Research Article |
Corresponding author: Jason L. Locklin ( jason.locklin@templejc.edu ) Academic editor: David Wong
© 2024 Jason L. Locklin, Josiah S. Moore, Robert F. McMahon.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Locklin JL, Moore JS, McMahon RF (2024) Comparative population dynamics of zebra mussel (Dreissena polymorpha) populations in two similar closely adjacent warm-water Texas reservoirs. Aquatic Invasions 19(3): 309-328. https://doi.org/10.3391/ai.2024.19.3.131793
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Zebra mussel (Dreissena polymorpha) population dynamics were recorded between 2 September 2019 and 26 September 2020 at marina sites in each of two adjacent central Texas water bodies, Belton (BL) and Stillhouse Hollow (SHL) Lakes infested in 2013 and 2016, respectively. Lake water temperatures were insignificantly different while dissolved oxygen, pH and Secchi Disk depths were slightly higher in SHL. Veliger densities in both populations peaked in late Fall 2019 with veligers becoming absent by January 2020. Veliger densities again peaked in May-August 2020. These fall and spring spawning periods resulted in the presence of fall and spring mussel settlement cohorts. Mussel densities on settlement plates were greater at SHL than BL. At both sites, Fall 2019 cohorts had a lifespan of approximately one year or less, experiencing mass mortality during peak water temperatures in late summer/early fall the year after initial cohort settlement. Shell growth rates of the Spring 2020 BL and SHL cohorts were 91.4 and 67.3 µm/day, over a 126 day growing period, respectively, falling within the range reported for mussel populations in other southwestern US water bodies. Rapid shell growth and maturation allowed initiation of spawning earlier than zebra mussel populations in cooler, higher latitudes. Rapid growth and early maturity allows southwestern US zebra mussel populations to rapidly attain peak densities after infestation followed by population declines as recorded in BL. That southwestern mussel populations rapidly attain post invasion peak densities allows little time for water using facilities to develop effective, environmentally acceptable means of protecting infrastructure from mussel fouling. Thus, plans to prevent/minimize mussel fouling should be made in advance of invasion. Similarly, water body managers should develop and implement plans to minimize invasion likelihood and for rapid response before invasion occurs.
settlement cohorts, shell growth rates, spawning times, temperature impacts, veliger densities, boom-bust
The invasive freshwater European zebra mussel (Dreissena polymorpha Pallas, 1771) was first found in North America during 1986 on the Canadian side of the Western Basin of Lake Erie byssally attached to natural gas well heads and well markers. Thereafter, it spread through Lake Erie, reaching Lake St. Clair (Michigan-Ontario) by 1988. It is considered to have been transported to North America as veliger larvae in the ballast waters of transatlantic ships released into the Great Lakes before entering ports (
In these three southwestern states, zebra mussels experience much higher summer water temperatures than at northern latitudes in their North American and native European ranges. Summer water temperatures in Kansas, Oklahoma and Texas approach or exceed the mussel’s previously considered 28–30 °C long-term upper thermal limit (
The elevated summer water temperatures that zebra mussels experience in these three south central US states have major impacts on their population dynamics including rapid growth rates, early maturity, bimodal spring and fall reproductive periods, and abbreviated lifes spans of approximately 12–16 months and 10–12 months for spring and fall cohorts, respectively (
The study was conducted at a marina site on Belton Lake (BL) (31.130394°N, -97.508359°W) and Stillhouse Hollow Lake (SHL) (31.020666°N, -97.525164°W) (Figure
BL (Figure
SHL is approximately 8 km southwest of the City of Belton. Construction was completed in 1968 for flood control, recreation, and municipal water supply (
At each lake, water temperature and dissolved oxygen (DO) were recorded hourly at 1 m, 6 m, and 11 m depths from 02 September 2019 – 24 September 2020 with submersible Onset HOBO U26 data loggers (Onset Computer Corporation, Bourne, MA, USA). Data were downloaded monthly and daily mean values for temperature and DO calculated. The SHL logger at 6 m was lost during May 2020 resulting in data loss thereafter. Additionally, discrete monthly measurements of pH, temperature, and DO were taken at 1 m intervals from the water’s surface to the bottom substratum using a YSI ProODO Optical Dissolved Oxygen Instrument (YSI Incorporated, Yellow Springs, OH, USA). Its readings were used to confirm data logger outputs and to capture this data at 1-m intervals throughout the water column. Dissolved oxygen values were computed as a percentage of full air O2 saturation (% DO) to allow O2 concentration levels to be expressed independently of temperature. Surface water levels during the 2019–20 study at both lakes were obtained from
