Zebra Mussel): the Importance of Long-Term Datasets in Invasion Ecology

Research article

Early life stages of Dreissena polymorpha (zebra mussel): the importance of long-term datasets in invasion ecology

Frances Lucy School of Science, Institute of Technology of Sligo, Ballinode, Sligo, Ireland E-mail: [email protected]

Received 12 July 2006; accepted in revised form 1 September 2006

Abstract

The early life stages of Dreissena polymorpha were studied in Lough Key, Co. Roscommon, Ireland during the reproductive season, 1998-2003. This involved weekly sampling of larval/veliger density, size distributions and settlement density. Low larval and adult densities of Dreissena in 1998 indicated that this was the first year of significant reproduction in Lough Key. Variation existed in seasonal larval densities, larval size distributions and juvenile settlement patterns among sampling weeks, years and monitoring sites from 1998 to 2003. In the early years of invasion (1998-2000) annual variations were observed in larval density and juvenile settlement. Increasing levels of larval density and settlement from 1998 to 2000 were typical for the early exponential growth phase of Dreissena invasions. The high level of successful recruitment in those years was evident from the exponential increase of the adult zebra mussel population. In subsequent years, these differences were likely related to environmental variations in summer water temperatures and food availability for veligers. In 2001, settlement estimates were extremely low relative to the larval densities present. Prolonged warm water temperatures in summer 2003, resulted in a long reproductive season and also high settlement rates. The variation between annual datasets observed in this study, implies that long term studies of the early life stages of Dreissena polymorpha is required to monitor the dynamics of this species within lake ecosystems.

Key words: Dreissena polymorpha, larvae, juvenile, Lough Key, recruitment, settlement, veliger

It is a fundamental ecological principle that both successful reproduction and the survival of Introduction sufficient early life stages to maturity are necessary for the success of any species’ Zebra mussels are thought to have colonised population. Dreissena polymorpha shares Ireland about 1993/1994, arriving as fouling on characteristics of many successful invasive the hulls of leisure craft from Britain (Minchin et species: rapid growth, prolific reproduction at an al. 2005, Pollux et al. 2003). Colonisation of early age (0-1+) and a relatively short life span. Lough Key is believed to have taken place in This usually provides the potential for rapid 1996 (Lucy 2005). Zebra mussel surveys have exponential growth of zebra mussel populations taken place in Lough Key, since 1998, when adult within a waterbody (Ehrlich 1989, McMahon zebra mussels were initially found. 1992, Nichols 1996).

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Researching the dynamics of early Dreissena Materials and methods life stages involved sampling larval/veliger densities, measuring larval size distributions and Site description estimating settlement of juveniles (plantigrade stage). This was carried out annually in Lough These studies have involved research on veliger Key from 1998 to 2003. The aim was to provide and juvenile zebra mussels (density and size), information on larval development within the adult zebra mussels (density and biomass) and plankton and also survival to a settled juvenile also on the nutrient status of the lake (Lucy and stage throughout the sampling seasons. Annual Sullivan 2001, Sullivan et al. 2003, Lucy 2005, datasets were interrogated to determine the Lucy et al. 2005). Lough Key (9km2) is located in varying dynamics of early life stages in Lough the upper Shannon River catchment (Graczyk et Key over a six year period (1998-2003). al. 2004) at an altitude of 45m O.D., and is The commencement of research in 1998, when relatively square in shape with a maximum length populations were still in their early invasive stage, of 4.2km and a maximum width of 4km (Figure provided an opportunity to monitor the exponen- 1). It has an estimated volume of 45.97 m3 x 106 tial growth of zebra mussels in Lough Key at both and a maximum depth of 23.5m (Toner 1979). larval and adult stages in the lake population. The lake is relatively shallow with a mean depth Continued studies until 2003 also provided data of 4.5m (Lucy et al. 2005). There are 13 islands on the annual status of Dreissena polymorpha in on the lake. Most near shore areas of the lake have Lough Key. a stoney substrate.

