastern parts of the Netherlands and several types of water bodies in the coastal areas with salinities above 5‰.

Future changes are expected for several environmental factors that affect establishment of populations of Quagga mussels in rivers, canals and lakes in the Netherlands (Table 4.4). A quantitative prediction of the effects of these changes on establishment success of Quagga mussels is currently not possible due to a lack of data and predictive models. However, overall it is expected that in large rivers an increase in the abundance of Quagga mussels will be limited by bank rehabilitation (e.g. removing of hard substrates) and an increase in peak discharges, wave stress due to expanding shipping activities, water depth fluctuations (desiccation) and increasing abundance of Ponto-Caspian gobies.

Table 4.4. Expert judgement of effects of future trends in environmental conditions on establishment and abundance of the Quagga mussel in the Netherlands.

Environmental factor Future trend Effect on density of Quagga mussels Water temperature* ↑ +

Salinity in coastal areas* ↑ -

Salinity of inland waters ↓ 0/+

River bank rehabilitation / ↑ - removing hard substrates River discharge / flow ↑ - velocity* Wave stress in rivers and canals ↑ -- due to increased shipping Water depth fluctuations / ↑ -- desiccation* Increase of abundance of Ponto- ↑ -- Caspian gobies in rivers *: Due to climate change; ↑: increase; ↓ decrease; --: negative; -: slightly negative; 0: neutral; +: slightly positive; ++: positive effect.

4.7. Explanations for low mussel densities in the rivers Rhine and IJssel

The absence or low densities of dreissenids at many sampling sites in the rivers Waal, Nederrijn and IJssel in 2011 was remarkable. It is at odds with previous sampling years and the lack of physiological limitation for dreissenids in the Netherlands. To try to establish a cause for the observed lack of abundance three possibilities are considered in detail for the 2011 sampling year: 1) temperature increases in the river Rhine as a result of thermal discharges and climate change, 2) the low water level in the rivers Waal and IJssel during field observations, and 3) the influence of invasive fish species predating on dreissenids.

Influence of temperature Temperatures in the river Rhine branches have increased consistently over the last 100 years due to thermal discharges and climate change. The yearly minimum and maximum river temperatures at Lobith have increased by circa 4 oC over the period 1908-2010 (Leuven et al., 2011). Increases in temperature could therefore have limited

40 the distribution of mussel species in these rivers. However, the maximum river temperature observed during field monitoring in this study was 28.5 oC measured in the river Waal at Nijmegen downstream of the thermal discharge of the Electrobel power station. This temperature lies within the range of maximum temperature tolerances found in the literature for Quagga mussels (Table 4.1). While this temperature may cause some limitation on the presence of Quagga mussels, the temperature condition found here was not representative of the Rhine river distributaries and the river Meuse in general. At most other locations maximum values for water temperature did not exceed 25 oC. No physiological limitation would occur for either species at these locations. To further examine temperature as a potentially influencing factor on survival, analysis was broadened to include historical data for the Netherlands. Data was taken from Waterbase.nl, a validated online database maintained by Rijkswaterstaat, the Dutch governmental body that is responsible for the management of the major waterways in the Netherlands. Temperature data of large rivers, canals and lakes in the Netherlands was limited to the minimum and maximum values for all Dutch monitoring stations for each month for the period 2001-2010. These data were plotted together with the maximum temperature tolerance of dreissenid mussels (Figure 4.5).

35.0

D. polymorpha 30.0 D. bugensis

25.0

C) o 20.0

15.0

10.0( Temperature

MIN 5.0

MAX 0.0 Jan-01 Jan-02 Jan-03 Jan-04 Jan-05 Jan-06 Jan-07 Jan-08 Jan-09 Jan-10

Figure 4.5: Upper temperature tolerance of dreissenid mussels in comparison with monthly maximum and minimum temperatures measured in the upper water layer of Dutch rivers, lakes and canals in the period 2001-2010 (For ranges of upper temperature tolerances of dreissenids see table 4.1).

Only Quagga mussel was found to be potentially limited by maximum temperatures but only for a limited duration and in a minority of years (2003, 2006 and 2010). It should be noted that this limitation will only occur in a very few locations. The wide range of observed maximum temperature tolerance for Quagga mussel suggests that some mussel populations may not be limited by the maximum temperatures recorded in Dutch freshwaters. Moreover, temperature readings were taken from the upper water layer and vertical temperature heterogeneity may create refuges of suitable habitat for dreissenids deeper in the water-body. It can be concluded, therefore, that maximum

41 temperatures will not limit both mussel species in the majority of surface water bodies in the Netherlands.

Influence of water level Another reason for the low abundance of mussels in the rivers Waal and IJssel in comparison to previous years and to the rivers Meuse and Nederrijn is the extreme low water level that occurred in the rivers Waal and IJssel before and during the sampling period.

The water levels in the Rhine distributaries show yearly fluctuations of several metres due to seasonal variability of river discharge. However, 2011 was a particularly dry year with water depths for the rivers IJssel and Waal remaining relatively shallow compared with the previous four years (Figures 4.6 and 4.7). The periods of low flow occurred just prior and during the sampling period and therefore would have had an impact on the sampled populations.

Mussels may display a habitat preference for deeper water in rivers that demonstrate greater water level fluctuations reducing the risk of aerial exposure. According to Smit et al. (1993) densities of Zebra mussels on stones in the river Rhine generally increase with water depth. The normal periods of low discharge partly overlap with the period of Zebra mussel reproduction. Consequently the probability of any stone being colonized will depend on its position relative to the lowest water level of that year. Mussels settled above the lowest water level during higher discharges will probably die, once water levels fall to minimum levels. However, in our field surveys no mussels were discovered attached to stones that would have been recently exposed during a drop in water level. This suggests that mussels may have detached from hard substrates thereby reducing the risk of desiccation. Jantz (1996) also noticed the negative effects of extreme low water events during four successive years (1989-1992) in the river Rhine causing declines in Zebra mussel abundance. Dense settlement of Zebra mussels could be found only at the lower parts of the river bank.

1000

800

600

400

200

0 01/01/ 31/01/ 02/03/ 01/04/ 01/05/ 31/05/ 30/06/ 30/07/ 29/08/ 28/09/ Date

Water depth Waterwith respect toNAP (cm) 2007 2008 2009 2010 2011

Figure 4.6: Year comparison of water levels in the river IJssel at Zutphen North (Data obtained from Rijkswaterstaat).

1400 1200 1000 800 600 400 200

0 Water depth NAP repsect depth (cm)with to Water 01/01/ 31/01/ 02/03/ 01/04/ 01/05/ 31/05/ 30/06/ 30/07/ 29/08/ 28/09/ Date 2007 2008 2009 2010 2011 Figure 4.7: Year comparison of water levels in the river Waal at Nijmegen Harbour (Data obtained from Rijkswaterstaat).

In contrast water depth in the river Meuse remained remarkably consistent within and between years (Figure 4.8). Mussels would therefore not have been exposed to a risk of desiccation due to a drop in water level that would have occurred, particularly this year, in the IJssel and Waal rivers.

1000

800

600

400

200

0 01/01/ 31/01/ 02/03/ 01/04/ 01/05/ 31/05/ 30/06/ 30/07/ 29/08/ 28/09/

Date Water depth Waterwith repsect toNAP (cm) 2007 2008 2009 2010 2011

Figure 4.8: Year comparison of water levels in the river Meuse at Mook (Data obtained from Rijkswaterstaat).

The Quagga mussel particularly has been shown to be less tolerant to aerial exposure than the Zebra mussel and habitat choice with regards to depth has been linked to tolerance to aerial exposure and desiccation in dreissenids (Ricciardi et al., 1995; Ussery & McMahon, 1995). The combination of remarkably low and inconsistent water level seen in the groyne fields of the rivers Waal and IJssel suggests, in extremely dry years, that these rivers provide a less suitable habitat. This is especially true of shallower waters in groyne fields, floodplain lakes and side channels. Our standard sampling method recovered mussels at a maximum depth of approximately 50-75 cm

43 below the then current water depth. Mussels living deeper in the water column in the rivers Waal and IJssel may have remained undetected.

Influence of predation by invasive fish A number of newly arrived exotic species in the river Rhine (fish and invertebrates) have made use of the southern invasion corridor, and originate from the Ponto- Caspian region (Bij de Vaate et al., 2002; Copp et al., 2005). Among these Ponto- Caspian species are fish belonging to the Gobiidae. Four invasive gobiid species have established large populations in the Rhine river system. At certain locations, the bighead goby (Neogobius kessleri), the round goby (Neogobius melanostomus) and the monkey goby (Neogobius fluviatilis) have become particularly abundant (Van Kessel & Spikmans, 2010), Numbers at which gobies are present can even exceed the levels of native fish numbers (Spikmans et al., 2010). Figure 4.9 demonstrates the remarkable increase in dominance of exotic over indigenous benthic dwelling fish in the large Dutch freshwaters in recent years.

Gobiidae are benthic fish and exhibit a preference for fast flowing river systems. In the Rhine river system the Gobiidae are still the most frequent in the main river branches (Van Kessel & Spikmans, 2010). Hard substrate constructed from basalt rocks is used to manage the river fairway. These riprap structures provide suitable living conditions for some of the Gobiidae, e.g. N. kessleri, N. melanostomus and Proterorhinus semilunaris (Adamek et al., 2007; 2010; Spikmans et al., 2010). Riprap provides habitat for fish to feed, spawn and shelter. This is particularly relevant as dreissenids occupy a similar habitat and will therefore be vulnerable to potential predation. High predatory pressure could explain the low abundance of dreissenid species found at sampled locations.

100

80 70 60 50 Indigenous 40 Exotic 30

20 percentage total percentage total abundance 10 0 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009

Figure 4.9: Relative abundance of indigenous to exotic benthic fish from samples taken from the former estuary Hollandsch Diep and the rivers Nieuwe Merwede and Oude Maas (adapted from Spikmans et al., 2010).

In a recent analysis of the diets of invasive Gobiidae present in the Dutch Rhine system, it was noted that dreissenid species constituted part of the diet of invasive

Gobiidae (Schiphouwer et al., 2011). Figures 4.10 and 4.11 indicate on the x-axis the frequency of occurrence of prey species in the stomachs of sampled goby species N. melanostomus expressed as a percentage of total numbers of individuals sampled. The y-axis expresses the ratio of total weight of a prey species found in stomach contents to the total weight of stomach contents of individuals where in that prey species was found. The contribution of dreissenids to the diet of N. melanostomus varied per habitat examined. Dreissenids were found most frequently in stomachs and represented the greatest proportion of total stomach contents of N. melanostomus sampled at the river Nieuwe Merwede (Figure 4.10). In contrast, dreissenids were found in relatively few stomachs and exhibited a low contribution to the overall stomach contents of individuals sampled from riprap in the river Waal (Figure 4.11).

The invasive gobiid N. kessleri was also examined in the study by Schiphouwer (2011). Dreissenids were found in the stomachs of only 6.3% of individuals at 1 out of 4 habitat types examined. Moreover, dreissenids contributed to only 5.4% of total stomach contents at this location. Dreissenids were absent from the stomach contents of N. kessleri sampled from riprap in the river Waal. No evidence of dreissenids was found in the stomach contents of P. semilunaris or N. fluviatilis at any location.

100

Pisces 90 80 Amphipoda 70 Dreissena 60 50 40 30 20 Isopoda Corbicula

prey specific prey abundance (%) 10 Gastropoda 0 0 20 40 60 80 100 Frequency of occurrence (%)

Figure 4.10: Feeding strategy plots with frequency of occurrence (%) and weight- based prey-specific abundance (%) of Neogobius melanostomus in the littoral zone of the river Nieuwe Merwede (n = 44) (adapted from Schiphouwer et al., 2011).

While dreissenids constituted a substantial part of gobiid diets in a limited number of locations examined, their dietary contribution to gobiids in the river Waal was relatively low. Unfortunately, the availability of dreissenids relative to other prey species was not compared with the contribution of dreissenids to overall stomach contents in the study by Schiphouwer (2011). It is therefore not possible to conclude if gobiids exhibit a preference to dreissenids over other prey species or if low contributions to stomach contents were due to low dreissenid availability as found in our study. Gobies seem to adapt to prey availability and dreissenids can contribute to a relatively large proportion of dietary intake (figure 4.10). The low contribution of dreissenids to stomach contents in the river Waal may be due to limited prey availability resulting from past gobiid

45 predation and low water levels. It therefore remains possible that predation by invasive gobiids, in addition to effects of low water levels, reduced overall abundance of dreissenids in the rivers IJssel and Waal to levels seen in the present study.

100

90 Amphipoda 80 70 60 50 40 30

ey specific ey abundance (%) 20 Corbicula pr 10 Dreissena Chironomids Isopoda 0 0 20 40 60 80 100 Frequency of occurrence (%)

Figure 4.11: Feeding strategy plots with frequency of occurrence (%) and weight- based prey-specific abundance (%) of Neogobius melanostomus at riprap in the river Waal (n = 41) (adapted from Schiphouwer et al., 2011).

5. Impact of the Quagga mussel

5.1. Macro-invertebrate composition in relation to mussel abundance

To explore the effect that Quagga mussel density has on the macroinvertebrate population, total macroinvertebrate density was plotted against the density of mussels found at each sampling point (Figure 5.1). Increasing densities of Quagga mussel tends to lead to an increase in macroinvertebrate density.

4000 3500

3000

) 2500

2 - 2000 R² = 0.1751 1500 1000

500 (individuals m (individuals 0

Macroinvertebrate density Macroinvertebrate 0 500 1000 1500 2000 2500 3000

Quagga mussel density (individuals m-2) Figure 5.1: The relation between the macroinvertebrate and Quagga mussel density on hard substrates in Dutch rivers.

To determine the effect that the Quagga mussel has on the macroinvertebrate community, a scatterplot was made comparing macroinvertebrate species richness with Quagga mussel density at each sampling point. Macroinvertebrate species richness tended to increase with Quagga mussel density (Figure 5.2).

7 6 R² = 0.1412 5 4

3 2

richness 1 0

0 500 1000 1500 2000 2500 3000 Macroinvertebratespecies

Quagga mussel density (individuals m-2)

Figure 5.2: The relation between macroinvertebrate species richness and Quagga mussel density on hard substrates in Dutch rivers.

Our observations support literature results. Dreissenid species are generally associated with increased benthic macroinvertebrate density and taxonomic richness,

and, when dreissenids are excluded, with decreased community evenness (Ward & Ricciardi, 2007). However, the densities of Quagga mussel found at our sampling sites were relatively low in comparison with other studies that examined the effect of mussel density on benthic organisms. High densities of Quagga mussel may inhibit certain macroinvertebrate species (French et al., 2009; Haynes et al., 2005). Therefore, increasing Quagga mussel density may not always be beneficial to other species.

