Research Article |
Corresponding author: James E. Gawel ( jimgawel@uw.edu ) Academic editor: Ian Duggan
© 2024 Shaina R. Myers, Hailey E. Germeau, Meghan McCann, Wyatt Cranston, Charles M. Crisafulli, Kena Fox-Dobbs, James E. Gawel.
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:
Myers SR, Germeau HE, McCann M, Cranston W, Crisafulli CM, Fox-Dobbs K, Gawel JE (2024) Establishment and ecological integration of the New Zealand mud snail in Spirit Lake, Mount St. Helens, Washington State, USA. Aquatic Invasions 19(3): 287-307. https://doi.org/10.3391/ai.2024.19.3.134082
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Mount St. Helens National Volcanic Monument was designated by the U.S. Congress in 1982 to conserve the landscape for natural regeneration, scientific research, education, and cultural resource preservation. However, this designation has not eliminated threats from the introduction of non-native species. The non-native New Zealand mud snail (NZMS), Potamopyrgus antipodarum, was first observed in 2016 along the SW shore of Spirit Lake at the foot of Mount St. Helens, despite the lake’s closure to public recreation and isolation from other known sites harboring NZMS. Our study mapped native and non-native snails on aquatic macrophytes in Spirit Lake, analyzed NZMS eDNA in Spirit Lake and surrounding waters, measured stable isotopes in snails and their food sources, and analyzed rainbow trout (Oncorhynchus mykiss) gut contents from a twenty-year survey to examine the patterns of spatial distribution, habitat occurrence, and resource use. Our results show that NZMS colonies were likely first established along the SW shore of Spirit Lake in 2015, and presently remain largely confined to the vegetated littoral zone along this same shoreline. The native snail species Gyraulus deflectus and NZMS co-occur on multiple macrophyte species, and δ¹⁵N and δ¹³C isotope data reveal they are consuming the same food sources, but no evidence was seen for competitive exclusion. The abundance and frequency of NZMS found in rainbow trout gut contents have increased since 2015 with a significant portion undigested. In addition, stable isotope analysis shows a negligible trophic tie between snails (both NZMS and G. deflectus) and rainbow trout, which may signal longer-term impacts on fish populations. Characterizing this invasion spatially and temporally elucidates the factors facilitating and hindering the spread of NZMS in a relatively young and dynamic subalpine lake ecosystem closed to public recreation, and may inform current and future management decisions.
rainbow trout, Potamopyrgus antipodarum, aquatic macrophyte, stable isotope analysis, Gyraulus deflectus
Globally, invasive species such as New Zealand mud snails (NZMS), Potamopyrgus antipodarum (Gray, 1843), have proven to decrease biodiversity and threaten the overall health of invaded ecosystems (
Disturbed landscapes, like Spirit Lake in Mount St. Helens National Volcanic Monument, are especially vulnerable to invasion. Spirit Lake was in the direct path of the massive debris avalanche, explosive lateral blast, and subsequent pyroclastic flows of the cataclysmic May 18th, 1980 eruption of the Mount St. Helens volcano (
Rainbow trout (Oncorhynchus mykiss) were first discovered to have repopulated Spirit Lake in 1993 (
Spirit Lake serves as a unique setting to study NZMS invasion because it is a relatively new, intensely disturbed ecosystem that is isolated from the typical industrial (transporting of aquaculture products, including fish hatchery stocking) and recreational activities (boating and fishing) often associated with the spread of NZMS (
Spirit Lake is located 8 km northeast of the summit of Mount St. Helens in southwestern Washington State, USA (Fig.
On two dates in October 2019 we gathered water samples from 18 sites for eDNA testing (Fig.
Sampling for aquatic macrophytes with attached snails occurred on multiple dates during the summers of 2021 and 2022. Samples of common and abundant macrophyte taxa (Myriophyllum spicatum, Charales (Class, Charophyceae)) , Ceratophyllum demersum, Potamogeton amplifolius, and filamentous algae) were gathered using a plant rake at water depths ranging from 1 to 5 m. Macrophyte samples were floated in water in a clear plastic tub and agitated by hand for 30 s to release any attached snails from the vegetation. Snails were allowed to sink to the bottom and separated from the vegetation. Subsequent periodic examination of the vegetation after agitation showed this method to be very effective at separating snails from vegetation, with < 1% of total snail abundance remaining on any vegetation sample. Any additional snails found in rechecked samples were not included in sample totals for method consistency. Macrophytes were then removed by hand, identified, and vegetation volume was estimated using a graduated beaker. The area of vegetation sampled was estimated using the diameter of the rake head, which was rotated on the pole axis to collect a circular sample of macrophytes. The remaining solids and detached snails were then transferred to plastic containers on ice for transport to University of Washington Tacoma for analysis. Snails were separated from any remaining solids, identified, and manually counted under a dissecting microscope. A subset of macrophyte and snail samples collected in 2021 were kept for stable isotope analysis.