Figure 1. Map of Lough Key

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Sampling methods position from a jetty at Site D. The settlement plates were suspended from a concrete anchor Sampling of early zebra mussel life stages weight, which held the plates firmly in mid-water (larvae/veligers and settled juveniles) has been (3m depth approx). All plates were conditioned largely adapted from a monitoring programme for one week to allow a bio-film to build up, thus designed by Marsden (1992). The scheduled encouraging settlement. On each sampling date sampling programme was designed to maximize beginning early/mid June either the bottom or the sampling during the summer season. Weekly middle plate was changed on a two-week rotation. sampling was generally implemented from July to Once recovered, the plates were placed in a September. Weeks for summer months are sectioned sample container and then examined assigned numbers, weeks 1- 4 for each month, in using a microscope for the presence of newly the format July week 1. During 2001-2003 settled juveniles. These were clearly visible on the 2 occasional sampling was also carried out earlier surface of the plates. The mean of 30 x 1 cm and later in the year. quadrats was obtained for each plate and an 2 A temperature datalogger (Vemco minilog estimated settlement density/m was extrapolated V3.04) was deployed at Site D to record from this data. A new settlement plate was temperatures every four hours between 2001 and replaced each time a plate was recovered. 2003. Temperature was also recorded with an alcohol thermometer at Site A and Site D at each Statistical analysis monitoring (1998-2003). Three-metre vertical tows were carried out at Mean veliger densities were calculated from data four monitoring sites (A-D) in 1998 and 1999 and for Sites A-D (1998-2003). It was considered at five sites (A-E) from 2000-2003 (Figure 1). A more representative to take mean values for all 64 µm mesh plankton net with a 30cm diameter sites rather than site-specific ones, due to the opening was used for veliger sampling, allowing known patchy distribution of larvae (Lucy 2005). collection of all veligers >70 µm. Size distribution results were compared For the monitoring programme each sample was statistically using descriptive statistics. As examined under a high magnification (80-100x) datasets were not normally distributed and the (Olympus CX-41), using cross polarized light variances were heterogeneous (Levene statistic, (Johnson 1995) using one-ml sub-samples in a p<0.05), Kruskal-Wallis and post-hoc Mann- Sedwick-Rafter Counting cell. Three one-ml sub- Whitney test tests (p<0.05) were applied to samples were counted and the veliger density per compare sample distributions. ml of concentrated sample calculated from the Statistical analysis determined that the size mean as below: distributions of veligers were not significantly different (Mann-Whitney test, P>0.05) at sampl- Number of veligers/ml x 25a b ing sites within sampling weeks. Weekly datasets Volume of Sample from different sites were therefore pooled for a = Volume in 25ml tube analysis to give a larger sample size for each week b = 3 x 3.14 x (0.3)2 = length of tow x π x radius (>250). Samples taken in consecutive weeks were of net mouth2 = 848L also analysed to determine whether they varied The microscope was fitted with an optical with regard to size distribution (P<0.05). Where micrometer and size distributions of veligers from significant differences were found, post-hoc tests Sites B, C and E were measured to the nearest 10 were carried out to determine which paired µm. Veliger density and size distribu-tions were samples were significantly different (P<0.05). The then analysed (Ni Chonmhara 1999, Commons percentage of veligers greater than 200µm/sample 2000, Duggan 2001, Marshall 2002, O’Mahony was calculated for each sample week (1998-2003) 2003, Lohan 2004). A mean density value was to determine the proportion of veligers close to obtained for each sample week from the different settlement. lake sites. Settlement analysis was based on cumulative Settled juveniles were sampled using 15x15 cm means for Sites A to D. Correlation analysis grey PVC plates with three plates deployed in (Pearson’s correlation coeffecient, significance series at each site as in Lucy and Sullivan (2001). level P<0.05) was used to compare the following: The rope was tied at the top to a navigational • Veliger density (week n) vs settlement buoy at monitoring sites A, B, C and E and held in (following week, n+1)

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• Percentage of veligers > 200µm (week n) vs settlement (week n+1) The statistical package SPSS 11 was used to carry out the various statistical analyses (Howit and Cramer 2003).

Results

Larval Densities in Lough Key

In terms of seasonal appearance, zebra mussel larvae were detected in the plankton as early as February 2000 (7.2oC) and March, 1999 (11oC) These were probably overwintering larvae as observed by Kirpichenko (1971). The first definite seasonal appearance of larvae occurred in May corresponding with site water temperatures greater than 12.5oC. Water temperature however, was generally in excess of 15oC during the reproductive season. Larval densities from 1998- 2003 are shown with associated water temperatures (Figure 2). The annual start of significant spawning in the lake was early July, with larvae appearing in samples until the beginning to the middle of October. Peak annual spawning was typically from June week 4 to August week 4. Larval densities (veligers/L) showed seasonal variation between years. In 1998 spawning was not detected at any site until July week 4. In 1999 and 2000 the spawning season was longer, particularly in 2000 when significant densities were recorded from June week 4. The spawning season was particularly long in 2003, with larvae detected from the second week in June and with significant numbers of larvae still present in the plankton in mid September 2003. Individual recorded peak densities increased yearly, from 1998 to 2003, with the exception of a decrease in 2001 (Figure 3). There appeared to be no relationship between water temperatures and larval densities in 1998 or 1999. In 2000 the highest larval density occurred the week following peak water temperatures. The maximum larval density coincided with peak temperatures in both 2001 and 2003 and appeared to be also related to temperature rises in 2002 (Figure 2). At each site larval numbers decreased Figure 2. Mean veligers/L (1998-2003) with temperature oC during autumn period, at the end of the spawning period and in October were detected only in low numbers.

