Lakes often exist in two alternative stable states: clear waters dominated by submerged aquatic vegetation and turbid states with an abundance of phytoplankton. Management decisions must balance the value of primary producers with recreational use. We monitored the phytoplankton community surrounding removal of invasive Potamogeton crispus, a submerged aquatic perennial. Focus was given to presence of cyanobacteria, which may thrive in the absence of macrophytes by virtue of phosphorus that would otherwise be stored in plant biomass. Results demonstrate that macrophyte removal can lead to an increase in cyanobacteria dominance, with sustained impacts after hand removal.
","acknowledgements":"We are grateful to the lake association members for providing access to the lake and contextual information regarding the lake's history.
","authors":[{"affiliations":["Penn State Berks, Reading, PA, US "],"departments":["Biology"],"credit":["conceptualization","formalAnalysis","methodology","writing_originalDraft"],"email":"sbp20@psu.edu","firstName":"Sarah D","lastName":"Princiotta","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0002-9152-4146"},{"affiliations":["Penn State Schuylkill, Schuylkill Haven, PA, US"],"departments":["Biology"],"credit":["formalAnalysis","dataCuration","methodology","investigation","writing_reviewEditing"],"email":"ejo5215@psu.edu","firstName":"Emily","lastName":"Ostergaard","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["Holy Family University, Philadelphia, PA, US"],"departments":["Biology"],"credit":["conceptualization","formalAnalysis","methodology","investigation","writing_reviewEditing","resources"],"email":"ecarroll2@holyfamily.edu","firstName":"Elizabeth","lastName":"Carroll","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[],"funding":"No funding to report.
","image":{"url":"https://portal.micropublication.org/uploads/e689d99d7dbb8978e802cfaa91cfaf64.JPG"},"imageCaption":"Percentage of the phytoplankton community composed of cyanobacteria where Potamogeton crispus was removed by hand or mechanically and otherwise left undisturbed (control). The month of June represents pre-treatment conditions. Letter cases indicate results of post-hoc Tukey HSD within each site.
","imageTitle":"Percentage of the phytoplankton community composed of cyanobacteria based on month and form of aquatic plant removal
","methods":"Field collection and Enumeration of Cyanobacteria by Microscopy
The study lake (Zmax 14 m, ~24 ha.) is a natural lake of glacial origin located in Pike County, Pennsylvania. Identifying information, including lake name, are not included here per sampling agreement. The vegetation within the drainage basin is primarily forested and the lake has no inlet streams. Routine lake monitoring from a central location on the study lake report a range of summer Secchi depth from 2.5 – 3 m, epilimnetic chlorophyll from 0.42 – 3.4 mg L-1, and epilimnetic total phosphorus from 4.45 – 5.75 mg L-1. The phytoplankton community is dominated by cyanobacteria genera that can produce cyanotoxins (Limnothrix, Aphanizomenon, Dolichospermum).
Curly-leaf Pond Weed (Potamogeton crispus), a submerged perennial, was first identified in the study lake during 2020-2021, composing ~12 acres of the shoreline in 2023. In July 2024, a combination of hand removal and mechanical harvest removed ~95% of P. crispus from the shoreline. Seven acres were treated by mechanical harvest (site MR) and five acres by hand removal (HR) over a two-day period. The mechanical harvester was able to both cut and collect aquatic macrophytes up to 1.3 m below the surface. Hand removal efforts sought to remove all P. crispus, including the roots, but the macrophyte commonly broke mid-stem. Each site, including an area that was not treated (control), was sampled three times over the course of the study period: one week prior to plant removal (June), and 29 (July) and 56 (August) days after removal.
During each sampling event, triplicate sub-surface (0.50 m) water was collected by Van Dorn bottle, passed through a 153-mm mesh, and stored in 250-mL polycarbonate bottles. Each sample was fixed with a final concentration of 2% Acid Lugol’s and stored in darkness prior to analysis. Samples were concentrated by settling over a 48-hour period after which the remaining ~20 mL was kept for microscopy. A minimum of 300 natural units were identified by light microscopy using a Zeiss Axiovert A1 at 400X magnification using the Utermol method (Paxinos and Mitchell, 2000). Phytoplankton, including cyanobacteria, were identified to genus apart from cells < 5mm diameter that lacked distinctive features, which were grouped as “unidentified nanoplankton.”