Overall the effects of current densities of Quagga mussels on the diversity and abundance of macroinvertebrates on sampled hard substrates in Dutch waterways appear to be positive. However, based on preliminary observations in the Kraaijenbergse plassen (Figure 4.2) and evidence abroad (Prragraph 4.3), a further increase of Quagga mussel density may reduce the abundances of a series of macroinvertebrate species.

5.2. Implications of metal accumulation in mussels for food chains

To compare metal accumulation of dreissenid species in the Netherlands, metal contents of Quagga and Zebra mussels mussels originating from various sampling sites were determined (For raw data see appendix 6). Table 5.1 demonstrates that in the Netherlands on average Quagga mussels bioaccumulate metals to a lesser degree than Zebra mussels. Exceptions to this are Arsenic (As), Lead (Pb) and Selenium (Se).

Table 5.1: Overview of current knowledge of bioaccumulation of metals in the Quagga mussel in comparison with the Zebra mussel in the Netherlands.

Sampling Location Data As Cd Cu Hg Ni Pb Se Zn Source period River Yen et al. Mean nd nd 2010 Nederrijn ↓ ↑ ↓ ↓ ↑ ↓ (2011) Yen et al. River Meuse Mean nd nd 2010 ↓ ↓ ↓ ↓ ↑ ↓ (2011) Single Matthews River Waal * * * * * * * * 2008 replicate ↑ ↑ ↓ ↑ ↓ ↑ ↓ ↓ (2009) Lake Ransijn Mean Nov-09 Markermeer ↓ ↓ ↓ ↓ ↓ ↑ ↑ ↓ (2011) Lake Ransijn Mean Jul-09 Markermeer ↓ ↓ ↓ ↓ ↓ ↑ ↓ ↓ (2011) Lake Ransijn Mean Nov-09 IJsselmeer ↑ ↓ ↓ ↓ ↓ ↑ ↑ ↓ (2011) Lake Ransijn Mean Jul-09 IJsselmeer ↑ ↓ ↓ ↓ ↓ ↑ ↓ ↓ (2011) 3/5 6/7 6/7 4/5 7/7 5/7 4/7 7/7 Total ↑ ↓ ↓ ↓ ↓ ↑ ↑ ↓ Nd: not determined; *: results obtained from a single sample may introduce bias to results; ↑ metal concentration found to be higher in Quagga mussels than Zebra mussels; ↓ metal concentration found to be lower in Quagga mussels than Zebra mussels.

Analysis of data obtained by Ransijn (2011) suggests that on average, when compared with the Zebra mussel, Quagga mussels in lake Markermeer accumulated Arsenic to a lesser degree than those present in lake IJsselmeer. There also appear to

be seasonal differences in mean Selenium concentrations between the two mussel species for these lakes. Analysis revealed that metal concentrations between various size classes did not significantly differ for these species (Ransijn, 2011). Mussels in lake Markermeer contained significantly more Nickel, Arsenic, Selenium and Cadmium than the mussels of lake IJsselmeer. Lead was the only metal that showed significantly higher values for Quagga mussel when compared with Zebra mussel. All other metals examined were present in higher concentrations in Zebra mussel (Ransijn, 2011). These results are supported by Yen et al. (2011) for the rivers Meuse and Nederrijn who observed that, in general, Quagga mussel exhibited significantly lower bio- concentration and bio-accumulation factors than Zebra mussel (p < 0.0001). In the study by Matthews (2009) however, average values for Arsenic, Cadmium, Mercury and Lead in Quagga mussel all exceeded those found in Zebra mussel. However, these results should be treated with caution as they originate from a single sample.

We expect that the metal concentration in Dutch surface waters will further decrease in future due to increasing water pollution control. Current metal contents in both species of dreissenids in Dutch rivers and lakes are much lower than those recorded one or two decades ago for Zebra mussels. Therefore, it is not expected that present-day metal accumulation by Quagga mussels will pose significant risks for predators.

5.3. Fouling of native unionid mussels

Large numbers of Zebra and Quagga mussels can attach themselves to shells of indigenous unionid mussels and may compete for food (Parker et al., 1998; Schloesser et al., 1996). Table 5.2 shows the total number of shells of indigenous unionids collected in various river systems in the Netherlands. The indigenous Painter’s mussel (Unio pictorum) is the abundant species of the subfamily Unioninae and the indigenous Duck mussel (Anodonta anatina) for subfamily Anodontinae. The indigenous Compressed river mussel (Pseudanodonta complanata) was the least abundant species.

Table 5.2: The total number of indigenous unionid shells collected and the percentage of individuals that were infested with exotic dreissenids (only specimen with double valves were used for analyses). Species1 N Infested shells (%) Unio pictorum 191 52.4 Unio tumidus 96 79.2 Anodonta anatina 87 37.9 Anodonta cygnea2 14 Not observed Pseudanodonta complanata2 2 50.0 1: The Netherlands contributes to a significant part of the geographical distribution area of these species; 2: Potentially red listed species (Gittenberger et al., 1998).

Dreissenids tended to colonise unionid mussels on the part of the shell close to the siphon which is exposed above the sediment. Both Unio pictorum and U. tumidus showed relatively high infestation percentages (52.4% and 79.2%, respectively). The

49 infestation for A. anatina and P. complanata was lower (37.9% and 50%, respectively). Infestation of the Swan mussel Anodonta cygnea with dreissenids was not yet observed. However, most shells of A. cygnea were found in waters where dreissenids were absent or present in very low densities.

A Box plot was produced to determine if there was a difference in shell length between clean shells and infested shells of U. pictorum. Figure 5.3 shows a noticeable difference in unionid mussel length distribution between the clean and infested shells. The median length of clean shells is significantly higher than the median length of infested shells. The boxes do not overlap, but the presence of a number of outliers should be noted for clean shells. The clean shells show a higher maximum length than infested shells, while the infested shells have a lower minimum length when the outliers are ignored.

Figure 5.3: Minimum, lower quartile, median, upper quartile and maximum length of clean and infested shells of the Painter’s mussel (numbers refer to outliers).

The clean shells of U. pictorum show significantly higher mean length, height, width and number of growth lines (Figure 5.4). The width/length ratio for clean shells was significantly lower that that of infested shells, indicating that dreissenid infestation caused limited length growth.

Regression analysis was carried out to determine if there was a difference in growth rate of the length, height and width of infested and clean shells. Figure 5.5 shows a statistically significant relationship between the number of growth lines and the length of U. pictorum. The slope of the regression line is steeper for clean as opposed to infested shells. The R2 value is higher for clean shells than for the infested shells.

12 * * 10

* 6 Clean

Size (cm) * Infested 4 *

0 Length Height Width Growth lines WL-ratio (x10) Figure 5.4: The average length, height, width and width/length (WL) ratio for clean and infested shells of the Painter’s mussel Unio pictorum. *: Mann-Whitney U tests showed that there was a significant difference in length (U=1549.5, df=189, p<0.001), height (U=1883.5, df=189, p<0.001), width (U=1808, df=189, p<0.001), number of growth lines (U=3105.5, df=189, p<0.001) and WL-ratio (U=3355.5, df=189, p<0.001) between the clean and infested shells. The error bars in the diagram show the standard deviations.

12 11 clean shells 10 Infested shells 9

8 Linear (clean shells)

Length(cm) 7 Linear (Infested 6 shells) 5 4 0 5 10 15 Growth lines

Figure 5.5: The shell length vs. the number of growth lines for the Painter’s mussel Unio pictorum. R2 for regression lines of clean and infested mussels were 0.5089 and 0.1736, respectively. The slope of the regression line for clean shells was 0.547 (F=92.229, df=90, p<0.001). The slope of the regression line for infested shells was 0.311 (F=20.580, df=99, p<0.001).

Quagga mussels probably have a similar impact on unionid mussels as Zebra mussels. However, there is a suggestion that Quagga mussels may attach less readily to unionid shells (Conn & Conn, 1993). In the event that Quagga mussels were to

replace Zebra mussels, impacts on native unionids are predicted to be similar or possibly slightly less than those seen at present.

Table 5.3: Occurrence of species replacement at sampling locations.

Water Location period Total mussel Quagga relative Species Reference body density abundance replacement? if increase increase applicable

River Bakenhof side 2009-2011 + + /- - This study Nederrijn channel River Randwijk, 2007-2011 - - - This study Nederrijn Wageningen River Middelaar 2009-2011 - + + This study Meuse River Grave 2007-2011 nd + ? This study Meuse Meuse- Dukenburgse Brug 2008-2011 + + / - - This study Waal canal Lake Bij de Vaate Trintelhaven 10-2006 to 2010 + / - + + / - IJsselmeer (2011) Lake Bij de Vaate Houtribsluizen 2-2008 to 10-2008 nd + ? IJsselmeer (2009) Lake Bij de Vaate Enkhuizerzand 3-2009 to 12-2009 nd + ? IJsselmeer (2010a) Bij de Vaate Lake (2010a), not named 6-2009 to 11-2009 nd + ? IJsselmeer Ransijn (2011) Lake Bij de Vaate Oostvaardersdiep 2-2008 to 10-2008 nd + ? Markermeer (2009) Lake Bij de Vaate 4-2009 to 12-2009 nd + / - ? Markermeer (2010a) Former river Bij de Vaate estuary Not named 2006-2008 nd + ? (2011) Hollandsch Diep nd: not determined; +: evidence for increase or replacement; -: no evidence for increase or replacement; +/-: no consistent trend; ?: unknown.

5.4. Species replacement

In total 11 locations were identified during the literature study where data from previous sampling efforts could be used to establish if the replacement of the Zebra mussel by the Quagga mussel was occurring (Table 5.3). Species replacement was considered to be occurring if the relative abundance of the Quagga mussel with respect to the overall dreissenid populations was increasing and if the density of the dreissenids as a whole remained stable or decreased, assuming that the influence of

52 other environmental factors did not play a role in species competition. An increase in overall density associated with an increase in Quagga mussel abundance indicates that the carrying capacity of the habitat has not been reached and that intra-specific competition is not an overriding factor in determining the relative abundances of the two species.

Consistent increases in Quagga mussel relative abundance occurred at eight out of 12 locations. Three locations demonstrated an inconsistent increase in relative abundance and one location showed a decrease in relative abundance. In the majority areas sampled the Quagga mussel continues to increase in abundance relative to the Zebra mussel. Seven out of 12 sources examined lacked mussel density data or data that could be used to calculate density. The possibility of species replacement could not be assessed at these locations. Of the remaining five locations, two demonstrated a consistent increase in mussel density, one demonstrated an inconsistent increase in density and two showed a decrease in density. The increase in the relative abundance of the Quagga mussel in relation to the Zebra mussel is emphasised when yearly relative abundances for locations in the Netherlands are examined (Figure 5.6).

Figure 5.6: Quagga mussel relative abundance in lake IJsselmeer and the former river estuary Hollandsch Diep (data: Bij de Vaate, 2008; 2010a; 2012; unpublished data B. Bij de Vaate).

Our results highlight the need to assess whether Quagga mussel colonization will result in a greater level of impact or different impacts to those resulting from the Zebra mussel in cases of species replacement or increase of total dreissenid biomass. If impacts are found to be similar, then prevention of the colonization of water bodies by the Quagga mussel where Zebra mussels are already present maybe a waste of resources. To assess the relative impact of the Quagga mussel in comparison with the Zebra mussel a table was produced that summarises the current knowledge with regard to the relative impact of the Quagga mussel for the impacts described in the current chapter.

Table 5.4. Relative impacts of the Quagga mussel in comparison to the Zebra mussel.

Impact Characteristic of impact Relative impact prediction Macroinvertebrates - / + X Waterfowl - / + ↑ Unionid mussels - 0 / ↓ Macrophytes + X Fish – benthic feeders + / - X Fish – pelagic feeders - X Cyanobacteria abundance - 0 / ↑ Parasites - 0 Economic - X + positive; +/- positive and negative; - negative; ↑ impact is greater; 0 impact is the same; ↓ impact is lower.; x no evidence to suggest that a greater impact will be experienced.

Table 5.4 indicates that, in the majority of cases, there is no evidence to suggest that the Quagga mussel will have a greater impact if it were to replace the Zebra mussel. However, evidence from the Great lakes in Northern America suggests that the condition of diving ducks, such as the lesser and greater scaup (Aythya affinis and Aythya marila) that feed on dreissenids, is effected by the higher concentrations of Selenium found in the Quagga mussel (Schummer et al., 2010). Evidence regarding unionid mussels is conflicting. It has been suggested that Zebra mussels are more likely than Quagga mussels to colonise unionid shells inferring a greater impact from Zebra mussel presence (Conn & Conn, 1993). Heiler et al. (2011), however, suggest that the impact of the Quagga mussel on European unionids will probably be similar to that of the Zebra mussel. Increased levels of toxic Cyanobacteria have been linked to Quagga mussels in the presence of lower concentrations of total phosphorus (Sarnelle et al., 2010). However, elevated abundances of Cyanobacteria, relative to other divisions of the phytoplankton community, have been observed and predicted in water bodies infested by both the Zebra and the Quagga mussel with no differentiation made between individual species (Zhang et al., 2011; Makarewicz et al., 1999).

There is a potential that certain impacts may be additive due to the differing depth habitat requirement of the dreissenid mussels (paragraph 4.5). According to preliminary observations in a deep lake in the Netherlands, species replacement is not expected at depths that are less suitable for the Quagga mussel where Zebra mussels are present. Moreover, the Quagga mussel may colonise at depths where Zebra mussels are not present. Coexistence of both species at differing depths and an increase in the overall biomass of dreissenids would result in additive effects. It should also be noted that during the initial stages of colonization, most dreissenid populations increase rapidly in size followed by a decline to more stable sustainable levels (Strayer & Malcom, 2006). The magnitude of impacts may, therefore, also reduce following the initial colonization period.

5.5. Changes in food webs and energy flow

Quagga and Zebra mussels show a remarkable ability of these invasive mussels to shift aquatic food webs and energy flow from pelagic-profundal to benthic-littoral

54 energy pathways. Higgins & Vander Zanden (2011) carried out a meta analysis of 190 studies from North America and Europe that incorporated the measureable effects of dreissenid species on lake and river ecosystems. Two main pathways of effect were identified. For the pelagic-profundal pathway, large mean reductions in phytoplankton (35% to 78%) and zooplankton (40% to 77%) biomass occurred and were dependent on habitat type. The largest effects were found in rivers, followed by littoral and pelagic habitats in lakes. In contrast, benthic energy pathways within littoral habitats of lakes and rivers showed dramatic increases in mean benthic algal and macrophyte biomass (170% to 180%), sediment associated bacteria (about 2000%), non-dreissenid zoobenthic biomass (160% to 210%), and total zoobenthic biomass, which includes dreissenid soft tissues (2000%).