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Larval Size Distributions

Statistical analysis determined that there was often a significant difference between size distributions in consecutive weeks in 2002 and 2003 (Table 1). This was rarely observed in 2001. Zebra mussel larval size distribution in 2003 was detailed (Figure 4). Small D veligers (70-80µm) were not well represented in the majority of samples. In most sampling weeks, veligers >260µm were not generally present in the plankton. Larger individuals were occasionally Figure 3. Maximum veligers/L 1998-2003 recovered, including one at 840µm sampled in September 2002.

Figure 4. Size distribution of zebra mussel veligers, July week 2 - September week 2, 2003

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Table 1. Significant difference (Mann-Whitney test, p<0.05) The percentage of veligers >200µm (Sites A between veliger size distributions in consecutive weeks and B combined) is given in Table 2. In general, (2001-2003) the proportion of larger veligers increased from Week 2001 2002 2003 July week 4 to August week 4, with an elevated July week 1 and July week 2 nd ns * percentage also occurring during the first two July week 2 and July week 3 ns ns * weeks of September in 1998 and 2002. July week 3 and July week 4 * ns ns July week 4 and August week 1 * ns * Settlement August week 1 and August week 2 * * * Cumulative settlement during the spawning August week 2 and August week season (1998-2003) was estimated (Figure 5). 3 ns * ns Annually, the highest settlement occurred during August week 3 and August week 4 ns * * the entire month of August (weeks 1 to 4). The August week 4 and September low settlement in 1998 was in the early invasive week 1 ns * * stages of Dreissena colonisation in Lough Key September week 1 and (Lucy and Sullivan 2001). The high settlement in September week 2 nd ns * 1999 and 2000 coincided with the exponential * = significantly different (p < 0.05); ns = not significantly increase in the lake’s dreissenid population (Lucy different; nd = no data et al. 2005a, b). Overall settlement was very poor

Table 2. Percentage of veligers > 200 µm in plankton samples, 1998-2003

% > July July July July Aug Aug Aug Aug Sep Sep 200 µm week 1 week 2 week 3 week 4 week 1 week 2 week 3 week 4 week 1 week 2 1998 nd nd nd 4.2 1.5 1.5 10.2 27.5 44.3 51.1 1999 nd nd nd 3.8 1.4 76.8 85 5.4 14.2 2.3 2000 0.3 1.5 4.7 7.9 11.2 12 10.1 1.1 nd nd 2001 9.1 15.1 0 2.5 19.7 2.9 12.5 19.7 nd nd 2002 0 1.2 6.3 8 26.9 30.5 14 6.6 18.4 27.3 2003 1 1.3 2.3 10.3 11.3 16.7 7 1 3.3 4.3 nd = no data

in 2002 (maximum, 4,000/m2, Site B, August week 2). Peak settlement in 2001 and 2002 occurred two weeks after peak larval density. In 2003, relative settlement was high and appeared to occur only one week after peak larval densities. Cumulative settlement vs mean larval density was compared for the years 2001, 2002, 2003 (Figure 6). Overall settlement was very poor in 2002 (maximum, 4,000/m2, Site B, August week 2). Peak settlement in 2001 and 2002 occurred two weeks after peak larval density. In 2003, relative settlement was high and appeared to occur only one week after peak larval densities. Statistical analysis showed larval densities (week n) vs settlement (week n +1) to be positively correlated in 1999 (r = 0.76, p = 0.017) and 2000 (r = 0.79, p = 0.06) and highly positively correlated in 2003

Figure 5. Cumulative zebra mussel juvenile settlement, (r = 0.96, p = <0.001). The proportion of veligers 1998 – 2003 > 200µm (week n) was highly correlated with

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settlement (week n+1) in 2003 (r=0.85, p=0.002). studies, as the level at which larvae were first No correlation existed for other sampling years. observed (Kirpichenko 1964, Einsle 1973, Stanczykowska 1977, Karatayev et al. 1998). Although occasional veligers were recorded in May at temperatures of 12.5oC to 13oC, these may have spawned from adult mussels in the littoral zone where temperatures had reached the 15oC required spawning threshold. Temperature readings indicate that in general the temperature during summer months ranged between 15 and 18oC. The higher temperatures recorded during the 2003 season resulted from prolonged warm weather during July and August.