At each monthly site visit, five vertical plankton net (50 µm mesh, 20 cm aperture) tows from 10 m depth allowed estimation of veliger densities from October 2019 – January 2021. Plankton tow samples were transported to the laboratory on ice where they were filtered and preserved in 70% ethanol for later microscopic veliger enumeration. The five tows were estimated to draw 1570.8 l of water through the plankton net. While mixing a plankton sample to suspend veligers, a 5 ml sample was drawn from the sample jar and released into the channel of a clear Plexiglass Bogorov Plankton Counting Chamber in which veligers were counted at 35× power from one end of the chamber channel to the other with a dissecting microscope equipped with a polarized light attachment making veliger shells birefringent and easily identifiable (
To estimate mussel settlement and densities across depths and time, sixteen 20×20 cm PVC settlement plates were deployed bimonthly in each lake on 27 August 2019, 20 September 2019, 22 December 2019, 23 February 2020, 25 April 2020, and 29 June 2020. Each set of plates remained in place through 26 September 2020. The settlement plates were placed horizontally along a weighted nylon rope attached to the marina superstructure and extending vertically to just above the lake bed. Four settlement plates each with a total surface area of 0.085 m2 separated by 5 cm PVC spacers were attached to the rope at depths of 1, 4.5, 8.4 and 11–12 m (sixteen plates total per rope). Readily identifiable mussels greater than approximately 2 mm in shell length (SL, the greatest linear distance from the anterior umbo to the posterior shell margin) on all deployed plates were counted monthly. Mussels with shell lengths <2 mm were not counted because they were too small to be accurately enumerated. Plates were exposed to air while shaded from sunlight only when mussels were being enumerated and were typically out of water for less than 10 minutes. To reduce mussel stress during counting, mussels were wetted with a spray bottle containing lake water. As in
Five settlement plates located at 6 m depth on a single rope were deployed in both lakes on 13 September 2019 to assess mussel shell length (SL) distributions and growth rates. Mussels were scraped from one of the plates on 23 May 2020, 26 June 2020, 25 July 2020, 29 August 2020, and 25 September 2020 with a sharp edged paint scraper and preserved in 70% ethanol. In the laboratory, sampled mussels were placed on a flatbed scanner and their shell lengths scanned at 600 dpi for measurement to the nearest 0.01 mm using Adobe Photoshop.
Lake water level variation throughout the sampling period was obtained from the Texas Water Development Board (
Water temperatures at the two sampling sites were also similar. Daily means of hourly temperature data at 1 m (surface), 6 m (middle) and 11 m (bottom) showed little thermal stratification from sampling initiation in September 2019 through March 2020 (Suppl. material
The pattern of water temperature variation discreetly measured monthly at 1 m intervals from the surface to a near bottom depth of 11 m (Suppl. material
Mean daily percent of full air O2 saturation (%O2) values were similar at both lake sites (Suppl. material
Discreet monthly %O2 determinations at 1-m intervals also differed between the two sites with relatively little hypoxia occurring at any depth in SHL while BL experienced periods of hypoxia during September 2019 and from July through August of 2020 (Suppl. material
pH in both lakes was greatest from January through March and lowest from July through September (Suppl. material
Secchi Disk depths recorded monthly from 29 September 2019 through 29 August 2020 were consistently higher at SHL than BL (Suppl. material
A seasonal pattern in mussel veliger density was recorded at both BL and SHL (Figure
Seasonal veliger density at SHL was similar to that of BL with the exception of not being sharply depressed on 28 August 2020 as recorded at BL. At SHL, no veligers occurred in the 20 September 2019 and 4 October 2019 samples (SWT = 29.1° and 28.3 °C). Veligers first appeared in the 27 October 2019 sample at 67.7 (±57.4) veligers 1000 l-1 (SWT = 20.8 °C), following which densities peaked at 5,817.0 (± 851.8) 1000 l-1 on 25 July 2020 (SWT = 28.9 °C). Thereafter, SHL veliger densities declined to 807.1 (±80.3) 1000 l-1 through 25 September 2020 (SWT = 26.2 °C), and fell to a minimum level of 2.6 (±4.7) 1000 l-1 on the final 01 January 2021 sample.