Mida et al. (2010) noted dramatic changes in the nutrient status of Lake Michigan in the United States that was attributed to Dreissena species. The originally mesotrophic lake became increasingly oligotrophic following the introduction and expansion of the Zebra and Quagga mussel. Reductions in the spring phytoplankton production were a result of high overall filtering capacities of the Dreissena population and the mixing of the water column during the isothermal period (Fahnenstiel et al., 2010; Mida et al., 2010). Dreissena mussels direct grazing influence is limited to within a metre adjacent to the mussels approximately therefore mixing of the water column plays an important role in determining their level of influence on phytoplankton (Edwards et al., 2005; Zhang et al., 2011). Dreissenids may compete with zooplankton which also feed on phytoplankton and are a critical link between primary production and pelagic fish production (Zhang et al., 2011; Garton et al., 2005). However, evidence that effects of dreissenids have translated to reduced zooplankton biomass in other systems is equivocal (Wu & Culver, 1991; Bridgeman et al., 1995; Johannsson et al., 2000). In addition, the level of competition may vary spatially and temporally depending on phytoplankton abundance (Zhang et al., 2011). Reduction in phytoplankton productivity has been associated with a sharp increase in summer concentrations of Silica linked to reduced diatom productivity following the introduction of the Quagga mussel. Conclusions linking the Quagga mussel to changes in primary productivity were based on (1) temporal coherence of documented changes and establishment of large populations of dreissenids, (2) seasonal-specific nature of documented changes and direct filtering effects of mussels (spring isothermal mixing only), and (3) calculated Quagga mussel clearance rate based on abundance and filtering rates compared to phytoplankton growth and turnover rates (Fahnenstiel et al., 2010). These changes will likely have important implications for the base of the fishery food web, as the pelagic region of a historically mesotrophic system becomes more oligotrophic and less able to support secondary production (Mida et al., 2010).

In Lake Michigan, North America, many invertebrates rely on the deep chlorophyll layer (DCL) as a habitat and food source. Recent changes in the DCL may contribute to future changes in the invertebrate population. For example, changes in phytoplankton species composition, attributed to dreissenid feeding, may have caused the decline of certain size classes of the opossum shrimp Mysis relicta, a species that has an important role in facilitating the transfer of energy from phytoplankton to fish and between the benthic and pelagic food webs (Johannsson et al., 2001; Nordin et al., 2008; Pothoven et al., 2010). However, present conditions are dependent on large

Quagga mussel populations and may not be sustainable (Mida et al., 2010). Nicholls et al. (1999) observed declines in chlorophyll a and a decoupling of the relationship between total phosphorus (TP) and chlorophyll a which, after ruling out other possible mediating factors, were attributed to the colonization of the US Canadian Laurentian Great Lakes by the Zebra and Quagga mussels. A substantially lower rate of change in chlorophyll at a given rate of change in TP and a lower yield of chlorophyll a per unit TP was observed after the arrival of Dreissena species (Nicholls et al., 1999). Turner (2010) observed that mussels living on soft substrate excreted higher levels of soluble reactive phosphorus (SRP) than mussels living on hard substrate. This has particular implications for water bodies invaded by Quagga mussels as they occupy soft sediment habitats at greater densities than Zebra mussels (Mills et al., 1996). This is consistent with patterns observed in Cayuga lake, New York, where hypolimnetic SRP concentrations did not increase with the arrival of the Zebra mussel, but began to rise only after the subsequent invasion of the Quagga mussel (Upstate Freshwater Institute, 2006). However, the influence of dreissenids on primary production may reduce following initial colonization. During the initial stages of colonization, most Dreissena populations increase rapidly in size followed by a decline to more stable sustainable levels (Strayer & Malcom, 2006). The increasing influence of predation and density-dependent factors would result in the decline of Dreissena populations to a level of greater sustainability. This decline would be reflected in a partial return of chlorophyll a and TP to levels seen prior to Dreissena establishment (Nicholls et al., 1999).

Examples of other physicochemical impacts related to dreissenid invasions are increases in ammonia and nitrate concentrations (Johengen et al., 1995; Effler et al., 1996; Makarewicz et al., 2000), increased nitrification and denitrification rates (Bruesewitz et al., 2006, 2008) and a decline in oxygen concentration (Effler et al., 1996; Caraco et al., 2000; Schloesser et al., 2005). Changes in nutrient availability have important implications for aquatic ecosystems, favouring the growth of filamentous alga (Heckey et al., 2004; Higgins et al., 2008), and Microcystis, a cyanobacterium that can also be found in lakes in the Netherlands with toxic strains that can threaten public health and deter zooplankton grazing (Ibelings et al., 1991; Vanderploeg, 2001; Raikow et al., 2004; Conroy et al., 2005). The greater influence of the Quagga mussel on SRP concentration when compared to the Zebra mussel may encourage the proliferation of Cyanobacteria and other nuisance species in newly invaded water bodies (Turner, 2010; Zhang et al., 2011). However, the relation between TP and Dreissena invasion as a trigger for cyanobacterial growth is not a simple one. When lakes with varying concentrations of TP were examined, dreissenid invasion caused the greatest increase in microcystin at lower concentrations of TP. Euphotic zone microcystin concentrations in invaded lakes with TP between 5 and 10 µg l-1 were about double that of lakes with TP ≥ 26 µg l-1 (Sarnelle et al., 2010). However, the concentration of TP at which cyanobacterial growth is increased by dreissenid invasions is not yet established and there is disagreement between various authors (Raikow et al., 2004; Knoll et al., 2008). Veligers are sensitive for toxic strains of Microcystis but they normally occur before the Microcystis blooms (Dionisio Pires et al., 2010).

If the Quagga mussel invades isolated lakes and tributaries where the Zebra mussel is absent and it reaches high densities (as already observed elsewhere), we expect that the impacts on food webs and energy flow will be high.

5.6. Effects on fish

The evidence pertaining to the effect that dreissenids have on the fish population relates to competition for habitat space and food at varying positions within the food web and provision of shelter against predation. Overlapping diets with invasive mussels may affect the survival of planktivorous life stages of fish through: (a) direct competition for the rotifers that are dietarily important for many larval fish and (b) indirect suppression of the phytoplankton which supports many zooplankton species (Thorp & Casper, 2003). Mitchell et al. (1996) reported a shift in Yellow perch (Perca flavescens) diet and concluded this was due to invasion of Oneida Lake by Zebra mussels. Other research has shown that dreissenids can retard growth but not survival of Fathead minnows, Pimephales promelas (Jennings, 1996). On the other hand, adults of many fish species now feed on dreissenids (Thorp et al., 1998) or other zoobenthos (e.g. amphipods) associated with benthic clusters of mussels (Thayer et al., 1997). Therefore, yellow perch may be harmed by dreissenids as larvae–juveniles but benefit as adults. Further evidence supporting the utilisation of dreissenids by fish as a major food source was found when the diets of 110 Lake chub (Couesius plumbeus) captured in 1999 in Canada indicated that they had been feeding primarily on dreissenids, not on the recovering mayflies (N.E. Mandrake, Fisheries & Oceans Canada, Burlington, Ontario, Canada, unpubl. Data). This dietary switch reduced predatory pressure on the recovering mayfly population. A recent study found that dreissenids serve as prey for some species of invasive gobiids in the Netherlands (Schiphouwer, 2011; see also section 4.7). Dreissenids were found most frequently in the stomachs and was represented in the greatest proportion of total stomach contents of N. melanostomus. However, the contribution of dreissenids to the diet of N. melanostomus varied for different habitat types. The results suggest that dreissenid invasion can encourage the colonization of other non-indigenous species that exploit these mussels as a food source, a process called facilitation causing accelerating invasions.

A number of studies have pointed towards a reduction in physiological condition of offshore fishes in lake Michigan in the 2000s relative to years previous to Dreissena invasion (Madenjian et al., 2006; Pothoven et al., 2006; Bunnell et al., 2009). Nalepa et al. (2009) noted a change in the diet of adult Whitefish (Coregonus clupeaformis) in Lake Huron, North America from the amphipod Diporeia to the Quagga mussel that reflected the alterations in the benthic community seen there. Since Diporeia have a much higher energy content than the Quagga mussel, contrasting density trends of the two organisms will have long term consequences to lake whitefish health (Nalepa et al., 2009). Observed impacts on the whitefish population in Lake Ontario were die-off, dispersal, declines in juvenile and adult condition and growth rates, delayed age-at- maturity and several years of reproductive failure (Hoyle et al., 2008). All of these studies attribute at least part of the decline in condition to either an observed or presumed decline of Diporeia in fish diets as Diporeia abundance has declined.

It should also be noted that increases in habitat complexity associated with high densities of dreissenids reduces the ability of benthivorous fish to successfully capture benthic invertebrates (Gonzalez & Downing, 1999; Cobb and Watzin, 2002; Beekey et al., 2004).

We expect that a future increase in Quagga mussel density in water bodies in the Netherlands may slightly reduce productivity of planktivorous fish and will only reduce benthivorous fish and macroinvertebrate species at locations with high abundances such as those observed in the Kraaijenbergse Plassen (e.g. see figure 4.2). Effect on fish communities are expected to be large in case of establishment of Quagga mussels in isolated water bodies where the Zebra mussel is still absent.

5.7. Effects on macrophytes

The presence of Quagga and Zebra mussels has been attributed to assisting in the recovery of certain macrophyte species by reducing water turbidity and therefore facilitating photosynthesis. During the 1980s, increases in water clarity due to dreissenids in the lower Detroit river were said to have made a possible contribution to the recovery of the American wild celery (Vallisneria americana Michx.) (Schloesser & Manny, 2007). In a study of Oneida Lake, New York in the United States clarity attributed to Zebra mussel filtration increased from 3.0 to 5.1 metres. In addition, macrophyte species richness increased, the frequency of occurrence increased for most species, and the composition of the macrophyte community changed from low- light–tolerant species to those tolerating a wide range of light conditions (Zhu et al., 2006). Stuckey & Moore (1995) observed that some aquatic plants lost due to increases in turbidity in western Lake Erie in the United States returned following the introduction of Quagga and Zebra mussel. The ability of dreissenids to increase water body clarity and resulting changes in the macrophyte population has wider implications. The physical structure provided by macrophytes is required by many zooplankton, invertebrates and fish species for feeding, nursery habitats or shelter against predation (Zhu et al., 2006). In Lake Veluwe in the Netherlands the growth of Chara beds, made possible through the clarification of the water column by Dreissena and reductions in the Bream (Abramis brama) population by commercial fishermen, resulted in a considerable increase in the number of fish species (Lammens et al., 2004). Other effects on macrophytes attributed to dreissenid invasion are reduced photosynthetic ability due to the attachment of mussels to and the weighing down of leaves and local enrichment of the substrate due to the deposition of pseudo-faeces (Zhu et al., 2007). Densities colonising leaves can vary from 200-2000 individuals per metre squared depending on plant species (Lewandowski & Ozimek, 1997) However, the authors suggest that these effects are of less importance to macrophytes when compared to the clarification of the water column.

We expect that a future increase in Quagga mussel density in water bodies in the Netherlands will reduce the nutrient contents and improve the transparency of the water, thereby facilitating growth of native macrophytes.

5.8. Effects on birds

Quagga and Zebra mussels are staple food for water birds such as diving ducks, such as Tufted Duck (Aythya fuligula) and Greater scaup (A. marila), and Coot (Fulica atra) (Mörtl et al., 2010; Van Eerden & De Leeuw, 2010). Lakes such as the IJsselmeer and Markermeer and the former estuaries Hollandsch Diep and Haringvliet are important overwintering areas for diving ducks. This is because of the presence of carpets of Zebra mussels on the bottom of these lakes which consists nowadays for the majority of Quagga mussels. The mussels can be grazed from a maximum depth of 6 metres. In how far the Quagga mussel has increased the carrying capacity of these areas for water birds is still unknown. Quagga mussels may compensate for the loss of Zebra mussels in the Markermeer (Noordhuis et al., 2010).

Elevated levels of Arsenic, Lead and Selenium in Quagga mussels in comparison with Zebra mussels suggest a higher risk of increased metal transfer to higher trophic levels in the event that the Quagga became the dominant species. Moreover, Selenium has been suggested to impact on staging and winter body condition and health of Lesser and Greater scaup. Due to potentially high tissue concentrations of Selenium in dreissenids, feeding on these mussels may influence hepatic Selenium concentrations to a greater degree relative to other prey for some species of ducks (Schummer et al., 2010). Sea duck may accumulate Selenium via alternate pathways such as by feeding on amphipods that have scavenged dead and broken dreissenids that are abundant after winter storms (Schummer et al., 2008). Certain species of diving duck could therefore bioaccumulate Selenium to a greater degree if Quagga mussel were to become the dominant prey species. Other potential pathways are intake of water, substrate (grit), plants, periphyton, and pseudo-faeces from dreissenids (Bruner et al., 1994; Ohlendorf, 2003).

There is evidence to suggest that dreissenid mussels have played a role in the deaths of fish eating birds through Clostridium botulinum intoxication. Mussels accumulate Clostridium botulinum type E toxin gene (spores) during filter feeding and then pass these spores on to fish during predation. These fish are then eaten by birds which suffer high levels of mortality as a result. Predation of the Round Goby (Neogobius melanostomus) that may feed in and around mussel beds has been identified as a reason for the high mortality of fish eating birds in Lake Erie, North America (Yule et al., 2006). A second route of transmission in the same lake has been postulated for benthic invertebrates. Not only do dreissenids concentrate the toxin as they filter water proximal to the sediments that contain the Clostridium bacteria, they also generate large amounts of faecal deposits that may contribute to the anoxic conditions favouring the proliferation of Clostridium (Holeck et al., 2004). Softer sediment is modified into a bed of living and dead mussels, shells, and faeces and pseudo-faeces accumulate, creating potential C. botulinum habitat. In Lake Erie, North America, benthic organisms (chironomids, oligochaetes, nematodes, Dreissena and mayflies) carry higher levels of spores than sediments, and chironomids contained some of the highest levels (Perez- Fuentetaja, 2011). Potentially, higher concentrations of spores within mussel beds may lead to increased concentrations of spores within benthic macro-invertebrates. Invertebrates can subsequently carry the spores at different depths, facilitating the

transfer of the bacteria to benthic feeding fish, salamanders (Necturus maculosus) and waterfowl (Perez-Fuentetaja, 2006).

Increased overall dreissenid biomass will increase the availability of food to diving ducks. This will prove beneficial to these predatory birds. The risk of Clostridium botulinum intoxification to individual birds will probably remain the same as the numbers of Dreissena consumed by individuals will remain the same. However, due to probable future improvements in water quality, health risks related to Selenium bioaccumulation are expected to decline.