Veliger Density The length of the spawning season (June– September) was typical for zebra mussel infested lakes in FSU, Europe and North America (Sprung 1989). The presence of occasional large postveligers outside the normal spawning season may have resulted either from prolonged duration in the plankton, with delayed development due to low temperature (Lewandowski 1982) or more likely from resuspension from the substrate as reported by Martel (1993). The latter could easily occur following stormy weather incidents, where settled juveniles could get washed off stones in the littoral zone, becoming resuspended in the plankton. Veliger densities in this study fall within the Figure 6. Settlement vs veligers/L (cumulative values) wide range reported in the literature (Kirpi- 2001-2003. chenko 1964, Lewandowski 1982b, Haag and Garton 1992, Nalepa et al. 1995). Results from Lough Key indicated that peak densities were Discussion found at three separate sites in summers 2000- 2004. Overall results from 1998 to 2000 seem to Temperature indicate that veliger densities and length of The temperate Irish climate is ideal for Dreissena spawning season are influenced by three main polymorpha as lakes rarely freeze in winter factors; parent population size; maturity of parent (species lower lethal temperature 0oC) and never population and temperature of lake water. It is reach the upper temperature limits of greater than interesting to note that even though the or equal to 32oC (Karatayev et al. 1998). The temperature range is small in terms of other maximum temperature range recorded during the international studies carried out in continental survey was 3.1oC to 22.4oC (2002-2003). climates, it still appears to have an impact on Increasing water temperatures during spring has spawning patterns. been widely reported as the primary Nineteen ninety eight was considered the first environmental factor in triggering the timing of year of significant spawning in Lough Key (Lucy reproduction in zebra mussels. Both temperature and Sullivan 2001). Overall densities were very and food availability can influence the course of low in that year, as could be expected from a the annual gametogenetic cycle, the rate of oocyte small parent population comprised of mainly 1+ development, gonad size and the onset of individuals. Figure 7 shows peak veliger density spawning (Borcherding 1995). Water temperatu- versus percentage adult zebra mussel cover on res of 15oC have been cited in many European stone indicating the exponential increase in the

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population between 1998 and 2001. In 1998 the early September, with larvae well represented late start of the spawning season may relate to the until the end of sampling in September week 3. reproductive development of the 1+ parent There may be several reasons why the generation, many of which may have taken until spawning cycle is prolonged over the summer and August to reach sexual maturity. early autumn. Variation in spawning patterns has been reported in a number of comparative studies (Gist et al. 1997). a) In spawning, each zebra mussel in principle is able to release gametes over a period of six to eight weeks (Walz 1973, Borcherding 1991). So the same individuals may be spawning sequentially, which could result in bimodal patterns in size distribution. b) Separate age cohorts of zebra mussels may develop at different rates and smaller (1+) individuals may spawn later in the season than older (2+) zebra mussels. One-year-old zebra mussels are known to spawn in Irish waters (Juhel et al. 2003) Figure 7. Zebra mussel adult density vs veligers/L c) Similar age cohorts may develop at

different rates and spawn over the entire summer

season. Smaller 1+ individuals become mature In 1999 veliger densities were relatively and spawn later in the season. In one study uniform between July week 2 and August week 4; Borcherding (1991) observed this phenomenon in although spawning probably started before this zebra mussels and similar results have also been but was not detected as it was outside the derived for marine species. sampling regime. The constant spawning level probably reflects the presence of a large Veliger Size Distribution proportion of 1+ individuals. Juhel et al. (2003) reported non-synchronous development of gonads Seasonal size distribution patterns actually in Irish zebra mussels, resulting in prolonged provide more useful information than larval spawning over a number of weeks. densities, because it is possible to trace larval size The early peak in 2000 (June week 4), patterns through to settlement stage over the sum- probably reflected the high water temperature mer period. This provides a bridge in information present at that time (19oC). This temperature is between the veliger/larval and settlement stages. relatively unusual at that early stage of the High proportions of small veligers (less than summer. The early peak also indicated that mature 110µm) were present early in each season with zebra mussels were present. By 2000 there was a corresponding low numbers of larger veligers, well-established cohort of 2+ zebra mussels and corresponding with the start of the spawning these would certainly have been ready to season. In both 2002 and 2003 mean size reproduce in addition to early maturing 1+ decreased in August week four due to a pulse in individuals. Peak larval density that year (July spawning increasing the proportion of small week 4) succeeded the second week of peak veligers (less than 110µm). This was particularly temperature in that year. Both these events apparent in 2003, where the mean size was only indicate how important temperature is as a trigger 96.6µm (Figure 4). The week of highest larval to mass spawning. Temperature effects may be density was two weeks earlier in August week 2 considered direct, with growth of adult mussels of 2003, which recorded the greatest size range of occurring when temperatures reach 10-12oC veligers (80-290µm). This suggests that the (Mackie 1991, Jantz and Neumann 1992, highest densities sampled represent the maximal Karatayev et al. 2006), or indirect due to spread in larval development resulting from increased availability of food (Mantecca et al. continual spawning rather than from peaks 2003). Larval peaks in 2002 and 2003 were achieved from single spawning incidents. closely related to maximal water temperatures. In Seasonal reduction in peak densities represent 2003 the continued high water temperatures in both increased rate of settlement (as in 2003) and late summer resulted in increased densities in a reduction in overall spawning.