Annual sampling of rainbow trout began at Spirit Lake in 2000 using hook and line and gillnet methods (Suppl. material
Aquatic insect larvae samples (Ephemeroptera, Plecoptera, Trichoptera, Odonata), aquatic mite samples (Hydrachna species), and amphibian tadpole samples (Anaxyrus boreas) were collected from benthic (log mat and littoral) substrates in the summers of 2018 and 2021. Arthropod specimens were scraped off submerged substrates with a modified brush and picked off substrates with forceps, and amphibians were captured with handheld dip nets. Emergent Ephemeroptera were collected from emergence traps (amphibious emergence trap - black and white, BugDorm, MegaView Science Co.) over logs and the lake surface. All samples were transported on ice, and stored frozen until they were prepared for stable isotope analysis.
Macrophyte samples were dried at 40 °C to a constant weight, and then pulverized in a mortar and pestle. Aquatic arthropod samples that were large enough were dissected, and head, thorax and legs were preferentially subsampled for analysis. Smaller arthropods, including mites and midge larva, were kept as intact individuals, and whole snail bodies were carefully extracted from their shells.
All samples were analyzed for carbon and nitrogen stable isotope ratios (reported as δ¹³C and δ¹⁵N values) at the University of Colorado Earth Systems Stable Isotope Laboratory using an elemental analyzer coupled to a Thermo Delta V Isotope Ratio Mass Spectrometer. Sample δ¹³C and δ¹⁵N values are reported relative to Vienna Pee Dee Belemnite and air N2 standards, respectively.
We assumed that the isotopic values of all samples were seasonally comparable and reflected the spring and summer growth season (May-September) in Spirit Lake. We used elemental C and N content to verify that invertebrate samples (comprised of chitin, proteinaceous materials, and soft tissues) were comparable among individuals; weight percent C/N ratios were within the range of 3.2 – 5.5 (except for 6 samples with higher ratios that were not isotopically anomalous and thus retained in the dataset). The tadpole tail and fin samples were fleshy and assumed to be primarily composed of skin, muscle, and connective tissues, and all C/N ratios fell within a range of 4.2–4.3. The rainbow trout fin tip sample C/N ratios were relatively invariant (range = 2.9–3.4), which suggested there were not substantial differences in tissue composition. We confirmed that the larval and emergent Ephemeroptera δ¹³C and δ¹⁵N values were not significantly different (t-test, p > 0.05) and combined these into a single dataset for that taxon. We used data collected from the few 2021 macrophyte samples to supplement a published Spirit Lake 2018 macrophyte dataset (
Rainbow trout sampling was performed from 2000–2021 along the SW shore of Spirit Lake (Fig.
Our eDNA results showed non-zero concentrations ranging from 2.37–173.31 copies mL-1 of NZMS DNA in all samples collected in shallow waters along the SW shore in Spirit Lake, while no detectable DNA copies were measured in field blanks. Concentrations ranging from 1.74–102.32 copies mL-1 were found in slower-moving tributaries feeding into the SW shore of the lake, while no detectable DNA copies were measured in the faster-moving, unstable Willow Springs tributary (the second southernmost inlet stream along SW shoreline; Fig.
eDNA results were consistent with multiple visual presence/absence surveys conducted in 2019–2021 that confirmed the presence of NZMS along the SW shoreline of Spirit Lake and in slow-moving, vegetated tributaries flowing into the lake. NZMS were not visually detected in surveys conducted in the fast-moving Willow Springs tributary, nor in Coldwater Creek or Coldwater Lake. A previous study using eDNA for detecting NZMS (
Like many benthic aquatic macroinvertebrates, stable substrates and limited flow velocities are required for NZMS population establishment (
Macrophyte-associated sampling of NZMS and other resident snails was performed in 2021–2022 to create a finer scale map (Fig.