Statistical Analysis
All data analysis was conducted in JMP 18.2.2. Normality and homogeneity of variance were confirmed with a Shapiro Wilk and Levene test, respectively. To meet the assumptions for statistical testing, cyanobacteria abundance and percentage of the community composed of cyanobacteria were log and logit transformed, respectively. One-way ANOVA with post-hoc Tukey HSD was used for each site to explore the impact of the removal method over time on cyanobacteria abundance and percentage of the community composed of cyanobacteria. Figure was made using R version 4.2.3.
","reagents":"","patternDescription":"Despite their evolutionary origins as key aquatic primary producers, dense proliferations, or “blooms” of potentially harmful cyanobacteria are an issue for water quality management in lakes and reservoirs worldwide. The drivers of cyanobacteria dominance and production of toxic secondary metabolites are complex and likely related to environmental conditions associated with global climate change (Paerl et al., 2016). An increased frequency and severity of cyanobacteria blooms are often associated with high surface water temperatures and anthropogenic eutrophication (Kosten et al., 2012; Chapra et al., 2017) Lake managers are now tasked with preventing and responding to cyanobacteria blooms that have been implicated in public health consequences for wildlife, pets, and humans (Backer et al., 2013; Trevino-Garrison et al., 2015; Skafi et al., 2021).
Another threat to freshwater ecosystems is the overgrowth of invasive, submerged aquatic vegetation (Kuiper et al., 2017), which may compromise use of recreational lakes for boating and fishing. Although important to the structure of lake ecosystems as a source of habitat, sediment stability, and nutrient storage (van Donk and van de Bund, 2002; Kovalenko et al., 2010), excess growth of submerged aquatic macrophytes can have negative impacts on water quality when decomposition releases large amounts of phosphorus and consumes dissolved oxygen (Asaeda et al., 2000). There are several methods to manage aquatic macrophytes including removal by either hand or motorized harvesters and chemical treatment with herbicides. Removal of excessive amounts of aquatic macrophytes should be conducted with great caution, as they stabilize the clear water state of shallow lakes (Scheffer et al., 1993). However, it can also be important to balance lake ecosystem health with recreational user preferences.
Aquatic macrophytes may act as natural control agents for cyanobacteria blooms via release of allelopathic compounds (Jasser, 1995), shading, and nutrient competition (Zhou et al., 2017). Field studies that document changes in phytoplankton community structure after removal of aquatic vegetation by various methods are lacking and produce mixed results (Morris et al., 2006; Maredová et al., 2021), especially in lakes that receive a temporally-restricted, rather than continuous, removal of dense stands of aquatic vegetation. We took advantage of lake management action to study the impacts of aquatic plant removal (Potamogeton crispus) by either hand or mechanical harvest on the presence of cyanobacteria. A control was provided by a site in which aquatic plants were undisturbed and present at a low density. We hypothesized that removal of P. crispus, either by hand or mechanical removal, would lead to an increase in cyanobacteria as representatives in the phytoplankton community, with potentially greater impacts on the hand removal site where fragmented plant matter could act as an inadvertent nutrient source. Removal of P. crispus may also enhance cyanobacteria growth due to reduced nutrient competition.
Prior to removal of P. crispus, there was no difference in the percentage of the phytoplankton community composed of cyanobacteria across sites (11% ± 2 SE). However, prior to any site modification, there were notable differences in the abundance of cyanobacteria by site (F2,3 = 15.41, p = 0.03), with a higher abundance of cyanobacteria in the site designated for mechanical removal relative to that designated for hand removal. Prior to any treatment, the abundance of cyanobacteria at the experimental sites destined for plant removal were not significantly different from the control site.
There was a significant effect of month on the percentage of the community composed of cyanobacteria at both the hand-removal (F2,4 = 24.85, p = 0.0055) and control site (F2,4 = 25.09, p = 0.0054). At the hand-removal site, the percentage of the phytoplankton community composed of cyanobacteria increased over time from 7% to 62%, with significant differences between June, prior to plant removal, and August (p = 0.0048). There was not a significant effect of month on the abundance of cyanobacteria at the hand removal site, suggesting the observed increase in percentage of the phytoplankton community composed of cyanobacteria may result from changes in community structure. It is possible that non-cyanobacteria members of the phytoplankton community did not respond as favorably to conditions associated with hand removal of P. crispus relative to cyanobacteria. Hand removal of P. crispus may have increased the availability of photosynthetic active radiation (PAR) and nutrients available to the phytoplankton, of which cyanobacteria are well-adapted at capitalizing.