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As statistical analysis showed, there was often that settlement takes place generally between 200 variation in size distributions between different and 260µm. sequential weeks during the sampling season, particularly from August onwards. This would appear to indicate that veligers were growing and Settlement settling, with more appearing at the smaller cohorts of the range, following new spawning Settlement rates reflect the survival of veligers incidents. The increase in the proportion of larger through the postveliger stage to the settled veligers as the season progressed indicated the juvenile. Following mortality at the trochophore development of veligers from the D-shaped stage to D-stage (Sprung, 1989), and from the D stage to larger pediveligers. to the umbonal stage (Stoeckel et al. 2004), The majority of veligers measured in samples studies indicate that larval mortality can also over the three-year period were between 100 and occur late in the cycle during metamorphosis and 150 µm (mainly umbonate). This may relate to settlement (Stanczykowska 1977, Lewandowski early settlement, dispersal or is more likely due to 1982a). Given that the size range of settled high mortality rates prior to metamorphosis into juveniles on plates varied from 200-400µm, it is the juvenile (Sprung 1989). Stoeckel et al. (2004) probable that the low proportion of larger veligers found highest larval mortality during the in the plankton reflected a combination of both transition from D stage to umbonal stage, early settlement and mortality. Mortality (range supporting the suggestion of a developmental 20-100%) could be due to a number of factors bottleneck as found in previous field studies such as water turbulences (Rehmann et al. 2003), (Schneider et al. 2003). It may also relate to predation by fish (Molloy et al. 1997), filtering by variation in size of same-aged larvae, which have copepods or by adult Dreissena (MacIsaac et al. been found to differ by as much as 120μm 1991), bacterial infection, egg quality or (Stoeckel et al. 2004). starvation (Sprung 1989). The presence of significant numbers of larvae Settlement plate data did provide some in late September 2003 was a new recording event indication of overall survival of veligers to the for Lough Key and a definite new peak in veliger settlement stage during each sampling season density at that time was probably related to the (1998-2003). Size distribution analysis of adults high water temperatures during the summer. This from stoney substrate in the years consecutive to increase could easily be explained by factors (a) settlement also provided information on or (c) above. There is no doubt that the spawning settlement rates and survival to the 1+ stage (Lucy season was prolonged in 2003. Theoretically, if 2005). temperatures were maintained above 15oC, It is not possible to determine exactly how long spawning would continue indefinitely as more veligers remain in the plankton due to a number of zebra mussels matured and began to reproduce. reasons: Warmer Irish summers may become a future • Spawning is ongoing throughout the consequence of global warming, impacting on the summer, providing a number of cohorts. reproductive cycle of Dreissena. Development rate is also known to differ within The strong correlation between seasonal veliger cohorts (Sprung 1989). This results in size density and the percentage of veligers greater overlap, which complicates exact estimation of than 200µm in 2003 also showed that the higher cohort settlement. densities reflected the presence of a large size • The data in this study suggest that range of veligers, some as great as 290µm. The postveligers settle at different sizes as recorded in correlation could also indicate increased survival the literature (Ackerman et al. 1994, Nichols of larvae or shorter development time due to 1996). increased water temperatures. Larvae appearing in • There were a low number of veligers samples at the beginning to the middle of October greater than 200µm in most larval samples and of sampling years were usually larger (>200um) also a high variation in the sample proportion of indicating that the spawning season was over for these ‘close-to-settlement’ veligers. the year. Data from settlement plates indicate that • Veligers were already present in the postveligers in Lough Key settled from 200µm plankton when seasonal sampling began each upwards. Veligers larger that 200µm were, summer. It was not possible therefore to gauge however, well represented in samples, indicating time of first seasonal settlement.