Mean densities (snail individuals m-3 fresh vegetation) and standard deviations by lake quadrant for snail species collected on aquatic macrophytes in Spirit Lake in 2021–2022.
Quadrant | n | P. antipodarum m-3 veg | G. deflectus m-3 veg | Lymnaea sp. m-3 veg |
---|---|---|---|---|
NW | 9 | ND | 27,230 ± 25,938 | 2,222 ± 6,667 |
NE | 10 | ND | 11,633 ± 16,922 | 51,856 ± 127,679 |
Leech Cove | 5 | 252,632 ± 405,529 | 57,065 ± 77,359 | 6,676 ± 6,726 |
Duck Bay | 8 | 104,463 ± 198,131 | 102,321 ± 100,573 | 3,500 ± 7,231 |
In 2021, examining rainbow trout gut contents as a spatially-linked bioindicator of NZMS presence/abundance, we sampled rainbow trout at four locations around Spirit Lake to see how fish consumption (Fig.
Both our eDNA and snail-macrophyte sampling results point to the SW shore of Spirit Lake as the initial point of NZMS colonization, as evidenced by the highest concentrations of NZMS in the study area. The SW shore of Spirit Lake has no established public access points and off-trail travel is discouraged. It is, however, the access point for lake researchers and tunnel maintenance work. Owing to the degree of this area’s isolation, it is likely that NZMS were introduced either by wildlife vectors (i.e., ducks/geese frequenting the area of the lake with highest macrophyte density;
A 2010 survey of aquatic macrophyte distribution in the lake showed only sparse aquatic vegetation between the SW shore and the NW arm (
In terms of water chemistry, Spirit Lake specific conductivity has been declining since the eruption, decreasing from 793 μS cm-1 in 1980 to 100 μS cm-1 in 2014; pre-eruption values of 19–27 μS cm-1 in 1974 may indicate specific conductivity values for the lake in the future (
Comparing NZMS to native snail species abundances in rainbow trout guts (Fig.
Mean densities (snail individuals m-3 fresh vegetation) of snail species collected on aquatic macrophyte species in Spirit Lake in 2021-2022. Within a given raked sample, all snail species in that sample are considered associated with all macrophyte species identified within that same sample.
snails m-3 vegetation | n | P. antipodarum | G. deflectus | Lymnaea sp. |
---|---|---|---|---|
Myriophyllum spicatum L. (ITIS) | 16 | 125,556 | 69,185 | 32,274 |
Charales (Order) | 13 | 81,260 | 35,076 | 5,231 |
Ceratophyllum demersum | 3 | 509,175 | 175,683 | 7,429 |
Potamogeton amplifolius | 13 | 85,193 | 54,618 | 6,949 |
Filamentous Algae | 4 | 34,706 | 89,412 | – |
Stable isotope analyses are routinely used to unravel aquatic food webs, and several studies have employed isotopic datasets to investigate the ecological role of NZMS in invaded ecosystems (
Carbon and nitrogen stable isotope (δ13C and δ15N) values of abundant and common groups of aquatic organisms in the Spirit Lake food web. Snail species = invasive, non-native NZMS (P. antipodarum) and native G. deflectus. Insect larva = Chironomidae, Ephemeroptera, Odonata, Plecoptera, Trichoptera. Aquatic mites = Hydrachna sp.. Amphibian tadpoles = Anaxyrus boreas. Ellipses are defined by mean δ13C and δ15N values ± standard deviations.
Carbon and nitrogen stable isotope (δ13C and δ15N) values of individual P. antipodarum and G. deflectus snails, and their primary diet sources in Spirit Lake. Periphyton and macrophyte ellipses defined by means ± standard deviations. Snail δ13C and δ15N values have been adjusted to account for isotopic trophic differences (mean ∆13Csnail-diet = 1.5‰, mean ∆15Nsnail-diet = 1.3‰,
As the scope of stable isotope sample collection for this study did not exhaustively sample all possible diet sources, we did not endeavor to quantify interactions between NZMS and other taxa in the Spirit Lake ecosystem. Even so, the degree of isotopic overlap between recently arrived NZMS and the resident G. deflectus demonstrated that both species were generalists whose diets similarly reflected resource availability. If either snail species were specialists of a particular resource, or combination of resources, we would expect a lower intraspecific variance primarily in δ¹³C values. Likewise, if the snail species were specialists of different resources, we would expect interspecific differences primarily in δ¹³C values. Thus, the isotopic data complement the snail-vegetation data which showed shared habitat use by the snail species, and together these results suggest that interspecies competition between the snails may increase in the future.