In the control site where aquatic plants were undisturbed, there was an initial, although non-significant, decline in the percentage of the community composed of cyanobacteria between pre-treatment conditions in June and July. However, cyanobacteria dominance (%) increased significantly between July and August (p = 0.0047). When considering cyanobacteria abundance at the control site, there was a significant effect of month (F2,4 = 41.75, p = 0.002), where cyanobacteria abundance also increased from July to August (p = 0.002), and the abundance in August was higher than the pre-treatment conditions (p = 0.01). It is worth noting that whereas the cyanobacteria population was kept low between June and July in the control site, there was a positive response of month on non-cyanobacteria members of the phytoplankton community within the same time frame. These results are indicative of the potentially negative allelopathic interactions between P. crispus and cyanobacteria or at least a differential response between the phytoplankton community to the presence of P. crispus.
In July but not August, there was a significant effect of site on the percentage of the community composed of cyanobacteria (F2,3 = 13.27, p = 0.03). A higher percentage of cyanobacteria were observed in the hand and mechanical removal sites relative to the control site where aquatic plants were undisturbed. Approximately one month after treatment, cross-site differences in cyanobacteria dominance (%) were no longer apparent. It may be interpreted that presence of excessive P. crispus had a negative impact on cyanobacteria that was temporarily relieved after removal of the aquatic macrophyte by either hand or mechanical measures. Our methodological approach does not allow us to interpret if this is due to regrowth of P. crispus, decomposition of fragmented plant material, or natural differences in cyanobacteria dominance that may occur within a single ecosystem. We suggest future studies to follow impacts of P. crispus removal through the fall germination period. This work provides a basis for targeted investigations that seek to balance invasive plant management with ecological health.
","references":[{"reference":"Asaeda T, Trung VK, Manatunge J. 2000. Modeling the effects of macrophyte growth and decomposition on the nutrient budget in Shallow Lakes. Aquatic Botany 68: 217-237.
","pubmedId":"","doi":"10.1016/S0304-3770(00)00123-6"},{"reference":"Backer L, Landsberg J, Miller M, Keel K, Taylor T. 2013. Canine Cyanotoxin Poisonings in the United States (1920s–2012): Review of Suspected and Confirmed Cases from Three Data Sources. Toxins 5: 1597-1628.
","pubmedId":"","doi":"10.3390/toxins5091597"},{"reference":"Chapra SC, Boehlert B, Fant C, Bierman VJ, Henderson J, Mills D, et al., Paerl. 2017. Climate Change Impacts on Harmful Algal Blooms in U.S. Freshwaters: A Screening-Level Assessment. Environmental Science & Technology 51: 8933-8943.
","pubmedId":"","doi":"10.1021/acs.est.7b01498"},{"reference":"van Donk E, van de Bund WJ. 2002. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany 72: 261-274.
","pubmedId":"","doi":"10.1016/S0304-3770(01)00205-4"},{"reference":"Jasser I. 1995. The influence of macrophytes on a phytoplankton community in experimental conditions. Hydrobiologia 306: 21-32.
","pubmedId":"","doi":"10.1007/BF00007855"},{"reference":"Kosten S, Huszar VLM, Bécares E, Costa LS, van Donk E, Hansson LA, et al., Scheffer. 2011. Warmer climates boost cyanobacterial dominance in shallow lakes. Global Change Biology 18: 118-126.
","pubmedId":"","doi":"10.1111/j.1365-2486.2011.02488.x"},{"reference":"Kovalenko KE, Dibble ED, Slade JG. 2010. Community effects of invasive macrophyte control: role of invasive plant abundance and habitat complexity. Journal of Applied Ecology 47: 318-328.
","pubmedId":"","doi":"10.1111/j.1365-2664.2009.01768.x"},{"reference":"Kuiper JJ, Verhofstad MJJM, Louwers ELM, Bakker ES, Brederveld RJ, van Gerven LPA, et al., Mooij. 2017. Mowing Submerged Macrophytes in Shallow Lakes with Alternative Stable States: Battling the Good Guys?. Environmental Management 59: 619-634.