5.9 Parasites of dreissenid species

There is currently a lack of empirical research into the potential of Quagga mussel to carry parasites. What little research has been done suggests that Quagga mussel can carry a similar combination of parasitic species as Zebra mussel (Popova & Biochino, 2001). Parasites found in this study were the trematode Aspidogaster limacoides, the leeches Caspiobdella fadejevi and Helobdella stagnalis, eggs of the water mites of the genus Unionicola, and representatives of nonspecific saprotrophic fungi of the genus Acremonium. The suggestion that Quagga mussel carries similar bacteria to Zebra mussel may have implications to human and animal health as Zebra mussel is frequently contaminated with the human enteric parasites Cryptosporidium parvum and Giardia lamblia (Graczyk et al., 2003). However, concentration over and above ambient water concentration does not occur as the number of parasites in mollusc tissue progressively increases in relation to the concentration of waterborne contamination, and decreases after cessation of the contamination (Graczyk et al., 2003). The ciliate Conchophthirus acuminatus has also been found in Quagga mussels. In this study both the Zebra and Quagga mussel, sampled from the same place, were found to contain C. acuminatus. However, prevalence was significantly lower in the Quagga mussel. This suggests that the Quagga may be an accidental host in which C. acuminatus cannot survive and/or reproduce (Karatayev et al., 2000).

There is also evidence that parasites may reduce the spread of dreissenid mussels by interfering with reproduction. A parasite of the Zebra mussel, the trematode Bucephalus polymorphus, predominantly infects and can totally destroy gonadal tissue (Laruelle et al., 2002). The parasite therefore uses the reproductive energy of the mussel, limiting reproduction, while leaving other tissues alone thereby allowing its host to live a normal lifespan. One record exists of infection of the Quagga mussel by B. polymorphus; a prevalence of 6% was reported (Chernogorenko & Boshko, 1992).

There is a possibility that Quagga mussels may carry higher densities of certain parasites than Zebra mussels. The parasitic oligochaete Chaetogaster limnaei was found to be slightly but statistically significantly more prevalent in Quagga mussel than in Zebra mussel (Conn et al., 1996). C. limnaei was associated mostly with gill surfaces with only one example associated with ovarian tissue. Some evidence of damage to gill and mantle epithilium was observed suggesting that these organisms were mildly pathogenic to both dreissenids species (Molloy et al., 1997).

The chironomid species Paratanytarsus sp. has been observed in both Quagga and Zebra mussel. However, the relationship between Paratanytarsus sp. and dreissenid mussels is thought to be commensal as no damage to mussels resulted from their occupation by this chironomid. Benefits to chironomids appear to be shelter from predation by fish and elevated supplies of dissolved oxygen and food particles. A maximum of six chironomid larvae per mussel was observed, however, a single larvae was most frequently encountered (Molloy et al., 1997).

Both Quagga mussel and Zebra mussel play host to a similar range of parasite. However, the risk of transferring parasites to other host species in the Netherlands may increase in case of further spread and increase of the total density of dreissenids.

5.10. Predators of dreissenid mussels

Quagga mussels will be consumed by various predators. The same predators are involved as for Zebra mussels. An extensive survey of these predators is presented by Molloy et al. (1997). It is well known that Zebra mussels are consumed in Europe by fish such as invasive gobies (Molloy et al., 1997; Schiphouwer, 2011), Roach (Rutilus rutilus) (Stanczykowska et al., 2010; Kobak & Kakareko, 2011) and Eel (Anguilla anguilla) (Bij de Vaate et al., 2010b), water birds such as the diving Tufted Duck (Aythya fuligula), Scaup (A. marila) and Coot (Fulica atra) (see paragraph 5.8; Mörtl et al., 2010; Van Eerden & De Leeuw, 2010), and mammals (brown rat Rattus norvegicus) (Aldridge, 2010).

Future increase in dreissenid biomass will be beneficial to predator species due to decreased inter- and intraspecific competition for food sources.

Figure 5.7: Smothering of Quagga mussels by the freshwater sponge Ephydatia fluviatilis observed in a lake connected to the river Meuse near Katwijk (Date: 16 October 2011; Photo: Peter Klok).

5.11. Competition by other sessile species

Quagga mussels dying can also result from smothering by sessile organisms such as sponges (Molloy et al., 1997). Smothering of Quagga mussels by the freshwater sponge Ephydatia fluviatilis was recently observed in a lake connected to the river Meuse (Figure 5.7). However, longterm effects of smothering on viability and abundance of Quagga mussels are unknown.

5.12. Economic consequences of dreissenid invasions

Dreissenids clog water intake pipes, water purification plants, and the cooling facilities of electric generating plants resulting in severe socio-economic impacts (Pimentel et al., 2005). This leads to severely impeded water flows and damage to these facilities. The removal of dreissenid mussels following industrial biofouling is costly. Other sectors potentially impacted by these species are aquaculture, managed lakes, boatyards / marinas, fisheries and public docks (Oreska & Aldridge, 2011). Information on the economic impact of dreissenids in Europe is scarce. In Britain the estimated yearly cost of controlling invasive species is £ 26.5 million (≈ 24 million Euros) per year and these estimates are highest for Canadian pondweed (Elodea canadensis) and the Zebra mussel (Oreska & Aldridge, 2011). An overview of the economic cost of dreissenid invasion in the Netherlands is lacking (Van der Weijden et al., 2007).

In a 2007 survey that incorporated all surface water-dependent drinking water treatment and electric generation facilities within the current range of Zebra mussels in North America, the costs of mitigation were estimated. Between 1989 and late 2004, approximately $267 million (≈ 200 million Euros) in total was spent on preventing and mitigating dreissenid infestation of electricity generation and water treatment facilities in North America (Connelly et al., 2007). It appeared that electrical generating facilities were spending more on mitigation and control than drinking water facilities, however this could not be tested for statistical significance due to small sample size (Connelly et al., 2007). Further impacts that were not included in this survey are other infrastructure impacts on industry and navigation, natural resources impacts such as those to fisheries, or economic impacts related to recreational boating and tourism. The total economic cost will therefore be far higher. A further estimate put the yearly damages of Zebra and Quagga mussels invading and clogging water intake pipes, water filtration, and electric generating plants in the United States at $1 billion (≈ 0.76 billion Euros; Army, 2002). Due to remarkable differences in type and location of water purification facilities and power plants in northern America and the Netherlands it will not be possible to extrapolate these cost estimates to the Dutch situation. Therefore, we recommend a detailed survey of societal costs of biofouling by dreissenids and other invasive species.

A method of gaining insight into the costs incurred is the examination of measures that need to be taken to prevent or mitigate against Quagga mussel invasion. Some of the following actions at the time of writing were already employed in, or could have been

62 used for, coping with Quagga mussels in lake Mead in the United States (Turner et al., 2011):

1. Establishment of educational and disinfection programs for recreational boaters to prevent introduction to new waters. 2. Chemical treatment of drinking waters or application of filters which can even filter out dreissenid larvae. 3. Application of coating materials for water intakes and associated equipment, or new intakes. 4. Physical removal of Quagga mussels colonizing water pipes, dam gates, boats or other highly infested infrastructures. 5. Setup of monitoring programs to assess the impacts and potential impacts on drinking water, infrastructure and the ecosystem. 6. Contracts with consulting companies to evaluate means to minimize the impacts. 7. Research projects addressing the need to monitor, control and prevent Quagga mussels. 8. Meetings and workshops to update and share information on Quagga mussels with other agencies.

Although no costs were calculated for these activities the impact is severe in terms of direct cost (e.g. control and prevention) and indirect losses (e.g. potential fishery decline). Future increased dreissenid biomass will increase the risk of biofouling of the water intakes of water purification plants and the cooling facilities of power plants. This will result in increased economic costs due to the increased requirement for mitigation of mussel fouling.

6. Scope of management measures

6.1. Preventive and management measures currently applied

Many different approaches to management of dreissenids have been considered and executed, most resulting in only limited success. To date, no single dreissenid mussel control technology has been proven to be 100% effective. None will work in all water settings, and many control measures pose significant risks to the environment. However, a wide variety of control methods do exist for dreissenids, and many are suitable or practical for some situations. Appendix 10 gives an overview of the treatments available. This chapter describes examples of management strategies applicable to preventing biofouling by mussels of the water system (e.g. lakes and rivers), infrastructure (e.g. water purification and power generation plants) and mitigation of vectors of colonization (e.g. watercraft).

6.2. Water system approach

It is expected that, without the implementation of effective prevention measures to reduce dispersal, the Quagga mussel will spread to all locations in the Netherlands where the Zebra mussel now occurs (paragraph 4.6). This means that many tributaries and isolated lakes, including several water bodies in Natura 2000 areas, are vulnerable to Quagga mussel establishment .

Early detection of dreissenids in previously uninfested water systems is important to increase the chances of successful eradication. If mussels are detected early, facility operators may have approximately three to five years to adjust systems before the population of mussels are large enough to restrict the flow of water, clog pipes, restrict water intakes, affect cooling systems and impede power generation (Hosler, 2011).

Monitoring programs should be considered for high priority water bodies where infestation is either most likely or would cause significant harm to water systems or other key resources (US Department of the Interior). Monitoring for dreissenids can be conducted in a variety of ways (e.g. visual inspection, substrate samplers, microscopic and DNA identification). Visual inspections involve the examination of submerged surfaces both visually and through touch, young Quagga mussel are described as feeling like sandpaper. Artificial substrate samplers are suspended at different depths to provide surfaces for any Quagga mussel veligers to colonise and then examined every few months (Santa Barbara County Parks Department, 2008).

To ensure early detection, monitoring programmes are recommended that focus on the microscopic identification of Quagga mussel veligers (Figure 6.1) and the detection of DNA of dreissenid species in plankton tow samples (Hosler, 2011). Based on previous experience, other methods of early detection such as substrate samplers and shoreline surveys have been less effective than plankton tow net sampling (Hosler,

2011). However, microscope and DNA detection are costly and time consuming (Santa Barbara County Parks Department, 2008).

Figure 6.1: Identification of Quagga mussel veligers by Cross Polarized Light Microscopy (Hosler, 2011).

Other activities that are recommended prior to the identification of dreissenids in a water system are (US Department of the Interior):

1. Develop Coordinated Response Plan(s) - This plan would detail policies, command and authority structure, strategies, communications, roles and responsibilities, and response actions to be implemented.

2. Perform Infestation Risk Assessment(s) – The purpose is to identify which water bodies are most at-risk of infestation within the geographic region of interest or management jurisdiction. Analysis would be based on the physiological tolerances of mussels outlined in chapter 4 and the conditions found at the specific water body (e.g. water chemistry, the presence of vectors such as recreational boats).

3. Perform Facility Vulnerability Assessment(s) – This activity may be completed as standalone or following the infestation risk assessment(s) and consists of a detailed inventory of critical water related infrastructure at a water body and how each component is likely to be affected by mussels should infestation occur. The results can be used to prioritize facility protection needs and actions.

When monitoring tests reveal a positive result for Quagga and Zebra mussels, then extended environmental risk assessment and more intense monitoring of the mussel population becomes applicable (Turner et al., 2011; Wong et al., 2011). Evaluating the environmental conditions gives management some idea of the likelihood of infestation or population explosion (Hosler, 2011).

During the course of this study a number of factors have been identified that can reduce the dominance of dreissenids in the water system. These are water depth fluctuations, substrate type and flow velocity. Quagga and Zebra mussels in 2011 were found to be much more abundant in the river Meuse where water depth is constant

compared with the rivers Waal and IJssel where water level is more varied and was remarkably low during the sampling period. Variation of water level may therefore be a viable management option for reducing the risk of Quagga mussel infestation. The use of materials during construction of water management structures and industrial facilities that discourage the settling and attachment of Quagga mussel veligers may help to reduce the chance of colonization. Examples are the replacement of metallic materials with polymeric or selecting smoother natural materials. Strategies are recommended to avoid the creation of refuges that offer protection from elevated flow velocity, i.e. void spaces in riprap and groyne structures, will reduce the possibility of mussel veliger settlement. The siting of structures vulnerable to mussel fouling at areas subject to current velocities of over 0.2 m/s will help prevent the settlement and development of mussel populations.

Once the Quagga mussel is established the chance that management measures will lead to complete extirpation, particularly for large water bodies, is low. In a recent US study a team composed of malacologists, limnologists, fisheries biologists, and hydrologists concluded that despite years of experience with Quagga mussel colonizations in Europe and North America, there is no way to eliminate Quagga mussels once they have colonized an area the size and volume (35.2 km3) of lake Mead (LAME, 2007). For these types of water body, containment through the management of colonization vectors maybe the only option. However, the possibility still exists that curative management measures may be successful for smaller water bodies. As well as reducing the risk of establishment, measures such as variation of water level, drainage and removal of refuges combined with strategies targeted specifically at infrastructure and the water system may be successful in removing Quagga mussels. The following paragraphs explore the possibilities for reducing the impact of watercraft as vectors of colonization and curative measures aimed at infrastructure.

6.3. Management of colonization vectors

Although dreissenids are relatively intolerant to prolonged emersion relative to other aquatic organisms, Zebra and Quagga mussels can survive a maximum of 22 days in water-saturated air (>95 percent relative humidity) at 15 oC (Ussery & McMahon, 1995). Anthropogenic mechanisms like recreational boating and the accompanying transport of infested fishing gear and boats can often be a more important determinant than water currents, flooding, attachment to animals or transport in fish guts (Padilla et al., 1996; Buchan & Padilla, 1999; Johnson et al., 2001; Britton & McMahon, 2005) and the spread of aquatic invasive species to the inland water bodies of North America can most likely be attributed to this mechanism (Bossenbroek et al., 2001; Johnson et al., 2001; Leung et al., 2006). Our own sampling has revealed evidence of hull contamination by both the Zebra and Quagga mussel in the Meuse at harbours in Plasmolen and Well. Analysis of hydrological connectivity in the Netherlands suggests that, while the Zebra mussel is present in relatively high densities, the Quagga mussel has not colonised more isolated water-bodies. However, it continues to increase in density in some of the main connected waterways e.g. the river Meuse. This suggests that, without proper decontamination, pleasure boats transported over land or

66 travelling upstream from infested water-bodies pose a threat to currently un-infested hydrologically isolated water-bodies in the Netherlands.

Figure 6.3: Highway signs designed to raise awareness of invasive species policy and laws (Dolphin & Boatner, 2011).

Figure 6.2: Flyer designed to

raise awareness of invasive

species programs.

Figure 6.4: Examples of signs placed at boating access sites (Dolphin & Boatner, 2011).

Table. 6.1: Minimum temperatures and durations required to induce 100% mortality in the Quagga mussel during hot water treatments.