The modest isotopic datasets presented for the common groups of aquatic organisms in the Spirit Lake ecosystem (Fig.
As NZMS and native snails (G. deflectus) were found in significant numbers in trout guts (Fig.
Carbon and nitrogen stable isotope (δ13C and δ15N) values of individual Spirit Lake rainbow trout (O. mykiss). “Snails” ellipses are defined by means ± standard deviations of P. antipodarum (black), and G. deflectus (white). “Trophic snails” ellipses and arrows represent the values for the same snail species after they have been adjusted to account for isotopic trophic differences between trout fin and snail tissue samples (mean ∆13Csnail-trout = 1.0‰,
The 1982 Congressional designation of the Mount St. Helens National Volcanic Monument limited future development and access to conserve the landscape for natural regeneration, scientific research, and cultural resource preservation (Public Law 97-243 §4, 1982: https://uscode.house.gov/statutes/pl/97/243.pdf). This designation has not meant that the Spirit Lake ecosystem has remained unimpacted by outside influences. The introduction of non-native aquatic macrophytes and now NZMS have all undoubtedly changed the ecology of the lake. However, this designation is meant to inform management actions to decrease the likelihood of altering the ecosystem through direct anthropogenic activities. For example, currently public access to Spirit Lake is limited to the Harmony Falls Trail #224 on the NE arm of the lake (Fig.
For NZMS, management decisions should seek to minimize the likelihood of increasing the speed or geographic extent of the invasion. NZMS have been found in Spirit Lake osprey droppings (vitality/mortality unknown; Gawel, unpublished data) and rainbow trout stomachs (alive), so wildlife spread is a possibility. However, in flowing waters downstream drift is a viable and significant means of transport for NZMS into new habitats (
More broadly, our field data support the lab results of
SRM: Formal analysis, Investigation, Writing - Original draft, Visualization; HG: Investigation, Visualization, Funding Acquisition; MM: Methodology, Investigation, Funding Acquisition; WC: Investigation, Funding Acquisition; CMC: Conceptualization, Methodology, Formal analysis, Investigation, Resources, Data Curation, Writing - Review and Editing, Visualization, Supervision, Funding Acquisition; KFD: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Resources, Writing - Review and Editing, Visualization, Supervision, Funding Acquisition; JEG: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Resources, Data Curation, Writing - Review and Editing, Visualization, Supervision, Project administration, Funding Acquisition
This work was supported by a grant from University of Washington Tacoma’s (UWT) School of Interdisciplinary Arts and Sciences’ Scholarship and Teaching Fund. The US Forest Service’s Pacific Northwest Research Station (PNWRS) also provided funding for this project. Co-authors Germeau and McCann were both supported by undergraduate research scholarships from the Washington Lake Protection Association and UW Tacoma Mary Cline Undergraduate Research Awards. Co-author Cranston was supported by a University of Puget Sound Geology Summer Research Grant. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of this manuscript.
All sample collection was completed following ethical practices and with the required permits or permission. Our research was approved and permitted by the US Forest Service and Washington Department of Fish and Wildlife, and permits are on file with co-author CM Crisafulli.
All data are available through Dryad (https://doi.org/10.5061/dryad.6t1g1jx71).
The authors thank Jeremy Davis (UWT), Avery Shinneman (University of Washington Bothell), Sierra Smith (Oregon State University and Mount St. Helens Institute (MSHI)), Heaven Denham (UWT), Moses Jouwsma (MSHI), Jim Johnson (MSHI and Pacific Northwest Research Station), and Audrey White (University of Puget Sound) for their help in field sample collection and laboratory sample identification and enumeration. We acknowledge the analytical contributions of the CU Boulder Earth Systems Stable Isotope Lab (CUBES-SIL) Core Facility (RRID:SCR_019300) and thank Ashley Maloney and Kathryn Snell. We also wish to acknowledge the thoughtful contributions of two anonymous reviewers who provided comments that greatly improved this manuscript.
Number of samples and year collected for stable isotope analyses, fish gut content analysis; and plant samples by lake region (tables S1–S3)
Data type: xlsx
Comparison of mean snail abundance on vegetation and in O. mykiss guts sorted by sampling region (fig. S1)
Data type: docx