","pubmedId":"","doi":"10.1007/s00267-016-0811-2"},{"reference":"Maredová N, Altman J, Kaštovský J. 2021. The effects of macrophytes on the growth of bloom-forming cyanobacteria: Systematic review and experiment. Science of The Total Environment 792: 148413.
","pubmedId":"","doi":"10.1016/j.scitotenv.2021.148413"},{"reference":"Morris K, Bailey PCE, Boon PI, Hughes L. 2006. Effects of plant harvesting and nutrient enrichment on phytoplankton community structure in a shallow urban lake. Hydrobiologia 571: 77-91.
","pubmedId":"","doi":"10.1007/s10750-006-0230-0"},{"reference":"Paerl HW, Gardner WS, Havens KE, Joyner AR, McCarthy MJ, Newell SE, Qin B, Scott JT. 2016. Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients. Harmful Algae 54: 213-222.
","pubmedId":"","doi":"10.1016/j.hal.2015.09.009"},{"reference":"Paxinos R. 2000. A rapid Utermohl method for estimating algal numbers. Journal of Plankton Research 22: 2255-2262.
","pubmedId":"","doi":"10.1093/plankt/22.12.2255"},{"reference":"Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E. 1993. Alternative equilibria in shallow lakes. Trends in Ecology & Evolution 8: 275-279.
","pubmedId":"","doi":"10.1016/0169-5347(93)90254-M"},{"reference":"Skafi M, Vo Duy S, Munoz G, Dinh QT, Simon DF, Juneau P, Sauvé Sb. 2021. Occurrence of microcystins, anabaenopeptins and other cyanotoxins in fish from a freshwater wildlife reserve impacted by harmful cyanobacterial blooms. Toxicon 194: 44-52.
","pubmedId":"","doi":"10.1016/j.toxicon.2021.02.004"},{"reference":"Trevino-Garrison I, DeMent J, Ahmed F, Haines-Lieber P, Langer T, Ménager H, et al., Carney. 2015. Human Illnesses and Animal Deaths Associated with Freshwater Harmful Algal Blooms—Kansas. Toxins 7: 353-366.
","pubmedId":"","doi":"10.3390/toxins7020353"},{"reference":"Zhou Y, Zhou X, Han R, Xu X, Wang G, Liu X, Bi F, Feng D. 2017. Reproduction capacity of Potamogeton crispus fragments and its role in water purification and algae inhibition in eutrophic lakes. Science of The Total Environment 580: 1421-1428.
","pubmedId":"","doi":"10.1016/j.scitotenv.2016.12.108"}],"title":"METHOD OF REMOVAL OF AQUATIC POND WEED VARIABILTY IMPACTS PRESENCE OF POTENTIALLY TOXIGENIC CYANOBACTERIA
","reviews":[],"curatorReviews":[]},{"id":"bedcc92d-fd75-4578-b087-39aaac55fd0b","decision":"revise","abstract":"Lakes often exist in two alternative stable states: clear waters dominated by submerged aquatic vegetation and turbid states with an abundance of phytoplankton. Management decisions must balance the value of primary producers with recreational use. We monitored the phytoplankton community surrounding removal of invasive Potamogeton crispus, a submerged aquatic perennial. Focus was given to presence of cyanobacteria, which may thrive in the absence of macrophytes by virtue of phosphorus that would otherwise be stored in plant biomass. Results demonstrate that macrophyte removal can lead to an increase in cyanobacteria dominance, with sustained impacts after hand removal.
","acknowledgements":"We are grateful to the lake association members for providing access to the lake and contextual information regarding the lake's history.
","authors":[{"affiliations":["Penn State Berks, Reading, PA, US "],"departments":["Biology"],"credit":["conceptualization","formalAnalysis","methodology","writing_originalDraft"],"email":"sbp20@psu.edu","firstName":"Sarah D","lastName":"Princiotta","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0002-9152-4146"},{"affiliations":["Penn State Schuylkill, Schuylkill Haven, PA, US"],"departments":["Biology"],"credit":["formalAnalysis","dataCuration","methodology","investigation","writing_reviewEditing"],"email":"ejo5215@psu.edu","firstName":"Emily","lastName":"Ostergaard","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["Holy Family University, Philadelphia, PA, US"],"departments":["Biology"],"credit":["conceptualization","formalAnalysis","methodology","investigation","writing_reviewEditing","resources"],"email":"ecarroll2@holyfamily.edu","firstName":"Elizabeth","lastName":"Carroll","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[],"funding":"No funding to report.