Temperature Duration (s) Application Pre-treatment Reference (oC) technique 80 5 hot water spray 2 weeks immersed in lake Comeau et al. (14.07 kPa) water at 11.85 oC ± 1.61 oC (20110 70 5 hot water spray 2 weeks immersed in lake Comeau et al. (14.07 kPa) water at 11.85 oC ± 1.61 oC (2011) 60 5 hot water spray 2 weeks immersed in lake Comeau et al. (14.07 kPa) water at 11.85 oC ± 1.61 oC (2011) 54 10 hot water spray 2 weeks immersed in lake Comeau et al. (14.07 kPa) water at 11.85 oC ± 1.61 oC (2011) 50 20 hot water spray 2 weeks immersed in lake Comeau et al. (14.07 kPa) water at 11.85 oC ± 1.61 oC (2011) 43 300 Immersion Immersed for 24 hours at 20 Beyer et al. oC (2011) 40 40 hot water spray 2 weeks immersed in lake Comeau et al. (14.07 kPa) water at 11.85 oC ± 1.61 oC (2011) 38 1200 Immersion Immersed for 24 hours at 20 Beyer et al. oC (2011) 33 7200 Thermoshocks Bruijs et al. (2010); Rajagopal et al. (2010a)

There are two viable approaches to the management of pleasure boat colonization vectors: public education and vessel decontamination (Hickey, 2010). These measures will be only effective in limiting dispersal of Quagga mussels to uninfested upstream sections of streams (river tributaries) and isolated water bodies (lakes that are not connected to the network of water ways) in the Netherlands. However, boat owner compliance is a vital requirement for the effectiveness of decontamination strategies and lack of boat owner awareness has been cited as a reason for dreissenid invasion in North American lakes (Mueting & Gerstenberger, 2011). Therefore an effective educational campaign that explains decontamination procedure and the reasons for decontamination is required. This will minimise the risk of infestation of isolated water- bodies by Quagga mussels. In the United States, outreach and education programmes use the internet and printed media to educate the public on the effects of invasive species and the responsibilities of pleasure boats users. Boat clubs, boat sellers and water-sports centres are identified and sent letters outlining pleasure boats user’s responsibilities and educational material that can be distributed to the public. Boat shows are used to communicate to pleasure boats users about invasive species and provide an opportunity to showcase printed materials (Figure 6.2 and appendix 11). Billboards are located at strategic locations along highways (Figure 6.3) and signs are placed at boating access sites to educate and remind pleasure boats users of their responsibilities before going on the water (Figure 6.4). Public presentations can be made to interest groups e.g. angling societies and training can be given to marina owners in the prevention of invasive species spread. Education programmes and other pleasure boats management strategies can be partly paid for by creating an aquatic invasive species prevention permit that is paid for yearly by pleasure boats users

68 making use of the water-system (Dolphin & Boatner, 2011). Bernat et al. (2010) described management strategies to prevent further spread of dreissenids by motor boats and sailing yachts in Spain. According to these authors knowledge of the location of jetties colonized by dreissenids is required to control navigation in the affected areas.

The invasion of hydrologically isolated water-bodies by the Zebra mussel in the Netherlands suggests that current procedures for decontaminating boats and equipment may not prevent the invasion of Quagga mussels to these water bodies. The following paragraphs describe recommendations for the decontamination of boats and equipment found in the literature.

The thermal treatment of boats and equipment is preferable to the use of chemical oxidisers e.g. chlorine, potassiumchloride and hydrogen peroxide, non oxidising chemicals e.g. molluscicides, copper sulphate and metal ions and high pressure sprays due to concerns related to their toxicity, disposal and potential damage to hull surfaces (Beyer et al., 2011). Thermal treatment is one of the most efficient, environmentally sound and cost effective methods (O’Neill & MacNeill, 1991). Many studies examining the upper temperature tolerance of Dreissena examined mussels that underwent a period of gradual acclimatisation (Spidle et al., 1995; Ussery & McMahon, 1995). This does not replicate methods used during thermal decontamination in practice where no initial acclimatisation occurs (Beyer et al., 2011). Thermoshock treatment with 33 oC for a period of two hours also appeared to be a very promising technique and resulted in 100% mortality of Quagga mussels (Bruijs et al., 2010; Rajagopal et al., 2010a). Table 6.1 summarises the results of research that examines the temperature required to induce 100% mortality in Quagga mussels applying methods that replicate those typically employed at cleaning stations. It is normally assumed that thermal tolerance of veligers is lower than that of adult mussels, however this assumption requires further study (Beyer et al., 2011).

It can be seen that the combination of a high pressure, high temperature water jet is much more effective than immersion in hot water alone. Differences in temperature tolerance and duration required to induce 100% mortality may alter according to season. Mussels taken from water at lower temperature, during winter, may require a longer duration of treatment before tissue reaches lethal temperature (Comeau et al., 2011). Therefore, special attention should be given to the pre-treatment when applying the results of these studies to real world situations. It is therefore recommended that hulls contaminated with Quagga mussels should be spray treated at a temperature of 60 oC for at least 5 seconds. The upper thermal limit of the Quagga mussel is in general lower than that of the Zebra mussel (Spidle et al., 1995; McMahon, 1996; Mills et al., 1996). Hot water treatments can therefore be carried out over a shorter duration when a boat is contaminated with Quagga mussels only, which may increase the compliance of boat owners (Comeau et al., 2011). However, it is unrealistic to expect that owners will differentiate between Quagga and Zebra mussels when their boats are undergoing decontamination. Therefore the minimum requirement for the removal of Zebra mussels should be applied i.e. 60 oC for 10 seconds (Morse, 2009). To increase treatment efficacy, inducing mussels to gape prior to application and / or delaying the

valve closure response by exposing mussels to air for several days should be encouraged (Morse, 2009).

To ensure that no residual contamination occurs special attention should be devoted to well sheltered areas where Dreissena tend to settle such as motors, anchors, intakes and outlets, trim tabs and centreboard slots (Morse, 2009). These are areas where the above guidelines may not apply as they would not receive a direct spray and water as runoff from other surfaces may cool to an ineffective temperature before it reaches them. Table 6.2 categorises these areas and give recommendations for treatments and further research.

Table 6.2: Hot water treatment recommendations for different boat structures to ensure full decontamination of Quagga mussels (adapted from Comeau et al., 2011).

Category Structure Recommendation for decontamination

Hull and other easily Hot water spray at 14.07 kPa and 60 oC for at 1 accessibly areas least 5 seconds

Gimbal and other difficult Tests required to determine duration required to to access areas reach lethal temperature. 2 Dependent on materials and ambient temperature

Ballast tanks, bladders Hot water treatment at ≤54 oC for durations that * 3 and other heat sensitive induce 100% mortality areas * Temperature above which sensitive components are at risk of damage (Zook & Phillips, 2009)

6.4. Management strategies for biofouling of infrastructure

Due to limitations in management strategies for removing Dreissena mussels on a water system level more targeted approaches to protect infrastructure need to be considered. Mussel control in cooling water systems is generally achieved by means of chlorination (Rajagopal et al., 2010b). In comparison to other oxidising biocides, chlorine is effective at low concentrations and against all fouling categories, from bacteria to molluscs (Rajagopal et al., 2002a). In spite of the efficacy of continuous chlorination, utilities still use intermittent chlorination to get rid of adult mussel populations, largely due to cost factors and the need to reduce discharge levels (Rajagopal et al., 2003; 2010b). Chlorination is therefore practiced either in continuous or intermittent modes. A review of literature indicated that majority of industries which follow intermittent chlorination use about 1–4 hours chlorination followed by 1–8 hours break cycle, depending on the water temperature and breeding season of mussels (Jenner et al., 1998; Claudi et al., 1994; Rajagopal et al., 1996; 2010b). Mussels are capable of protecting themselves from the deleterious effects of chlorine by shutting their shells. They have the ability to sustain themselves on anaerobic metabolism for a considerable length of time, often for several days (Rajagopal, 1997).

Efficacy of chlorine as an anti-foulant depends on various parameters, most importantly residual levels of chlorine and contact time (Mattice & Zittel, 1976; Rajagopal et al., 2002). A survey of existing literature shows that at residual levels commonly employed (1 mg l-1) in power station cooling circuits, mortality takes several days (Rajagopal et al., 2003). Experimentation by Rajagopal et al. (2003) found that even when concentrations were as high as 3 mg l-1 mussels were able to protect themselves against chlorine by closing their shell valves, surviving for long periods. This indicates the inherent limitation of intermittent chlorination (4 hours on and 4 hours off cycle) in situations where mussels are involved. A break in chlorination after 4 hours, invariably resulted in resumption of valve activity comparable to the control readings, indicating complete recovery. On the other hand, shell valve openings of continuously chlorinated mussels remained low as compared to control experiments throughout the experimental period. It is recommended therefore that power stations effected by Dreissena mussel fouling review intermittent chlorination as a method of mussel eradication.

In experimentation, 95% mortality of Zebra mussels has been achieved after 552 hours of continuous exposure to 1 mg l-1 residual chlorine (Van Benschoten et al., 1995) and 882 hours continuous exposure at 0.5 mg l-1 residual chlorine for mussels removed from the Dutch Rhine (Rajagopal et al., 2002a). Continuous dosing of at least 0.5 mg l-1 residual chlorine was found to be required before shell opening was critically impaired (Rajagopal et al., 2002b). Therefore, 0.5 mg l-1 residual chlorine appears to be the minimum chlorine level to be dosed continuously, for the successful control of Zebra mussels in the Netherlands. As an alternative to continued dosing of chlorine, pulse chlorination takes advantage of the recovery period that mussels undergo following chlorine exposure. During continued exposure to chlorine, mussels close their shells, switch to anaerobic metabolism and stop filter feeding. Once chlorination stops, mussels reopen their shells, switch back to aerobic metabolism and, following a period of recovery, begin filter feeding. Pulse chlorination involves the intermittent exposure of mussels to chlorine. Chlorine dosing is restarted just prior to the resumption of filter feeding at the end of the recovery period (Rajagopal et al., 2010b). In this way mussels are prevented from feeding in a similar way to that of continuous dose chlorination. Moreover, the constant switching from anaerobic to aerobic metabolism between periods of exposure and non-exposure leads to rapid physiological exhaustion (Bruijs et al., 2010). Importantly, the duration of the recovery period differs for different mussel species, therefore the treatment needs to be tailored to the specific mussel species involved (Rajagopal et al., 2010b). This method is considerably better for the environment and, in nearly all situations where pulse chlorination is applied, chlorine levels remain within limits set by the regulator (Bruijs et al., 2010).

Temperature is an important factor that can determine the exposure time required to achieve 100% mussel mortality. For example, for dreissenids taken from the river Rhine in the Netherlands, 1,026 h is required to reach 95% mortality using 0.5 mg l-1 residual chlorine at 10 oC, compared to 456 hours at 0.50 mg l-1 chlorine and 25 oC (Rajagopal et al., 2002a). Moreover, vulnerability to biocides may vary due to seasonal effects. In Autumn and early Spring Zebra mussel may be more tolerant to biocides

71 because they have lower metabolic rates (Quigley et al., 1993) and reduced filtration rates (Kilgour & Baker, 1994), which result in less exposure to toxicants.

There are a number of disadvantages to the use of chlorine, however. The prolonged dosing period required for chlorine to control dreissenids results in delays during which the negative effects of biofouling on infrastructure will continue. Chlorine is rather expensive and hazardous to transport, store, and handle. Chlorine dosed into pipelines that exit into open ecosystems can impact deleteriously on non-target biota in the recipient waters. Moreover, continuous dosing in raw water produces ecotoxic trihalomethanes (THMs) by reaction with organic material in the water (Bernabeu et al., 2011). Therefore it makes sense to examine possible alternatives to the current use of chlorine to mitigate mussel fouling. One such alternative is the BioBullet (Figure 6.5). The approach involves the microencapsulation of crystals of potassium chloride (KCl) which is toxic to zebra mussels, with particles that are edible to zebra mussels (Aldridge et al., 2006, Elliott et al., 2010). The main benefits of this method are:

Targeted exposure to dreissenid mussels. Low dosage of toxin. Continuous dosing not required.

Figure 6.5: Scanning electron micrograph (SEM) of Bio- Bullets. Scale bar is 100 µm. (Aldridge et al., 2006).

In initial experimentation an initial 12 hour dosing of BioBullets resulted in 60% mortality of mussels. The authors predicted an overall mortality of 84% following a second dosing. To examine the potential toxicity of BioBullets to non-target organisms, 120 individuals of the indigenous unionid mussel Anodonta anatina were exposed to water containing KCl at a concentration that reflected that seen following BioBullet dissociation. Individuals of A. anatina were exposed for 12 hours and then transferred to tanks containing de-chlorinated tap water and observed for 7 days. No mortality was observed in either experimental or control groups following exposure. Unionids are likely to be some of the most sensitive filter-feeding organisms in recipient waters (Bogan, 1993). It was therefore concluded that that BioBullets containing KCl and dosed at the levels used in the experimentation are unlikely to impact on nontarget biota (Aldridge et al., 2006).

Other ongoing research is focussed on the use of bacteria as a biocontrol agent for both Zebra mussels and Quagga mussels in power generation plants (Molloy, 2008). A strain of the bacteria Pseudomonas fluorescens has been identified that will induce >90% mussel mortality under laboratory conditions. Tests to assess the effects of this strain of P. fluorescens on non-target species were carried out on Daphnia magna. Results indicated that P. fluorescens was not lethal to this species. However further research is required to establish the correct dosage of bacteria for large scale plant treatments and the economic viability of commercial application of the treatment. Moreover, results for dreissenid mortality were not always consistent requiring further refinement of the treatment process (Molloy, 2008).

Photo-catalysis (an oxidation process based on sunlight) has been put forward as a further mechanism that can mitigate against dreissenid fouling of irrigation equipment. The main benefits of the process are (Malato et al., 2007; 2009):

The employment of robust equipment that requires low maintenance. The use of hazardous chemicals can be avoided or reduced to low concentrations. The economic and ecological advantage from using sunlight.

Water to be treated is dosed with a photo-catalyst (e.g. titanium dioxide or hydrogen peroxide with a catalytic dose of iron) and passed through an apparatus that allows exposure to sunlight (Figure 6.6).

Figure 6.6: Pilot plant for wastewater detoxification using photo-catalysis (Bernabeu et al., 2011).

In controlled experimentation approximately 70% damaged dreissenid larvae (Figure 6.7) were observed after 2 hours of solar irradiation with 0.2 and 0.5 g l-1 of titanium dioxide. Treatment with hydrogen peroxide (10 mg l-1) and iron could be a promising alternative as approximately 80% damaged larvae were detected in only 3 hours irradiation (Bernabeu et al., 2011).

Figure 6.7: Damage suffered by veliger larva following hydrogen peroxide treatment (Bernabeu et al., 2011).

The use of quaternary ammonia cleaning solutions has been suggested as an additional method for the decontamination of small scale equipment. In an experiment by Britton et al. (2011), Quagga mussel veligers were subjected to a 3% solution of quaternary ammonia cleaning solution for different durations and survival was assessed by examining ciliary movement within a 2 minute period following exposure. If no ciliary movement was observed the veliger was assumed to be dead. It was found that a 5 minute exposure duration was insufficient to kill 100% of tested veligers. However a 10 minute exposure was effective in killing all tested veligers, but not immediately after treatment. An additional 60 minutes were required after the quaternary ammonium solution was removed before 100% mortality was achieved (Britton et al., 2011).