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The datasets and correlation analysis ment can be defined as the transfer from the (settlement vs veliger density; settlement vs pelagic phase to the benthic, recruitment shows veligers greater than 200µm) did, however, settlement combined with post-settlement definitely indicate that a development cycle mortality. The increase in adult zebra mussel exists. Most veligers were greater than or equal to densities in Lough Key in 1999 and 2000 100µm in weeks of peak density and would be indicates that recruitment was high in 1998 and well into their first week of life, according to 1999. Even though veliger densities continued to growth rate of 4µm/day from a trochophore larva increase in 2001 and 2003, the phenomenon of (70µm) (Sprung 1989, Kern et al. 1994). By widespread settlement on various substrates noted combining this information with the size distribu- above was not noted from 2001 onwards, tion analysis in Lough Key, a two to three-week suggesting lower overall recruitment. It would development time for 2001 and 2002, and a one to seem likely that the overall observed reduction in two-week development time for 2003 can be settlement was due to lack of food resource for estimated. The amount of time required for larval larvae in the plankton as they depend on food development varies inversely with temperature particles (phytoplankton, Cyanobacteria, bacteria (Nichols 1996). Higher water temperatures may and detritus) of between 1-4µm and may starve therefore have resulted in a shorter development when phytoplankton is dominated by larger or time for 2003 as noted in another study by smaller algal species (Sprung 1989). Borcherding (1991). The high settlement rate in 2003 may have Conclusions been due to a decrease in development time related to the high water temperatures (degree-day Early life stage monitoring is often used to detect related), which lead to an increased survival rate. the presence of zebra mussels in waterways and in Faster development would decrease the opportu- such instances is used as a short term measure. nities for predation, as larvae would be present in This Lough Key study shows the variation in the water column for a shorter length of time. The larval density, size distributions and settlement higher temperatures in 2003 also resulted in an over a six year period from the early invasive increase in productivity (food availability) which stages through the exponential rise in the zebra would also give higher settlement. The two to mussel population. Future changes may occur due four-week development time concurs with Sprung to lake ecosystem factors or due to external (1989) but estimates vary within the literature environmental pressures, e.g. global warming. with some as high as five weeks (Walz 1973). With the increasing development of compute- Some European studies show zebra mussel larvae rized ecosystem modeling, it is important that present in the plankton for not more than ten days long term variation be taken into account rather (Kachanova 1961, Hilbricht-Ilkowska and than using single annual datasets. This variation Stanczkowska 1969, Lvova 1977 and 1980). can only be measured by long term monitoring as Recruitment on settlement plates in 2002 was exemplified by this research. poorer than in any other year. Zero + individuals were nevertheless well represented as the first age Acknowledgements cohort in adult samples taken in early 2003 (Lucy 2005). This highlights the fact that only a very Thanks to my students at the Institute of small proportion of zebra mussels (2 settled Technology, Sligo: Ms Elaine Ni Chonmhara, Mr juveniles out of 10,000s of veligers produced) Enda Commons, Ms Sharon Duggan, Ms Audrey need to survive to juvenile stage to maintain their Marshall, Ms Karen O’ Mahony and Mr Justin numbers in the lake. These inconsistencies in the Lohan for processing the veliger samples for this abundance of developing life stages and in research. Thanks to Monica Sullivan and Dan successful recruitment are consistent with other Minchin for assistance with field work. I also studies (Haag and Garton 1992, Doka 1994, wish to acknowledge The Irish Environmental Nalepa 1995). Protection Agency for provided funding for most In the early years of invasion (1998-2000), of this study (NDP project 2000-MS-5-M1). during the exponential growth phase, extensive Grateful thanks also to Mr. Peter Walsh for all his settlement was noted on aquatic plants, on buoy help steering me around Lough Key since 1998. I chains to a depth of 7.5m and also on the ropes would also like to thank DB Conn for reviewing used for attaching settlement plates. While settle- an earlier version of this research. Finally I would