","image":{"url":"https://portal.micropublication.org/uploads/e689d99d7dbb8978e802cfaa91cfaf64.JPG"},"imageCaption":"Percentage of the phytoplankton community composed of cyanobacteria in aquatic sites where Potamogeton crispus was removed by hand or mechanically and otherwise left undisturbed (control). The month of June represents pre-treatment conditions. Individual one-way ANOVA tests were conducted within each treatment site to investigate the influence of removal method over time on the percentage of the phytoplankton community composed of cyanobacteria. Letter cases in the figure indicate results of the post-hoc Tukey HSD.
","imageTitle":"Percentage of the phytoplankton community composed of cyanobacteria based on month and form of aquatic plant removal
","methods":"Field collection and Enumeration of Cyanobacteria by Microscopy
The study lake (Zmax 14 m, ~24 ha.) is a natural lake of glacial origin located in Pike County, Pennsylvania. Identifying information, including lake name, are not included here per sampling agreement. The vegetation within the drainage basin is primarily forested and the lake has no inlet streams. Routine lake monitoring from a central location on the study lake report a range of summer Secchi depth from 2.5 – 3 m, epilimnetic chlorophyll from 0.42 – 3.4 mg L-1, and epilimnetic total phosphorus from 4.45 – 5.75 mg L-1. The phytoplankton community is dominated by cyanobacteria genera that can produce cyanotoxins (Limnothrix, Aphanizomenon, Dolichospermum).
Curly-leaf Pond Weed (Potamogeton crispus), a submerged perennial, was first identified in the study lake during 2020-2021, composing ~12 acres of the shoreline in 2023. In July 2024, a combination of hand removal and mechanical harvest removed ~95% of P. crispus from the shoreline. Seven acres were treated by mechanical harvest (site MR) and five acres by hand removal (HR) over a two-day period. The mechanical harvester was able to both cut and collect aquatic macrophytes up to 1.3 m below the surface. Hand removal efforts sought to remove all P. crispus, including the roots, but the macrophyte commonly broke mid-stem. A central location within each site, including an area that was not treated (control), was sampled three times over the course of the study period: one week prior to plant removal (June), and 29 (July) and 56 (August) days after removal.
During each sampling event, triplicate sub-surface (0.50 m) water was collected by Van Dorn bottle, passed through a 153-mm mesh, and stored in 250-mL polycarbonate bottles. Each sample was fixed with a final concentration of 2% Acid Lugol’s and stored in darkness prior to analysis. Samples were concentrated by settling over a 48-hour period after which the remaining ~20 mL was kept for microscopy. A minimum of 300 natural units were identified by light microscopy using a Zeiss Axiovert A1 at 400X magnification using the Utermol method (Paxinos and Mitchell, 2000). Phytoplankton, including cyanobacteria, were identified to genus apart from cells < 5mm diameter that lacked distinctive features, which were grouped as “unidentified nanoplankton.”
Statistical Analysis
All data analysis was conducted in JMP 18.2.2 and the figure was made using R version 4.2.3. Normality and homogeneity of variance were confirmed with a Shapiro Wilk and Levene test, respectively. To meet the assumptions for statistical testing, cyanobacteria abundance and percentage of the community composed of cyanobacteria were log and logit transformed, respectively. To investigate the influence of removal method over time within each site (hand removal, mechanical removal, no removal) a one-way ANOVA with post-hoc Tukey HSD each for cyanobacteria abundance and percentage of the phytoplankton community composed of cyanobacteria. To compare the influence of removal method (hand removal, mechanical removal, no removal) on the percentage of the phytoplankton community composed of cyanobacteria, a one-way ANOVA with post-hoc Tukey HSD was applied for each month after treatment was applied (July, August) with site as the independent variable. Due to significant differences across sites on the abundance of cyanobacteria measured prior to removal method, we did not pursue abundance as a dependent variable for an exploration of the effect of removal method across sites.