A strategy that can be used in association with decontamination is prevention of mussel settlement through the application of chemical coatings. The most common type of anti-fouling coating is a surface paint that leaches a biocide into the water to repel organisms. For example copper and copper-nickel mesh has been found to be extremely effective at preventing fouling by dreissenid mussels (Dormon et al., 1996). However, coatings using copper and more recently tributyl tin (TBT) have been phased out due to evidence of toxicity to non-target organisms (Angarano, 2007; Wells & Systema, 2009). Coatings based on foul-release mechanisms are effective and would limit initial settlement and strength of attachment, but are mechanically weak and are subject to failure due to detachment and abrasion. In general, protective coatings such as coal tar, epoxy or other anti-corrosion anti-abrasion agents are not considered effective against mussel settlement. Increasing restrictions on the chemical mitigation and control methodologies used to prevent their macrofouling, particularly organometallic or oxidizing chemicals, continue to stimulate research efforts to develop effective yet environmentally benign antifouling agents against this species and other macrofouling organisms (Angarano, 2007). New coatings that prevent fouling by creating slippery surfaces through reduced surface tension have been developed. Examples of these include the use of non-metal fouling repellents in traditional coatings, non-toxic foul-release coatings (ablative hydrophilic polymer films and low free surface energy films), and thermal spray coatings (slow dissolution of metal ions

74 repels fouling organisms) (Yebra et al., 2004). However, due to their cost, the use of chemical coatings should be targeted and applied in combination with other prevention strategies. In a recent American study, the cost of applying anti-fouling silicone coatings to hydropower facilities in the Columbia River Basin was estimated to be $127 (≈ 96 Euro) per m2 over a five-year period. The effective lifespan of silicone coatings is limited to 6 years therefore the economic feasibility of their use is brought into question. Moreover, many coatings lack long-term, objective assessment of their lifespan, durability, and performance (Wells & Systema, 2009).

7. Discussion

7.1. Hydrological connectivity and vectors of colonization

The results indicate that the dispersal of the Quagga mussel is hindered by a lack of hydrological connectivity and facilitated by the presence of colonization vectors such as watercraft and temporary structures such as pontoons and floats that are moved between water bodies. Samples taken from tributaries of large rivers and hydrologically disconnected water bodies contained no Quagga mussel individuals. The sampling locations in these tributaries lie upstream of possible colonization sources. The most likely method of upstream spread is through the movement of adult stages fixed to the bottom of ships and barges (Keevin et al., 1992). The presence of river traffic increases the probability of shipping being a major contributor to the dispersal of Dreissena in the Netherlands. In fact, the presence of only a single vessel may be sufficient to inoculate a water body that has suitable impoundment and water quality characteristics (Allen & Ramcharan, 2001). Substrate sampled in the rivers Berkel, Schipbeek and Niers were predictably devoid of mussels. These locations lie upstream of known populations of mussels and are characterised by a general absence of watercraft meaning that the chance of Dreissena colonization is relatively low. Only the Zebra mussel was found in the Oude IJssel. This sampling point is located upstream of established mussel populations but the river is used by commercial shipping and pleasure boats alike. Colonization of the Oude IJssel by the Quagga mussel will in all likelihood occur in the future. Quagga mussels were found attached to the hulls of pleasure boats in the Harbours at Plasmolen and Well, therefore there exists the potential for Quagga mussels to use this vector to colonise upstream habitats. Quagga mussels may be less able to remain attached to watercraft and therefore less able to exploit this as a vector of colonization. In flowing water Zebra mussels produce more byssus threads than Quagga mussels (Peyer et al., 2009). If mussels are attaching to watercraft hulls in transit a lower attachment strength may result increasing the risk of detachment.

We observed a slower dispersal of Quagga mussels over isolated water bodies than in continuous water bodies like large rivers and other waterways. This phenomenon was also described for the Zebra mussel (Bidwell, 2010). The attachment of mussels to watercraft that are then transported overland is an important mechanism in determining the potential for colonization of hydrologically isolated water bodies. Mussels may either attach to colonization vectors directly or attach to macrophytes that have become entangled in pleasure craft. Attachment to macrophytes has been implicated in the spread of Zebra mussels both by drift (Horvath & Lamberti, 1997) and overland transport on boats (Wilson et al., 1999; Johnson et al., 2001). While overland dispersal of the Zebra mussel can result from the actions of a wide variety of potential natural and human-mediated methods, transient recreational boating is commonly perceived as the primary means by which the species is transported between unconnected bodies of water (Johnson et al., 2001). The absence of the Quagga mussel in the river Vecht and lakes Rijkerswoerdse plassen and Aamsche plas may be explained by its relative intolerance to drying compared to the Zebra mussel as

observed by Allen & Ramcharan (2001) and Ricciardi et al. (1995) and the length of time mussels would need to tolerate out of water while being transported overland. Moreover, Quagga mussels appear less able to attach to macrophytes than Zebra mussels (Diggins et al., 2004). If Quagga mussels are less likely to attach to macrophytes then macrophytes are also less important as vectors for overland and drift dispersal. An alternative explanation is that no Quagga mussels were present at the original colonization source, made more probable by the more recent and ongoing establishment of this species in Western European waters. Other mechanisms for upstream movement of veligers have been put forward in the literature which may play a role in upstream dispersal where physical barriers such as weirs are not present. The movement of currents upstream facilitating veliger transport can occur due to winds and retentive eddies that develop near the shore (Thorpe et al., 2002). Johnson & Carlton (1996) argued that the only likely natural mechanism for colonising upstream areas was transportation by aquatic birds or other aquatic animals (e.g. turtles and muskrats).

The importance of overland transport to dispersal combined with the observation that the Quagga mussel has yet to invade hydrologically isolated water bodies whether watercraft are present or not, demonstrates a need to focus on the prevention of dispersal via this mechanism. The importance of management measures such as watercraft decontamination to prevent overland dispersal should not be underestimated.

7.2. Direction of colonization

Upstream spread suggests that active dispersal mechanisms e.g. attachment and transport on ships hulls, are an important factor for colonization in the river Meuse. However the presence of a younger population at Grave suggests that passive downstream spread also plays a role in dispersal. Populations of Quagga mussel have also been discovered upstream in the river Meuse at Namen in Belgium (Bij de Vaate, personal communication, 2011; Marescaux et al., 2012) and in the river Moselle in France (Bij de Vaate, personal communication, 2011). Therefore, passive dispersal by water flow may also originate from beyond the Dutch border. Graphs illustrating the size frequency distribution of mussel populations at each of these locations give a more detailed overview of population structure (Figures A5.1-A5.4, appendix 5).

7.3. Presence and abundance in relation to environmental factors

The main channel velocity was observed to be above that could be tolerated by both dreissenid species. However, channel velocity is widely variable dependent on where measurements are taken. Flow velocities recorded near river banks and near the river bottom are lower than those observed in the main channel (Section 4.4). Areas of lower flow velocity will provide refuges for dreissenid species. It should be noted that mussels may be able to acclimatise to adverse pH, temperature and salinity conditions (Bij de Vaate, 2008; Bowman & Bailey, 1998; Thorp et al., 1998) resulting in a less black and white interpretation of physiological tolerance. It is apparent that for the

physicochemical parameters considered, few would limit the spread of either dreissenid species at the observed sites within the Netherlands.

7.4. Effect of temperature and salinity on byssal thread development

Differences in temperature and salinity were observed to do little to determine the possibility of species replacement when examining byssal thread production alone. However, the greater ability of Zebra mussels to produce byssal threads may facilitate dispersal. It has been observed that in flowing water Zebra mussels produce more byssal threads than Quagga mussels, which is in accordance with the observation that Zebra mussels remains dominant in areas with a higher water velocity when both species co-occur (Peyer et al., 2009). This has implications for the ability of Quagga mussels to utilize certain vectors of colonization, particularly watercraft. Water passing over a ship’s hull may inhibit byssal production in Quagga mussels and, assuming individual byssal thread strength is similar for both species, increase the risk of detachment. Byssal growth inhibition at extremes of temperature and salinity would increase this risk for the Quagga mussel particularly. This would reduce the ability of Quagga mussels to use watercraft as vectors for colonization. This may help to explain why this species arrived in the Netherlands after the Zebra mussel (in addition to the much smaller native distribution range of the Quagga mussel compared to the Zebra mussel).

7.5. The effects of shipping on flow velocity

It cannot be concluded, that water velocities at the sampled locations limit the presence of either species of Dreissena as the maximum flow velocities described in table 4.1 were determined in experiments using constant flow velocities. Moreover, both dreissenid species were present at three out of five locations where flow velocities exceeded the upper velocity limit described in literature. Mussels were predominantly found in voids within riprap, attached to the underside of stones. The protection offered by stones creates a microhabitat that is shielded from the adverse effects of flow velocity fluctuation.

Maximum tolerance values for water velocity were derived from experimental data on its effect on filter feeding in adult mussels. However, current velocity and turbulence will also affect the ability of mussel veligers to settle and attach to substrate. It is therefore recommended that further research is carried out to determine the effects of shipping and flow velocity fluctuation on dreissenids.

7.6. Metal accumulation in Quagga mussels and implications for food chains

Dreissenid mussels have a profound effect on food webs, in the case of high densities. They are the staple diet of many fish species (Karatayev et al., 1997) and populations of certain waterfowl species have been reported to alter their dietary intake and migration patterns in response to the ready availability of zebra mussels (Petrie &

Knapton, 1999). The replacement of Zebra mussel by Quagga mussel and differences in the way these two species accumulate metals may affect predator species occupying higher trophic levels (see paragraph 5.4 and 5.8).

Possible toxicity of Cadmium and Copper would be of most concern to predator species foraging on Zebra or Quagga mussels (Rutzke et al., 2000). In the majority of Dutch studies the Zebra mussel was seen to accumulate Cadmium to a greater degree than the Quagga mussel on average. In the river Waal, Cadmium appears in greater concentration in the tissues of Quagga mussel than in the Zebra mussel replicate containing the maximum concentration of Cadmium. However, lower levels of Cadmium in samples of Quagga mussel were observed in mussels originating from the rivers Meuse and Nederrijn and lakes IJsselmeer and Markermeer contradicting this observation (Yen et al., 2011; Ransijn, 2011). Quagga mussel has been seen to accumulate Copper to a lesser degree than Zebra mussel in the rivers Nederrijn and Meuse and lakes IJsselmeer and Markermeer (Yen et al., 2011; Ransijn, 2011). In laboratory studies with mussels collected at the outflow of Lake Ontario, Johns & Timmerman (1998) showed that both species bio-concentrated Copper, Cadmium and Zinc but Quagga mussels accumulated higher levels of Cadmium while Zebra mussels concentrated higher levels of Copper and Zinc. This supports the results of Dutch studies for Copper and Zinc but contradicts results for Cadmium. The weight of evidence suggests, therefore, that Copper and possibly Cadmium bioaccumulation may pose a reduced risk for predators if Quagga mussel was to replace Zebra mussel in the Netherlands.

7.7. Fouling of native unionid mussels

It has been demonstrated that dreissenid infestion inhibits the growth of the unionid mussels. This growth inhibition may result from blocking of the unionid siphons as well as competition for food by dreissenidss attached to unionid shells. Blocking of the unionid siphons may eventually lead to mortality. Caraco et al. (1997) reported a decline in phytoplankton when dreissenids were introduced to a river. Dreissenids compete directly with unionids for algal cells and suspended particulate organic matter (Parker et al., 1998) and laboratory experiments have demonstrated a species specific, nutritional stress on unionids from competition with dreissenids (Baker & Hornbach, 1997). Baker & Hornbach (1997) reported acute physiological effects of dreissenid infestation on two American unionid species. Oxygen uptake and grazing rate was significantly lower when the shell was infested with dreissenids. Parker et al. (1998) reported a lower organic material content in the gut of heavily infested American unionid species that confirms a lower food uptake. Fouled mussels had a lower physiological condition than unfouled mussels. In a European study Painter’s mussel Unio pictorum showed a stronger decline in glycogen, an indicator of mussel condition, with increasing zebra mussel load (Sousa et al., 2011).

Infestation of unionids by Zebra and Quagga mussel can result in high levels of unionid mortality. In the upper St. Lawrence River unionids suffered heavy (90-100%) mortality at sites where dreissenids occurred in high densities (i.e. 4000 – 20,000 m-2), significant declines were observed when mean infestations exceeded 10 dreissenids

per unionid (Ricciardi et al., 1996). Ohnesorg et al. (1993) stated that indigenous unionid mussels were extirpated from the main channels of the Detroit river in North America as a direct result of dreissenid infestation. A theory for mechanisms that enhance unionid mortality is the interference of normal activity (feeding respiration and locomotion) in such a way as to cause the unionid to expend energy reserves required for surviving winter (Ricciardi et al., 1996). Zebra mussel is more likely to exist on unionid substrate suggesting that the replacement of Zebra mussel by Quagga mussel would reduce the impact of mussel fouling on unionids (Conn & Conn, 1993). However, a study of unionid mussels in the river Main indicated that individuals of A. anatina are overgrown with both dreissenid species (Heiler et al., 2011). The authors concluded that the impact of Quagga mussel on European native fauna will be probably similar to that of Zebra mussel.

A comparison with historic and recent distribution maps do not indicate local extinction of European unionids as a result of fouling by dreissenids, although a bias in results due to difference in monitory effort for both periods has to be taken into account (Gittenberger et al., 1998). Therefore extirpation of European unionid species by dreissenid infestation is not expected, which is in contrast with results of studies of American unionids (Schloesser et al.,1996; Schloesser et al., 1998). European unionids are still common in river systems after the introduction of the Zebra mussel 200 years ago.

Fouling of unionids by dreissenids has been seen to have indirect effects on other species. The European bitterling, Rhodeus amarus lays its eggs in unionid mussels. A recent investigation was carried out to discover the effect that dreissenid fouling has on the likelihood of unionid mussels becoming hosts to the European bitterling. Only 27% of Zebra mussel-fouled Painter’s mussels hosted bitterling, while 47% of unfouled ones hosted bitterling (Zu Ermgassen & Aldridge, 2010).

7.8. Species replacement

At only one location was species replacement confirmed (the river Meuse at Middelaar). Species replacements were also reported for the river estuary Haringvliet and lake Volkerakmeer, with relative abundances of Quagga mussels of >95 and 99% related to total number of dreissenids, respectively (Bij de Vaate et al., 2010b, 2011). There is evidence to suggest that species replacement is occurring at Trintelhaven in lake IJsselmeer, but this cannot be confirmed due to variations in overall mussel density during the period examined. A consistent approach and a focus on mussel density as-well as overall abundance is required to determine whether the Quagga mussel is replacing the Zebra mussel in Dutch freshwaters.