Mussels occurred on settlement plates after initial deployment on 02 September 2019 through final sampling on 26 September 2020 in both lakes (Figure
Zebra mussel settlement times and mean densities on settlement plates deployed in Belton (BL) (Figure 9A–F) and Stillhouse Hollow (SHL) (Figure 9G–L) Lakes bimonthly throughout a year-long study at depths of 1 m (red lines), 4.7 m (yellow lines), 8.4 m (sky blue lines) and near the bottom at 11–12 m (navy blue lines). The horizontal axis is date and the vertical axis is mussel density. Arrows in each graph indicate dates of settlement plate deployment. Settlement plates deployed on 27 October 2019 at BL were lost on 23 May 2020 (Figure
Mussel settlement patterns were associated with veliger presence. Fall veliger presence at the BL and SHL sites (Figure
When analyzed by a one tailed t-test assuming unequal variances, mean densities of mussels on the four settlement plates across depths of 1, 4.7, 8.4, and 11–12 m combined over the course of the study was significantly higher in SHL relative to BL (p range = 0.0030–0.049) at 10 of 11 sampling periods, and only not being significantly different (p = 0.139) in the 28 June 2020 sample (Figure
Combined mean densities of zebra mussels recorded from 24 November 2019 – 26 September 2020 on settlement plates deployed at depths of 1.0, 4.7, 8.4, and 11–12 m on 2 September 2019 in Belton (yellow) and Stillhouse Hollow Lakes (red) when mussels had settled on plates at all four depths. Vertical lines above bars indicate standard deviations of the mean. Red asterisks above paired bars indicate significant difference in mean mussel density determined by a t-test assuming unequal variances (p ≤ 0.05). P values for each paired set of mussel densities at the two lakes are indicated above the yellow Belton Lake density bars.
Long-term studies of zebra mussel population dynamics in three Texas water bodies, including the BL site, have indicated that they have spring and fall settlement cohorts that die out during the following year’s late summer-to-early fall period following chronic exposure to elevated water temperatures (
Shell length-frequency distributions of generation cohorts of zebra mussels sampled from settlement plates at (A) Belton and (B) Stillhouse Hollow Lakes. The horizontal axis is sampling date and the vertical axis is shell length in millimeters. Horizontal bars indicate percent of the total sample at each 0.1 mm in shell length. White lines connect mean sample shell lengths for different mussel settlement cohorts, i.e., 2019 fall cohort (upper line) and 2020 spring cohort (lower line). Vertical white bars about mean cohort shell length points are standard deviations.