","reagents":"","patternDescription":"Despite their evolutionary origins as key aquatic primary producers, dense proliferations, or “blooms” of potentially harmful cyanobacteria are an issue for water quality management in lakes and reservoirs worldwide. The drivers of cyanobacteria dominance and production of toxic secondary metabolites are complex and likely related to environmental conditions associated with global climate change (Paerl et al., 2016). An increased frequency and severity of cyanobacteria blooms are often associated with high surface water temperatures and anthropogenic eutrophication (Kosten et al., 2012; Chapra et al., 2017) Lake managers are now tasked with preventing and responding to cyanobacteria blooms that have been implicated in public health consequences for wildlife, pets, and humans (Backer et al., 2013; Trevino-Garrison et al., 2015; Skafi et al., 2021).
Another threat to freshwater ecosystems is the overgrowth of invasive, submerged aquatic vegetation (Kuiper et al., 2017), which may compromise use of recreational lakes for boating and fishing. Although important to the structure of lake ecosystems as a source of habitat, sediment stability, and nutrient storage (van Donk and van de Bund, 2002; Kovalenko et al., 2010), excess growth of submerged aquatic macrophytes can have negative impacts on water quality when decomposition releases large amounts of phosphorus and consumes dissolved oxygen (Asaeda et al., 2000). There are several methods to manage aquatic macrophytes including removal by either hand or motorized harvesters and chemical treatment with herbicides. Removal of excessive amounts of aquatic macrophytes should be conducted with great caution, as they stabilize the clear water state of shallow lakes (Scheffer et al., 1993). However, it can also be important to balance lake ecosystem health with recreational user preferences.
Aquatic macrophytes may act as natural control agents for cyanobacteria blooms via release of allelopathic compounds (Jasser, 1995), shading, and nutrient competition (Zhou et al., 2017). Field studies that document changes in phytoplankton community structure after removal of aquatic vegetation by various methods are lacking and produce mixed results (Morris et al., 2006; Maredová et al., 2021), especially in lakes that receive a temporally-restricted, rather than continuous, removal of dense stands of aquatic vegetation. We took advantage of lake management action to study the impacts of aquatic plant removal (Potamogeton crispus) by either hand or mechanical harvest on the presence of cyanobacteria. A control was provided by a site in which aquatic plants were undisturbed and present at a low density. We hypothesized that removal of P. crispus, either by hand or mechanical removal, would lead to an increase in cyanobacteria as representatives in the phytoplankton community, with potentially greater impacts on the hand removal site where fragmented plant matter could act as an inadvertent nutrient source. Removal of P. crispus may also enhance cyanobacteria growth due to reduced nutrient competition.
Prior to removal of P. crispus, there was no difference in the percentage of the phytoplankton community composed of cyanobacteria across sites (11% ± 2 SE). However, prior to any initiation of treatment, there were notable differences in the abundance of cyanobacteria by site (F2,3 = 15.41, p = 0.03), with a higher abundance of cyanobacteria in the site designated for mechanical removal relative to that designated for hand removal. Prior to any treatment, the abundance of cyanobacteria at the experimental sites destined for plant removal were not significantly different from the control site.
There was a significant effect of month on the percentage of the community composed of cyanobacteria at both the hand-removal (F2,4 = 24.85, p = 0.0055) and control site (F2,4 = 25.09, p = 0.0054). At the hand-removal site, the percentage of the phytoplankton community composed of cyanobacteria increased over time from 7% to 62%, with significant differences between June, prior to plant removal, and August (p = 0.0048). There was not a significant effect of month on the abundance of cyanobacteria at the hand removal site, suggesting the observed increase in percentage of the phytoplankton community composed of cyanobacteria may result from changes in community structure. It is possible that non-cyanobacteria members of the phytoplankton community did not respond as favorably to conditions associated with hand removal of P. crispus relative to cyanobacteria. Hand removal of P. crispus may have increased the availability of photosynthetic active radiation (PAR) and nutrients available to the phytoplankton, of which cyanobacteria are well-adapted at capitalizing.
In the control site where aquatic plants were undisturbed, there was an initial, although non-significant, decline in the percentage of the community composed of cyanobacteria between pre-treatment conditions in June and July. However, cyanobacteria dominance (%) increased significantly between July and August (p = 0.0047). When considering cyanobacteria abundance at the control site, there was a significant effect of month (F2,4 = 41.75, p = 0.002), where cyanobacteria abundance also increased from July to August (p = 0.002), and the abundance in August was higher than the pre-treatment conditions (p = 0.01). It is worth noting that whereas the cyanobacteria population was kept low between June and July in the control site, there was a positive response of month on non-cyanobacteria members of the phytoplankton community within the same time frame. These results are indicative of the potentially negative allelopathic interactions between P. crispus and cyanobacteria or at least a differential response between the phytoplankton community to the presence of P. crispus.