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like to acknowledge Alexander Karatayev for Hunter RD and Bailey JF (1992) Dreissena polymorpha reviewing this manuscript. (zebra mussel): colonisation of soft substrata and some effects on Unionid bivalves. Nautilus 106: 60-67 Jantz B and Neuman D (1992) Shell growth and population References dynamics of Dreissena polymorpha in the River Rhine. In: Neumann, D and Jenner, HA (eds) The zebra mussel Ackerman JD, Blair S, Nichols SJ and Claudi R (1994) A Dreissena polymorpha: Ecology, biological monitoring review of the early life history of zebra mussels and first applications in the water quality management. (Dreissena polymorpha): comparisons with marine Gustav Fisher, Stuttgart, pp 49-66 bivalves. Canadian Journal of Zoology 72: 1169-1177 Johnson LE (1995) Enhanced early detection and enumeration Borcherding J (1991) The annual reproductive cycle of the of zebra mussel (Dreissena spp.) veligers using cross- freshwater mussel Dreissena polymorpha Pallas in lakes. polarized light microscopy. Hydrobiologia 312: 139-146 Oecologia 87: 208-218 Juhel G, Culloty SC, O’Riordan RM, O’ Connor J, De Faoite Borcherding J (1995) Laboratory experiments on the influence L and McNamara R (2003) A histological study of the of food availability, temperature and photoperiod on gonad gametogenic cycle of the freshwater mussel Dreissena development in the freshwater mussel, Dreissena polymorpha (Pallas, 1771) in Lough Derg, Ireland. Journal polymorpha. Malacologia 36: 15-27 of Molluscan Studies 69: 365-373 Commons E (2000) The zebra mussel in Lough Key - veliger Kachanova A.A. (1961) Some data on the reproduction of research 1999. Unpublished BSc dissertation. Institute of Dreissena polymorpha Pallas in Uchinsk reservoir. Trudy. Technology, Sligo Vses. Gidrobiol. Obsc. 11: 117-121. Doka SE (1994) Spatio-temporal dynamics and environ- Karatayev AY, Burlakova LE and Padilla DK (1998) Physical mental predictions of recruitment in industrial and factors that limit the distribution and abundance of nearshore Dreissena populations of Lake Erie. MSc Dreissena polymorpha (Pall.). Journal of Shellfish Dissertation, University of Guelph, Ontario Research 17: 1219-1235 Duggan S (2001) An investigation of Dreissena polymorpha Karatayev AY, Burlakova LE and Padilla DK (2006) Growth in Lough Key. Unpublished BSc dissertation. Institute of rate and longevity of Dreissena polymorpha (Pallas): a Technology, Sligo review and recommendations for future study. Journal of Ehrlich PR (1989) Attributes of invaders and the invading Shellfish Research 25: 23-32 processes: vertebrates. In: Drake JA, Mooney HA, di Kern R, Borcherding J and Neumann D (1994) Recruitment of Castri F, Groves RH, Kruger FJ, Rejmanek M and a freshwater mussel with a planktonic life-stage in running Williamson M (eds) Biological Invasion: a global waters – studies on Dreissena polymorpha in the River perspective, scope 37. John Wiley and Sons, Chichester, Rhine Archiv fuer Hydrobiologie 131: 385-400 pp. 315-328 Kirpichenko M.J (1964) Phenology, abundance and growth of Einsle U (1973) Zur horizontal und vertikalverteilung der Dreissena larvae in the Kujbysev reservoir. In: Sbornik larven von Dreissena polymorpha Pallas im pelagial des (ed.) Biologija Drejsseny I borba z nej. Izat Nauka, Bodensee-Obersees (1971). Gwf-wasser/abwasser 114: 27- Moskva 30 Lewandowski K (1982a) The role of early developmental Garton DW and Haag WR (1993) Seasonal reproductive stages in the dynamics of Dreissena polymorpha (Pall.) cycles and settlement patterns of Dreissena polymorpha in (Bivalvia) populations in lakes I. Occurrence of larvae in western Lake Erie. In: Nalepa, TF and Schloesser DW the plankton. Ekologia Polska 30: 81-109 (eds) Zebra mussels, Biology, Impacts and Control. Lewis Lewandowski K (1982b) The role of early developmental Publishers, Florida, pp. 111-128 stages in the dynamics of Dreissena polymorpha (Pall.) Gist DH, Miller MC and Brence WA (1997) Annual (Bivalvia) populations in lakes II. Settling of larvae and reproductive cycle of the zebra mussel in the Ohio River: a the dynamics of number of settled individuals. Ekologia comparison with Lake Erie. Archiv fur Hydrobiologie 138: Polska 30: 223-286 365-379 Lohan J (2004) An investigation of the early life stages of the Graczyk TK, Conn DB, Lucy F, Minchin D, Tamang L, zebra mussel, Dreissena polymorpha in Lough Key, 2003. Moura LNS and DaSilva AJ (2004) Human waterborne Unpublished BSc dissertation. Institute of Technology, parasites in zebra mussels (Dreissena polymorpha) from Sligo the Shannon River drainage area, Ireland. Parasitology Lucy F (2005) The dynamics of zebra mussel (Dreissena Research 93: 385-391 polymorpha) populations in Lough Key, Co. Roscommon, Haag WR and Garton DW (1992) Synchronous spawning in a 1998-2003. PhD dissertation, Institute of Technology, recently established population of the zebra mussel, Sligo Dreissena polymorpha, in western Lake Erie, USA. Lucy F and Sullivan M (2001) The investigation of an Hydrobiologia 234: 103-110 invasive species, the zebra mussel Dreissena polymorpha Hillbricht-Ilkowska A and Stanczykowska A (1969) The in Lough Key, Co Roscommon, 1999. Desktop study no. production and standing crop of planktonic larvae of 13. Irish EPA, Wexford, 38pp Dreissena polymorpha (Pall.) in two Mazurian lakes. Pol. Arch. Hydrobiol. 16:193-203 Lucy F, Sullivan M and Minchin D (2005) Nutrient levels and Howitt D and Cramer D (2003) A guide to computing the zebra mussel population in Lough Key. ERTDI Report statistics with SPSS11 for windows. Revised edition. Series No. 34. EPA, Wexford. Available at: Prentice Hall, Harlow www.epa.ie/EnvironmentResearch/ReportsOutput/FileUpl oad,8806,en.pdf Last accessed July 11 2006