Spring 2020 cohorts first settled on 26 June 2020 at both sites after appearance of high veliger densities on 23 May 2020 (Figure
The physiochemical similarity of BL and SHL sampling sites allows a relatively direct comparison of the impact of post-invasion time on their population dynamics. During our study, SHL veliger density was much higher than at the BL site. At the time of our study, zebra mussels were known to have been present in BL since 2013 and SHL since 2016. In 2015, two years after invasion, peak BL sampling site veliger density at 1–1.5 m depth was 165,054 1000 l -1. By 2017, peak densities had fallen to 19,281 1000 l-1 (
Such long-term density declines after attaining density maxima as reported for zebra mussel populations in warm water southwestern US water bodies have been labeled as boom-bust dynamics by
Mussel densities on settlement plates at the SHL site were consistently significantly higher than at the BL site corresponding to higher veliger concentrations during the spring 2020 reproductive period. At peak average density on 25 July 2020, SHL site density at 25,732 mussels m-2 was 6.4 times greater than that of the BL site of 4,027 mussels m-2. Earlier studies recorded much higher mussel densities at the BL site between 2015 and 2017 (
Mussels on sampling plates at both sampling sites had life spans of approximately one year or less with individuals from the previous 2019 spring and fall reproductive periods dying out by July (SHL) or September (BL) during 2020. Similar late summer adult mussel die offs have been reported for other mussel populations in southwestern US water bodies including Oologah Lake, Oklahoma (
The one year life spans of southwestern zebra mussel populations may be a result of adult mussels being unable to consume phytoplankton/bacterioplankton at rates needed to sustain metabolic demands leading to tissue loss (i.e., starvation) and eventual mortality as reported by
At both sites, spring cohort mean shell lengths were significantly different on the final 25 September 2020 sampling date of 11.5 ± 3.3 (BL) and 8.5 ± 3.9 (SHL), allowing mean shell growth rates over a shell growth period of 126 days to be estimated as 91.4 and 67.3 µm/day, respectively. The elevated shell growth rates of BL relative to SHL mussels may have been a result of higher food availability and/or lower zebra mussel densities reducing food competition. Greater chlorophyll a concentrations at the BL site relative to the SHL site during 2021–2022 (Locklin, unpublished) are suggestive of increased food resources at BL. Overall shell growth rates for the 2020 spring mussel generations at both sites were lower than those reported in other southwestern US water bodies. During 2016–17 spring season mussel shell growth rates at the BL site were estimated to be 127.9 µm day-1 (
Our study presents evidence that Dreissena polymorpha in warm southwestern US water bodies exhibit more rapid shell growth rates and shorter life spans of approximately one year compared to mussels from cooler, higher latitudes in North America and Europe. Rapid growth allows early maturation and spawning. Spring cohorts spawn the subsequent fall and spring and fall cohorts spawn the following spring. Rapid growth leads to mussels in southwestern water bodies to relatively rapidly attain peak densities after initial invasion. The ability of mussels in southwestern water bodies to rapidly achieve high densities allows little time for water using facilities to develop effective and environmentally acceptable means of protecting their infrastructure from mussel fouling. As such, southwestern US water using facilities should consider developing mussel macrofouling control plans, acquire needed equipment and make modifications for prevention and management of zebra mussel infestations in advance of potential mussel invasion. Similarly, managers of uninfested water bodies should develop plans to minimize the likelihood of mussel introduction and for a rapid response to mussel invasion before mussels invade their water bodies. Early planning and preparation will allow application of effective mitigation and control procedures during the early stages of infestation.
Further studies of dreissenid population dynamics in southwestern US water bodies are required to establish whether abbreviated life spans, high growth rates, and early reproduction leading to rapid zebra mussel population expansion and damage to water using infrastructure and aquatic habitats will be the norm for warm southwestern US water bodies. Especially needed are long-term studies to determine if post invasion mussel population decline is a general characteristic of zebra mussels in southwestern water bodies because it could impact decisions regarding development of mussel macrofouling mitigation/control plans for raw-water using infrastructure and management plans for response to mussel invasions.
Jason L. Locklin: research conceptualization, sample design and methodology, investigation and data collection, data analysis and interpretation, writing original draft, and review and editing. Josiah S. Moore: investigation and data collection, data analysis and interpretation, and writing original draft. Robert F. McMahon: data analysis and interpretation, writing original draft, and writing, review and editing.
This study was funded by a grant from the Temple Health and Bioscience District. The funding agency had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.
The research was conducted under a Texas Parks and Wildlife Exotic Species Permit No: RES 09 16-121 awarded to Jason L. Locklin.