In July but not August, there was a significant effect of site on the percentage of the community composed of cyanobacteria (F2,3 = 13.27, p = 0.03). A higher percentage of cyanobacteria were observed in the hand and mechanical removal sites relative to the control site where aquatic plants were undisturbed. Approximately one month after treatment, cross-site differences in cyanobacteria dominance (%) were no longer apparent. It may be interpreted that presence of excessive P. crispus had a negative impact on cyanobacteria that was temporarily relieved after removal of the aquatic macrophyte by either hand or mechanical measures. Our methodological approach does not allow us to interpret if this is due to regrowth of P. crispus, decomposition of fragmented plant material, or natural differences in cyanobacteria dominance that may occur within a single ecosystem. We suggest future studies to follow impacts of P. crispus removal through the fall germination period. This work provides a basis for targeted investigations that seek to balance invasive plant management with ecological health.
","references":[{"reference":"Asaeda T, Trung VK, Manatunge J. 2000. Modeling the effects of macrophyte growth and decomposition on the nutrient budget in Shallow Lakes. Aquatic Botany 68: 217-237.
","pubmedId":"","doi":"10.1016/S0304-3770(00)00123-6"},{"reference":"Backer L, Landsberg J, Miller M, Keel K, Taylor T. 2013. Canine Cyanotoxin Poisonings in the United States (1920s–2012): Review of Suspected and Confirmed Cases from Three Data Sources. Toxins 5: 1597-1628.
","pubmedId":"","doi":"10.3390/toxins5091597"},{"reference":"Chapra SC, Boehlert B, Fant C, Bierman VJ, Henderson J, Mills D, et al., Paerl. 2017. Climate Change Impacts on Harmful Algal Blooms in U.S. Freshwaters: A Screening-Level Assessment. Environmental Science & Technology 51: 8933-8943.
","pubmedId":"","doi":"10.1021/acs.est.7b01498"},{"reference":"van Donk E, van de Bund WJ. 2002. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany 72: 261-274.
","pubmedId":"","doi":"10.1016/S0304-3770(01)00205-4"},{"reference":"Jasser I. 1995. The influence of macrophytes on a phytoplankton community in experimental conditions. Hydrobiologia 306: 21-32.
","pubmedId":"","doi":"10.1007/BF00007855"},{"reference":"Kosten S, Huszar VLM, Bécares E, Costa LS, van Donk E, Hansson LA, et al., Scheffer. 2011. Warmer climates boost cyanobacterial dominance in shallow lakes. Global Change Biology 18: 118-126.
","pubmedId":"","doi":"10.1111/j.1365-2486.2011.02488.x"},{"reference":"Kovalenko KE, Dibble ED, Slade JG. 2010. Community effects of invasive macrophyte control: role of invasive plant abundance and habitat complexity. Journal of Applied Ecology 47: 318-328.
","pubmedId":"","doi":"10.1111/j.1365-2664.2009.01768.x"},{"reference":"Kuiper JJ, Verhofstad MJJM, Louwers ELM, Bakker ES, Brederveld RJ, van Gerven LPA, et al., Mooij. 2017. Mowing Submerged Macrophytes in Shallow Lakes with Alternative Stable States: Battling the Good Guys?. Environmental Management 59: 619-634.
","pubmedId":"","doi":"10.1007/s00267-016-0811-2"},{"reference":"Maredová N, Altman J, Kaštovský J. 2021. The effects of macrophytes on the growth of bloom-forming cyanobacteria: Systematic review and experiment. Science of The Total Environment 792: 148413.
","pubmedId":"","doi":"10.1016/j.scitotenv.2021.148413"},{"reference":"Morris K, Bailey PCE, Boon PI, Hughes L. 2006. Effects of plant harvesting and nutrient enrichment on phytoplankton community structure in a shallow urban lake. Hydrobiologia 571: 77-91.