7.9. Effects on macroinvertebrates

Our results demonstrate that increasing densities of Quagga mussel at hard substrates tend to lead to an increase in macroinvertebrate density and species richness.

However, available literature data on the influence of dreissenids on benthic macroinvertebrates are conflicting.

Empirical evidence suggests that increases of some benthic species do occur following proliferation of dreissenids (Griffiths, 1993; Stewart & Haynes, 1994; Howell et al., 1996). Mussel residency on soft sediment has profound effects on invertebrate biodiversity. For example Bially & MacIsaac (2000) noted that mussel-sediment habitat supported between 462% and 703% more taxa, and between 202 and 335% more individuals (exclusive of dreissenids) than adjacent soft sediment lacking mussels. Dense aggregations of dreissenids generally cause local increases in the total density and taxonomic richness of smaller-bodied benthic macroinvertebrates (Ward & Ricciardi, 2007). An example from the Netherlands of a species that may have benefited from the increased abundance of the Quagga mussel is a freshwater snail, the River Nerite (Theodoxus fluviatilis) at Enkhuizerzand in lake IJsselmeer. Abundance of this locally rare species has increased due to the increased availability of food sources (sessile algae). The increase in the abundance of algae is probably due to the increased clarity of lake water that has resulted from Quagga mussel filter feeding (Bij de Vaate et al., 2009).

Other studies, however, have found that the increases are only temporary (Haynes et al., 1999) or the response of macroinvertebrates was negative rather than positive (Nalepa et al., 2007). For example, on rocky substrata, dreissenids may competitively exclude other primary space occupiers, such as netspinning caddisflies and large snails (Wisenden & Bailey, 1995; Ricciardi et al., 1997; Ward & Ricciardi, 2007). Furthermore, a reduction in evenness has also been associated with dreissenid invasions, indicating that some macroinvertebrate species benefit disproportionately from the modified habitat (Ward & Ricciardi, 2007). Nalepa et al. (2009) noted a decrease in the abundance of amphipods Diporeia spp., sphaeriid mussels and chironomids in Lake Huron, North America that coincided with an increase in Quagga mussel abundance while Zebra mussel numbers remained stable. These authors concluded that the observed reductions in macroinvertebrate abundance were most likely attributed to the increases in Quagga mussel abundance. Studies examining Lake Ontario in Canada and Lake Erie in North America also attributed the decline of zooplankton populations of Diporeia spp. to the establishment of Quagga mussel citing food competition or the toxic effects of pseudofaeces as possible mechanisms (Dermott, 2001; Lozano et al., 2001; Watkins et al., 2007).

8. Conclusions and recommendations

8.1. Conclusions

Literature data and sampling results show that the Quagga mussel has rapidly extended its distribution to a large proportion of all the hydrologically connected waterways in the Netherlands (from the river Meuse in the south to the Princes Margriet canal in the North and from the river Rhine in the east to the large river estuaries and lakes in the western part of the country). However, overall abundance and density at sampled sites was still relatively low.

There are a number of factors that potentially determine the characteristics of Quagga mussel spread. The analysis of physiological tolerances suggests that typical physico-chemical ranges found in Dutch surface waters do not eliminate the potential for colonization of Quagga and Zebra mussel. Substrate type was found to be a major determinant of local mussel distribution. Both the Quagga and Zebra mussel were observed to prefer hard substrata (riprap, metal canal bank supports, their shells and those of other molluscs) over soft substrata (sand, mud). In general, dreissenids have been observed to prefer natural hard substrates over metallic and lastly polymeric substrata like PVC.

The Quagga mussel is present to a much lesser degree in hydrologically isolated water bodies than in the network of water ways (interconnected rivers and lakes by canals). These include locations upstream of current populations of Quagga mussel or landlocked water bodies such as isolated lakes. Isolated water bodies are vulnerable to infestation due to the movement of contaminated watercraft and other waterborne structures upstream or overland. Commercial shipping and transient recreational boating are commonly perceived as the primary means by which dreissenids are transported between connected and unconnected bodies of water. Quagga mussels have been observed attached to pleasure boats indicating that they are able to use these as a vector for colonization. This is supported by observations in the river Meuse and in several rivers abroad that suggest that colonization has also occurred in an upstream direction, only possible in the presence of colonization vectors. Efficient decontamination will reduce the possibility that the Quagga mussel will invade currently uninfested hydrologically isolated locations. However, the possibility of further spread cannot be completely ruled out due to the presence of other less important colonization vectors such as waterfowl and rodents.

Observations of relative abundance indicate that Quagga mussels are contributing to an increasing percentage of overall dreissenid abundance in the Netherlands. However, due to data limitations, species replacement could be confirmed at only a few locations.

Quagga and Zebra mussels prefer habitats with relatively low flow velocity. Quagga mussels appear to be more sensitive to current flow than Zebra mussels.

Dreissenid mussels have incurred major economic costs as a result of mitigation strategies to prevent biofouling. The locations of (new) water intake pipes and other structures at power stations and water purification installations could be selected using these factors to minimise the risk of biofouling with mussels.

If the Quagga mussel were to directly replace the Zebra mussel then types and magnitudes of impact related to mussel colonization is judged to be similar for the majority of ecological effect categories. Exceptions to this are impacts to waterfowl where negative effects of Selenium bioaccumulation could be greater and to unionid mussels where effects of shell fouling may be similar or less.

There is some evidence to suggest that replacement of the Zebra mussel by the Quagga mussel may lead to an increase in the potential for cyanobacterial growth. However, research examining the effect of individual mussel species on Cyanobacteria is limited.

Dreissenid mussels constitute an important food source for waterfowl and fish. In general, Quagga mussels exhibit metal bioaccumulation factors that are lower than that of the Zebra mussel. However, higher tissue concentrations of Arsenic, Lead and Selenium in the Quagga mussel may increase the risk of toxicity prey species.

Dreissenid mussels can reduce lake turbidity which stimulates aquatic macrophyte growth and allow their return at locations where these plants have been lost due to eutrophication. However, there is no evidence to suggest that the replacement of Zebra by Quagga mussels will strengthen or weaken this effect.

Evidence examining the effects on macroinvertebrate populations is mixed, however, changes in the macroinvertebrate population are likely to occur as a result of increased Quagga mussel abundance.

Although the amount of research carried out on the parasitic load is limited, the Quagga mussel has been observed to carry a similar range of parasites to the Zebra mussel. The only exception of this is Chaetogaster limnaei that was found in higher abundance in the Quagga mussel.

Finally, It should be emphasised that many of these effects are dependent on the abundance and density of dreissenid mussels present in any one water body. The low abundance of dreissenid mussels found suggests that impacts described above would be limited in the sampled water bodies.

8.2. Effective management options

Recommendations for control measures are made in relation to the mechanisms that are most likely to facilitate the spread and high population densities of the Quagga mussel in the Netherlands.

Watercraft have been determined to be the major vector that will facilitate the spread of his species to currently uninfested water bodies. Therefore, implementation of (legal) procedures for the decontamination of watercraft and other waterborne structures (e.g. buoys, pontoons, temporary jetties) can be effective. Current guidelines and procedures for the decontamination of watercraft and other waterborne structures are reviewed out in chapter 6 of this report.

The inclusion of environmental factors that encourage or limit dreissenid mussel colonization in water management and design of structures within water bodies can be effective in discouraging their further spread, biofouling and negative effects at high population densities. Relevant factors are current velocity, water level, substrate choice, shelter availability, water depth, and habitat heterogeneity (e.g. presence of aquatic macrophytes).

Public awareness campaigns on the presence, vectors for spread and potential ecological, economical and public health effects of Quagga mussels can be an effective tool to raise the level of support for management options, such as the decontamination of watercraft. Several (non) governmental organisations in North America have a large body of knowledge on design and execution of public awareness campaigns to prevent unwanted spread of dreissenids mussels.

8.3. Recommendations for further research

To enhance the body of knowledge regarding the effects and management of Quagga mussels in the Netherlands further research is recommended in the following areas:

The effectiveness of current watercraft decontamination measures to limit spread of Quagga mussels and other invasive species to isolated water bodies.

The economic impact of dreissenids in the Netherlands, including positive as well as negative effects.

The level of total phosphorus concentration in aquatic systems that would precipitate cyanobacterial growth following Quagga mussel colonization.

The impacts of high densities of Quagga mussels on the food webs in various types of ecosystems.

The effects of current velocity and wave disturbance on microhabitat use of dreissenids mussels due to commercial and recreational shipping.

Analyses of future temporal trends in dreissenid mussel density and potential species replacement in different water types at different depths.

Bioaccumulation of metals and organic contaminants in dreissenid mussels for different water types and toxicological risks of (protected) water birds that use dreissenids as staple food.

Long term monitoring of effects of dreissenid mussel fouling on the health, survival and population viability of native unionids in various types of ecosystems.

The influence that Quagga mussel colonization has on recovery of aquatic macrophyte vegetation in eutrophicated water bodies.

Acknowledgements

We thank the Invasive Alien Species Team (Netherlands Food and Consumer Product Safety Authority of the Dutch Ministry of Economic Affairs, Agriculture and Innovation) for financial support of this study (project reference TRCPD/2010/3092). Ir. J. Wiebe Lammers and Dr. Ir. José H. Vos of the Invasive Alien Species Team delivered constructive comments. The authors also thank Bart Grutters, Martijn Schiphouwer, Yen Le Thanh, Aryan Ransijn, Saskia Smits and Michiel Verhofstad for help with field work, laboratory analyses or experiments, Marije Orbons for assistance with identification of macroinvertebrates, Martin Versteeg for delivering monitoring devices, Germa Verheggen for technical advises regarding water quality analyses and Peter Klok for delivering photos of Quagga mussels.

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Appendices

Appendix 1. Literature study search terms

Dreissena Tweekleppingen Uitheemse

Verspreiding Quaggamossel Exoten

Nederland Invasive Polymorpha

Abundantie Mossels Bugensis

Vreemde soorten Demographics Kolonisatie

Driehoeksmossel Plants Dynamics

Macroinvertebrates Age Vectors

Tolerance Prevention Unionid

Physiological Fouling Toxin

Tolerance Metal Botulinum

Control Bioaccumulation Macrophytes

Management Accumulation Parasites

Population Socio-economic Zebra

Quagga

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Appendix 2. Literature study search tools, information and data sources

Organisation name Web address

kenniscentrum voor integraal www.riza.nl waterbeheer

Directie Kennis en Innovatie (DKI) www.rijksoverheid.nl

waarneming.nl http://waarneming.nl/index.php

STOWA www.stowa.nl

Rijkswaterstaat www.rijkswaterstaat.nl

Stichting VeldOnderzoek Flora en http://www.voff.nl/ Fauna

Deltares http://publicwiki.deltares.nl/display/WIKI/Public+Wiki

DAISIE (European alien species www.europe-aliens.org/ information)

Global invasive species website www.issg.org/database/welcome/

European Invertebrate Survey http://www.naturalis.nl (EIS)

Werkgroep Exoten http://www.werkgroepexoten.nl

Atlasproject Nederlandse http://www.anemoon.org/anm Mollusken (ANM)

Nederlands soortenregister www.nederlandsesoorten.nl

Global biodiversity information http://data.gbif.org facility

nlbif biodiversiteitsportaal http://www.nlbif.nl

Helpdesk Water http://www.helpdeskwater.nl/

Antwerpse Koepel voor http://www.provant.be/leefomgeving/natuur_en_landschap/koepel_voor_natu Natuurstudie (ANKONA) urst/

UK Environment Agency www.environment-agency.gov.uk

US National Oceanic and www.habitat.noaa.gov Atmospheric Administration

US Army Corps of Engineers http://el.erdc.usace.army.mil/index.cfm

17th International Conference on http://www.icais.org/ Aquatic Invasive Species

104

Utah Division of Wildlife Resources http://wildlife.utah.gov/dwr/

Aquatic Nuisance Species Task http://www.anstaskforce.gov/default.php Force

US Bureau of Reclamation http://www.usbr.gov/

US Environmental Protection www.epa.gov/epahome Agency

The University of Texas Arlington http://dspace.uta.edu/

Meridian Initiative (2010) http://www.100thmeridian.org/

Database name Web address

Online public access catalogue www.kdc.kun.nl/adlib-opac.html (OPAC)

Web of science http://apps.isiknowledge.com

SCOPUS http://www.scopus.com/home.url

Dutch central catalogue / PiCarta / http://picarta.pica.nl online contents

Science.gov www.science.gov

Grey literature in the Netherlands http://picarta.pica.nl (GLIN)

Greynet http://www.greynet.org/greysourceindex.html

Opensigle http://opensigle.inist.fr/

Milieuliteratuurbestand (MLB) www.allesovermilieu.nl

Virtual Library Web address

BUBL link, Infomine, PSIgate http://bubl.ac.uk/, http://infomine.ucr.edu/, http://www.intute.ac.uk

Metasearch engine Web address

Oaister, Metacrawler, Scirus www.oaister.org, www.metacrawler.com, www.scirus.com