We thank Sam Poster, Brittany Lokcu, Alex Flory, Jessica Konkler, and Tyler Wilson for their assistance in the laboratory and field. We also thank Jacob Wilson for providing editorial feedback on the manuscript, and the staff at Frank’s (BL) and Stillhouse Hollow (SHL) Marinas for allowing us to access and attach equipment to the marina’s infrastructure during the study. Two anonymous reviewers made important contributions to the manuscript
Water level variation at Belton and Stillhouse Hollow Lakes
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Explanation note: fig. S1. Water level variation at (A) Belton and (B) Stillhouse Hollow Lakes over the course of the sampling period. Dashed lines in both figures indicate conservation pool level.
Daily means with standard deviations of hourly water temperatures recorded
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Explanation note: fig. S2. Daily means with standard deviations of hourly water temperatures recorded at approximate depths of 1 m (red)), 6 m (white) and the bottom at 11 m (blue) at the (A) Belton Lake and (B) Stillhouse Hollow Lake sampling sites. The data logger at 6 m depth in Stillhouse Hollow was lost during May 2020 resulting in no further temperature records at that depth.
Discrete monthly water temperatures recorded during sampling of zebra mussels
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Explanation note: fig. S3. Discrete monthly water temperatures recorded during sampling of zebra mussels at 1 m intervals from the water’s surface to the bottom at sampling sites in (A) Belton Lake and (B) Stillhouse Hollow Lake. Bottom sampling depths were as great as 13 m at Belton Lake and 12 m at Stillhouse Hollow Lake during infrequent periods of high water. Water temperatures at depths of 1 through 11 m that were sampled continuously are connected by solid lines.
Daily means with standard deviations of hourly percent of full air O2 saturation values recorded
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Explanation note: fig. S4. Daily means with standard deviations of hourly percent of full air O2 saturation values recorded at approximate depths of 1 m (red), 6 m (white) and the bottom at 11 m (blue) at the (A) Belton and (B) Stillhouse Hollow Lake sampling sites. The data logger at Stillhouse Hollow Lake was lost during May 2020 resulting in no further oxygen records at that depth.
Percent of full air O2 saturation values recorded during sampling of zebra mussels
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Explanation note: fig. S5. Percent of full air O2 saturation values recorded during sampling of zebra mussels at 1 m intervals from the water’s surface to the bottom at the sampling sites in (A) Belton Lake and (B) Stillhouse Hollow Lake. Bottom sampling depths were as great as 13 m at Belton and 12 m at Stillhouse Hollow Lake during infrequent periods of high water. Percent of full air O2 saturation values able to be sampled continuously throughout the sampling periods are connected by solid lines of different colors representing different depths to a maximum of 11 m at both sites.
Monthly pH values recorded at 1 m depth intervals from the water surface to the bottom at the sampling sites
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Explanation note: fig. S6. Monthly pH values recorded at 1 m depth intervals from the water surface to the bottom at the sampling sites of (A) Belton Lake and (B) Stillhouse Hollow Lake. Bottom sampling depths were as great as 13 m at BL and 12 m at SHL during infrequent periods of high water. Values of pH able to be sampled continuously throughout the sampling period are connected by solid lines of different colors representing different depths to a maximum of 11 m at both sites.
Monthly Secchi Disk depth measurements at the sampling sites
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Explanation note: fig. S7. Monthly Secchi Disk depth measurements at the sampling sites of (A) Belton (red) and (B) Stillhouse Hollow (blue) Lakes.
Annual means and paired T-test values for water temperature, O2 concentration measured as percent of full air O2 saturation, and pH
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Explanation note: table S1. Annual means and paired T-test values for water temperature, O2 concentration measured as percent of full air O2 saturation, and pH at depths ranging from 1–11 meters at the sampling sites on Belton and Stillhouse Hollow Lakes, Texas, along with mean Secchi Disk depths sampled approximately monthly from 9 July 2019 – 25 September 2020. Significant differences between lakes are indicated by red p values marked with an asterisk.