181

F. Lucy

Lvova AA (1977) The ecology of Dreissena polymorpha in polymorpha) in Saginaw Bay, Lake Huron: population Uchinskoe reservoir. Candidate dissertation, Moscow recruitment, density and size structure. Journal of Great University Lakes Research 21: 417-434 Lvova AA (1980) Ecology of Dreissena polymorpha (Pall). Ni Chonmhara E (1999) The zebra mussel in Lough Key, Trudy Vserossijskogo gidrobiologicheskogo obshchestva 1998-1999. Unpublished BSc dissertation. Institute of 23: 101-119 Technology, Sligo. Mackie GL (1991) Biology of the exotic zebra mussel, Nichols SJ (1996) Variations in the reproductive cycle of Dreissena polymorpha, in relation to native bivalves and Dreissena polymorpha in Europe, Russia and North its potential impact in Lake St. Clair. Hydrobiologia 219: America. American Zoologist 36: 311-325 251-268 O’ Mahoney K (2003) An investigation of Dreissena MacIssac H, Sprules WG and Leach JH (1991) Ingestion of polymorpha in Lough Key. Unpublished BSc dissertation. small-bodied zooplankton by zebra mussels (Dreissena Institute of Technology, Sligo. polymorpha): can cannabalism on larvae influence Pollux B, Minchin D, Van der Velde G, Van Alen T, Van der population dynamics? Canadian Journal of Fisheries and Staay S and Hackstein J (2003) Zebra mussels in Ireland Aquatic Science 48: 2051-2060 (Dreissena polymorpha), AFLP-fingerprinting and boat Molloy DP, Karatayev, AY Burlakova LE, Kurandina DP and traffic both indicate an origin from Britain. Freshwater Laruelle F (1997) Natural enemies of zebra mussels: Biology 48: 1127-1139 predators, parasites and ecological competitors. Reviews Rehman CR, Stoeckel JA and Schneider DW 2003. Effect of in Fisheries Science 5: 27-97 turbulence on the mortality of zebra mussel veligers. Mantecca P, Vailati G, Garibaldi L and Bacchetta R (2003) Canadian Journal of Zoology 81: 1063-1069 Depth effects on zebra mussel reproduction. Malacologia Schneider DW, Stoeckel JA, Rehman CR, Blodgett KD, 45: 109-120 Sparks RE and Padilla DK(2003) A developmental Marsden JE (1992) Standard protocols for monitoring and bottleneck in pelagic larvae: implications for spatial sampling zebra mussels. Illinois Natural History Survey, population dynamics. Ecology Letters 6: 352-360 Biological Notes 138 Sprung M (1989) Field and laboratory observations of Marshall A (2002) An investigation of Dreissena polymorpha Dreissena polymorpha larvae: abundance, growth, in Lough Key. Unpublished BSc dissertation. Institute of mortality and food demands. Archiv fur Hydrobiologie Technology, Sligo 115: 537-561 Martel A (1993) Dispersal and recruitment of zebra mussel Stanczykowska A (1977) Ecology of Dreissena polymorpha (Dreissena polymorpha) in a nearshore area in west- (Pall.) (Bivalvia) in lakes. Polskie Archiwum central Lake Erie: the significance of postmetamorphic Hydrobiologii 24: 461-530 drifting. Canadian Journal of Fisheries and Aquatic Stanczykowska A. and Lewandowski K (1993) Thirty years of Science 50: 3-12 studies of Dreissena polymorpha ecology in Mazurian McMahon RF (1992) The zebra mussel – the biological basis lakes of Northeastern Poland. In: Nalepa TF and of its macrofouling and potential for distribution in North Schloesser DW (eds) Zebra mussels, Biology, Impacts and America. Corrosion 92, NACE Annual Conference and Control. Lewis Publishers. Florida, pp. 3-38 Corrosion Show. Houston Stoeckel, JA, Padilla DK, Schneider DW and Rehmann, CR Minchin D, Lucy F and Sullivan M (2002a) Zebra mussel: (2004) Laboratory culture of Dreissena polymorpha Impacts and Spread. In: Leppakoski E, Gollasch S and larvae: spawning success, adult fecundity and larval Olenin S (eds) Invasive Aquatic Species of Europe: mortality patterns. Canadian Journal of Zoology 82: 1436- Distribution, Impacts and Spread. Kluwer Press, 1443 Dordrecht, pp 135-146 Sullivan M, Lucy F and Minchin D (2002) The association Minchin D, Lucy F and Sullivan M (2005) Ireland: a new between zebra mussels and aquatic plants in the Shannon frontier for the zebra mussel Dreissena polymorpha Pallas. River system, Ireland. Aquatic Invaders 13: 6-9 Oceanological and Hydrobiological Studies 34:19-30. Toner PF (1979) The trophic status of Irish lakes, Lough Key. Available at: www.oandhs.org/articleB.php? An Foras Forbatha, Dublin category=3&article=109 Last accessed July 11 2006 Walz N (1973) Studies on the biology of Dreissena Nalepa TF, Wojik JA, Fanslow DL and Lang, GA (1995) polymorpha Pallas in the Lake of Constance. Archiv fuer Initial colonization of the zebra mussel (Dreissena Hydrobiologie Supplementband 42: 452-458

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