105

Appendix 3. Sampling locations

mussel

255

353

267

311

124

633

ensity ensity 1719

2268

per d

uagga Q

elative elative

relative relative

detailed detailed

Analysis

sampling

abundance

present

watercraft

non observed non

none observed none

Colonisation vectors vectors Colonisation

connected

Hydrological Hydrological

connectivity

disconnected

connected in winter connected

type

river

arina

marina

stream

channel

drainage drainage

major river major

major major

major river major

Water Water

309600

421800

419400

415700

41610

397600

414200

412900

414100

404800

404700

oordinates

Amersfoort Amersfoort

177000

153500

179700

189550

189500

19170

202000

193800

194200

196800

193800

198400

198300

198200

with with

Niers Niers

/ description

euse

r by ferry r by

Location

iver mouth iver

South of Eijsden South of

north of Alem ferry Alem of north

polder pumping station, Grave station, pumping polder

Middela

Cuijk by ferry Cuijk by

Plasmolen marina Plasmolen

marina at Well at marina

upstream of confluence confluence of upstream

Gennep

confluence

upstream of M upstream

Afferden

upstream of Eckeltsche Beek Eckeltsche of upstream

body

Meuse

Niers

Meuse

Water

River River

River Niers River

River River

Beek

Eckeltsche Eckeltsche

Beek

Eckeltsche Eckeltsche River M River

106

901 459

m per

mussel

density density

present

present Quagga Quagga

not present

gradient

Analysis

emperature emperature

elative abundance elative

detailed sampling detailed

elative abundance elative

relative abundance relative

present

watercraft

rowing boat rowing

none observed none

Colonisation vectors vectors Colonisation

watercraft (rowing boats) (rowing watercraft

connected

Hydrological Hydrological

connectivity

disconnected

connected in winter connected

seasonal connection seasonal

ake

anal

tream

tream tream

canal

ajor river ajor

major river major

Water type Water

(fishladder)

oxbow oxbow

floodplain lake floodplain

434200

434250

436500

434000

438100

42420

432400

432600

432800

43075

43030

43020

43030

43020

4297

42940

42930

4290

42880

4298

429700

431200

431100

429800

431200

430700

431400

430800

oordinates

Amersfoort Amersfoort

198750

198700

196000

198800

194400

18470

179400

179500

179400

18520

18570

18560

18570

1942

18870

18860

18870

1904

194200

192300

196900

196400

197300

199500

201400

Duits Duits

heetuin heetuin

Nijmegen

/ description

near

field

Duits Gemaal Duits

burg ferry burg

field

Location

ear Nederrijn confluence Nederrijn ear

ear Waalbrug in Nijmegen Waalbrug in ear

ear Waalbrug in Waalbrug in ear

ear Waalbrug in Nijmegen Waalbrug in ear

outh of Linge inlet Linge of outh

ownstream of Hollands of ownstream

Linge inlet Linge

Doorne

Zevenaar ferry Zevenaar

Hatert

Ewijk

Electrobel Nijmegen Electrobel

Gemaal

Hollands

Waal floodplain Waal

Ooij Ooij gro

Bisonbaai

flooded quarry pit quarry flooded

Kaliwaal

Kekerdom floodplain lake floodplain Kekerdom

Milligen floodplain lake floodplain Milligen

Milligen groinfield Milligen

body

Waalcanal

Waal

Water

canal

Pannerdens

canal

Pannerdens

canal

Pannerdens

canal

Pannerdens

canal

Pannerdens

River Waal River

Het Het Meer

Oude Waal Oude

River Waal River

River River

River Waal River

River Waal River River Waal River

107

449

142

295

114

per m per

density density

present

Quagga mussel Quagga

Analysis

elative abundance elative

detailed sampling detailed

elative abundance elative

relative abundance relative

present

watercraft

canoes canoes only

none observed none

Colonisation vectors vectors Colonisation

ted

passivedownstream dispersal of veligers mussel

connected

connec

connected

disconnected

ws a

Hydrological connectivity Hydrological

thatallo

river

lake

river

arbour

canal

harbour

major major

major river major

Water type Water

side channel side

568400

503750

436100

438700

395400

500400

473500

473400

472500

473300

463700

462800

460800

451600

446000

445800

44130

441300

441800

438700

438200

434250

oordinates

185900

211100

187800

188000

136300

200900

208100

208200

211000

216900

211500

214800

210200

204800

207900

199700

17340

176100

175600

192500

192600

177700

187100

198650

Amersfoort c Amersfoort

populations Quagga of mussel

/ description

Linge side of dam of side Linge

Location

Grou

Dalfsen

Elst

Arnhem

Tilburg

South of Zwolle South of

North of Deventer harbour of Deventer North

Deventer harbour Deventer

Deventer

Bathmen

Zutphen

Warnsveld

Zutphen

Dieren

Doesburg

Rheden Ferry Rheden

Wageningen harbour Wageningen

Schoutenwaard

Bakenhof side channel side Bakenhof

Bakenhof at Arnhem at Bakenhof

Lingebrug, Zetten Lingebrug,

Elst

inlet

body

Plas

canal

ssel

Water

Linge

defined as defined connection a to upstream

* *

Princes Margriet Kanaal Margriet Princes

River Vecht River

Aamsche Aamsche

plassen

Rijkerswoerdse

Wilhelmina canal Wilhelmina

River IJssel River

River I River

Schipbeek

Twente

River Berkel River

River IJssel River

Apeldoornsch canal Apeldoornsch

River IJssel River

River Nederrijn River

River Linge River

River Linge River River River

108

Appendix 4. Overview of equipment used during field sampling

Company name Equipment name Parameter measured

Radiometric Copenhagen, Titralab 80 pH Denmark

Hydrobios Appartebau Gmbh, Secchi Disc Turbidity Germany

Van Vugt Instrumentatie, TAD-micro flow meter Flow velocity Hilversum, the Netherlands

WTW Wissenschafttlich- Multi 340i / set Conductivity, temperature Technische Wekstatien, Weilheim, Germany

TFA-Dostmann GmbH & Co. KG, Maxima-Minima-Thermometer Temperature Germany

109

Appendix 5. Sizes of sampled dreissenids in the river Meuse

35 Dreissena polymorpha

30 Dreissena bugensis

10 Number of individualsof Number 5

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 Size (mm)

Figure A5.1. Population structure of sampled dreissenid populations in the river Meuse at Eckertsedijk near Afferden (MaSii).

18 Dreissena polymorpha 16 Dreissena bugensis

Number ofNumberindividuals 4

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Size (mm)

Figure A5.2. Population structure of sampled dreissenid populations in the river Meuse near Milsbeek at the junction with the river Niers (MaSi).

110

50 Dreissena polymorpha 45 Dreissena bugensis

Number of individualsof Number 15

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Size (mm)

Figure A5.3. Population structure of sampled dreissenid populations at the river Meuse at Middelaar (MaS1).

35 Dreissena polymorpha Dreissena bugensis 30

Number of individualsof Number 10

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 Size (mm)

Figure A5.4. Population structure of sampled dreissenid populations at the river Meuse at the polder pumping station at Grave (MaW2).

111

Appendix 6. Mean tissue metal concentrations of dreissenid species

Table A6.1: Tissue metal concentrations of Zebra mussel (mg kg-1).

Sampling Location Data As Cd Cu Hg Ni Pb Se Zn Source period Yen et al. River Rhine Mean nd 1.2 16.6 nd 12.7 7.2 5.3 123.8 2010 (20110 Yen et al. River Meuse Mean nd 5.1 33.9 nd 41 8.7 5.3 269.5 2010 (2011) Matthews River Waal Mean 3.2 1.5 30.4 0.1 14.8 2.5 7.4 108.6 2008 (2009)

Ransijn Lake Markermeer Mean 7.4 2.2 21.5 0.6 38.4 0.9 5.0 75.9 Nov-09 (2011)

Ransijn Lake Markermeer Mean 7.6 2.4 21.2 0.1 38.1 0.7 6.2 92.0 Jul-09 (2011) Ransijn Lake IJsselmeer Mean 4.7 1.0 21.6 0.1 28.1 1.0 3.8 86.7 Nov-09 (2011) Ransijn Lake IJsselmeer Mean 4.7 1.1 22.6 0.0 24.5 1.8 3.6 117.5 Jul-09 (2011) nd: Analysis not undertaken

-1 Table A6.2: Tissue metal concentrations of Quagga mussel (mg kg ).

Sampling Location Data As Cd Cu Hg Ni Pb Se Zn Source period Yen et al. River Rhine Mean nd 1.1 17.9 nd 12.0 6.8 5.7 114.8 2010 (2011) Yen et al. River Meuse Mean nd 5.0 17.9 nd 18.1 8.2 7.0 170.8 2010 (2011) Single Matthews River Waal 4.3 1.9 18.5 0.2 11.2 5.1 7.1 105.7 2008 replicate (2009) Lake Ransijn Mean 7.0 1.1 14 0.3 14.6 2.2 5.1 68.9 Nov-09 Markermeer (2011) Lake Ransijn Mean 7.0 1.8 14.6 0.0 12.8 1.4 5.3 81.8 Jul-09 Markermeer (2011) Ransijn Lake IJsselmeer Mean 5.0 0.9 11.8 0.0 13.5 1.6 3.9 63.8 Nov-09 (2011) Ransijn Lake IJsselmeer Mean 4.9 1.0 11.7 0.0 11.9 2.5 3.2 64.1 Jul-09 (2011) nd: Analysis not undertaken

112

Appendix 7. Average current velocity of the Rhine river branches

Flow velocity in main channel River branch (cm s-1)

Lower Rhine 70-200

River Waal 70-200

River IJssel 30-110

River Nederrijn / Lek <10-110

(adapted from: Van den Brink et al.,1993).

113

Appendix 8. Macroinvertebrate species composition at detailed sampling sites

119

103

273

252

155

125

Grave, the River Meus River the Grave,

Sampling points Sampling

M4: Middelaar, the river Meuse river the Middelaar, M4:

P5: Polder pumping station, pumping P5: Polder

125

112

Nederrijn

iver iver

Non

species

indigenous indigenous

sp.

Total abundance

sp.

B5: Bakenhof, Arnhem, the the Arnhem, B5: Bakenhof,

S5: Schoutenwaard, Wageningen, the river Nederrijn Nederrijn the Wageningen,river S5: Schoutenwaard,

E5: Ewijkseplaat, Ewijk, the river Waal river the Ewijk, E5: Ewijkseplaat,

tigrinus

villosus

ischnus

nymphs

Species

trichiatus

robustum

Jaera istri Jaera

Micronecta Micronecta

Gammarus Gammarus

curvispinum

Beetle Larva

Chironomidae

Gammarus

Chelicorophium Chelicorophium

Ancylus fluviatilis Ancylus

Dikerogammarus

Dikerogammarus Dikerogammarus

Echinogammarus Echinogammarus Echinogammarus Echinogammarus

114

Appendix 9. Fluid detachment parameter of Quagga mussels

Fluid detachment parameter (DP) for natural, polymeric and metallic materials of differing surface roughness (adapted from Ackerman et al., 1996).

Surface Material Number of mussels DP.10-3 Mussel length roughness Standard Mean Standard Remaining Detached error Mean (mm) (Pa.m2) error (mm) (Pa.m2)

Natural substances Concrete Smooth 1 26 7.4 0.5 9.2 0.2 Rough 1 30 6.3 0.5 8.9 0.2 Wood Smooth 1 33 6.6 0.5 9.1 0.2 Rock Rough 11 55 8.9 0.9 10.4 0.4

Polymeric substances CT-E Smooth 0 23 7.5 0.7 11.2 0.2 PMMA Smooth 1 53 2.5 0.3 7.7 0.2 PTFE Smooth 0 23 1.9 0.2 7.7 0.3 Medium 0 12 5.7 0.9 10.7 0.6 Rough 1 23 6.2 0.7 11.7 0.3 PVC Smooth 0 58 5.6 0.5 8.7 0.3 Medium 4 29 7.8 0.7 10.4 0.4 Rough 0 23 5.8 0.8 8.9 0.4

Metallic substances

Aluminium Smooth 1 28 4.2 0.5 8.6 0.2 Steel Smooth 2 27 10.5 0.9 11.4 0.3 Medium 2 18 11.0 1.0 12.4 0.3 Rough 2 16 10.8 0.9 11.1 0.3 Stainless Smooth 2 73 4.2 0.4 7.9 0.2 steel Medium 0 26 6.9 0.6 9.4 0.2 Rough 2 29 7.3 0.7 10.6 0.4

115

Appendix 10. Treatments methods for controlling dreissenid fouling

Table A10.1: Non-chemical treatments methods (U.S. Bureau of Reclamation, 2008).

Method Life Stage Effectiveness Duration of Treatment Notes Must isolate population; Useful Oxygen Reservoir management starvation All 2 weeks + at 0 mg l-1 scheme if hypolimnion can be

increased Juveniles 2 days at 0 oC Freezing 100% 5-7 h at – 1.5 oC Must dewater system Adults Under 2 h at -10 oC Juveniles Immediate at 36 oC Must dewater system for Desiccation 100% 5 h at 32 oC Adults several days 21 days at 25 oC Veligers in seconds at May affect other species, 10-380 kHz Cavitation All 100% reduced success in high flows, Juveniles in min needs power source Adults in a few hours Veligers in seconds at May impact other species, Ultrasound All 100% 39-41 kHz needs power source Adults in 19-24 h Veligers, Intermittent at 200 Hz Structural integrity may be Vibration 100% juveniles and 10-100 kHz threatened Juveniles – 4 h Lethal to many species, UV radiation All 100% effectiveness limited by Adults - continuous turbidity and suspended solids Benthic mats Juveniles, Initial tests promising for (disposable Up to 99% 9 weeks adults limited infestations substrates) Bacterial toxin, Low toxicity to other Pseudomona organisms, few treatments All 95% 6 h fluorescens needed, not yet available in (experimental) commercial quantities. Low frequency 4 to 12 min at 20 Hz – Juveniles Inhibits settling Not lethal, needs power source sound 20 kHz Low voltage Prevents Immediate results at 8 Adults Not lethal, needs power source electricity settling volt AC Plasma pulse Juveniles, Prevents intermittent high Not lethal, private technology technology adults settling energy pulses Manual Juveniles removal (scraping, Variable N/A Adults mechanical filtration) Lethal to Electric field Juveniles, juveniles May affect other species, Seconds pulse adults Inhibits adult needs power source settling Harvest of potential predatory Predation All Low Continuous species must be limited

116

Table A10.1: Chemical treatments methods Dreissena (U.S. Bureau of Reclamation, 2008).

Duration of Method Life Stage Effectiveness Notes Treatment Non-oxidising chemicals Copper ions Veligers 100% 24 h at 5 mg l-1 Lethal to other aquatic species Potassium ions All 100% Less than 10 mg l-1 Lethal to other (KOH) aquatic species Potassium ions All 100% Continuous at 160- Lethal to other -1 (KH2PO4) 640 mg l aquatic species Potassium salts Juveniles, adults Prevents 50 mg l-1 Lethal to other (KCl) settlement mussel species, All 50% 48 h at 150 mg l-1 non-toxic to fish at 95-100 % 3 weeks at 95-115 required dose rate mg l-1 Chloride salts Veligers, juveniles 95-100% 6 h at 10,000- Low cost, low 20,000 mg l-1 environmental Impacts, very high dosage rates Copper sulphate All 55% 5 h 300 mg l-1 at Lethal to other 22.5 oC aquatic species 40% 5 h 100 mg l-1 at 22.5 oC 50% 48 h 2-2.5 mg l-1 at 17 oC Oxidising chemicals Chlorine Veligers 100% 0.25-5 mg l-1 in 1 to Lethal many 9 days aquatic species All 90% 2.0 mg l-1 continuous Adults 95% 0.3 mg l-1 in 14-21 days Adults 75% 0.5 mg l-1 in 7 days Chlorine dioxide Veligers 100% 0.5 mg l-1 24 h Most successful on ClO2 veligers Chloramine Veligers 100% 1.2 mg l-1 24 h Less toxic to other 95% 1.5 mg l-1 aquatic life than continuous chlorine Hydrogen peroxide Veligers, juveniles 100% 6 hours High dosage rates required. Lethal to other aquatic species Ozone All 100% Veligers in 5 h at Lethal to other 0.5 mg l-1; Adults in aquatic species 7 days at 0.5 mg l-1 Potassium All 90-100% 2.0 mg l-1 for 48 h Must have high permanganate continuous dosage, lethal to other species

117

Appendix 11. Example of a protocol for watercraft decontamination.

118

119

120

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