","pubmedId":"","doi":"10.1007/s10750-006-0230-0"},{"reference":"Paerl HW, Gardner WS, Havens KE, Joyner AR, McCarthy MJ, Newell SE, Qin B, Scott JT. 2016. Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients. Harmful Algae 54: 213-222.
","pubmedId":"","doi":"10.1016/j.hal.2015.09.009"},{"reference":"Paxinos R. 2000. A rapid Utermohl method for estimating algal numbers. Journal of Plankton Research 22: 2255-2262.
","pubmedId":"","doi":"10.1093/plankt/22.12.2255"},{"reference":"Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E. 1993. Alternative equilibria in shallow lakes. Trends in Ecology & Evolution 8: 275-279.
","pubmedId":"","doi":"10.1016/0169-5347(93)90254-M"},{"reference":"Skafi M, Vo Duy S, Munoz G, Dinh QT, Simon DF, Juneau P, Sauvé Sb. 2021. Occurrence of microcystins, anabaenopeptins and other cyanotoxins in fish from a freshwater wildlife reserve impacted by harmful cyanobacterial blooms. Toxicon 194: 44-52.
","pubmedId":"","doi":"10.1016/j.toxicon.2021.02.004"},{"reference":"Trevino-Garrison I, DeMent J, Ahmed F, Haines-Lieber P, Langer T, Ménager H, et al., Carney. 2015. Human Illnesses and Animal Deaths Associated with Freshwater Harmful Algal Blooms—Kansas. Toxins 7: 353-366.
","pubmedId":"","doi":"10.3390/toxins7020353"},{"reference":"Zhou Y, Zhou X, Han R, Xu X, Wang G, Liu X, Bi F, Feng D. 2017. Reproduction capacity of Potamogeton crispus fragments and its role in water purification and algae inhibition in eutrophic lakes. Science of The Total Environment 580: 1421-1428.
","pubmedId":"","doi":"10.1016/j.scitotenv.2016.12.108"}],"title":"METHOD OF REMOVAL OF AQUATIC POND WEED VARIABILTY IMPACTS PRESENCE OF POTENTIALLY TOXIGENIC CYANOBACTERIA
","reviews":[{"reviewer":{"displayName":"Keith Fritschie"},"openAcknowledgement":false,"status":{"submitted":true}}],"curatorReviews":[]},{"id":"4f549cab-6b97-4f01-9fcd-681224395b48","decision":"accept","abstract":"Lakes often exist in two alternative stable states: clear waters dominated by submerged aquatic vegetation and turbid states with an abundance of phytoplankton. Management decisions must balance the value of primary producers with recreational use. We monitored the phytoplankton community surrounding removal of invasive Potamogeton crispus, a submerged aquatic perennial. Focus was given to presence of cyanobacteria, which may thrive in the absence of macrophytes by virtue of phosphorus that would otherwise be stored in plant biomass. Results demonstrate that macrophyte removal can lead to an increase in cyanobacteria dominance, with sustained impacts after hand removal.
","acknowledgements":"We are grateful to the lake association members for providing access to the lake and contextual information regarding the lake's history.
","authors":[{"affiliations":["Penn State Berks, Reading, PA, US "],"departments":["Biology"],"credit":["conceptualization","formalAnalysis","methodology","writing_originalDraft"],"email":"sbp20@psu.edu","firstName":"Sarah D","lastName":"Princiotta","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0002-9152-4146"},{"affiliations":["Penn State Schuylkill, Schuylkill Haven, PA, US"],"departments":["Biology"],"credit":["formalAnalysis","dataCuration","methodology","investigation","writing_reviewEditing"],"email":"ejo5215@psu.edu","firstName":"Emily","lastName":"Ostergaard","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["Holy Family University, Philadelphia, PA, US"],"departments":["Biology"],"credit":["conceptualization","formalAnalysis","methodology","investigation","writing_reviewEditing","resources"],"email":"ecarroll2@holyfamily.edu","firstName":"Elizabeth","lastName":"Carroll","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[],"funding":"No funding to report.
","image":{"url":"https://portal.micropublication.org/uploads/e689d99d7dbb8978e802cfaa91cfaf64.JPG"},"imageCaption":"Percentage of the phytoplankton community composed of cyanobacteria in aquatic sites where Potamogeton crispus was removed by hand or mechanically and otherwise left undisturbed (control). The month of June represents pre-treatment conditions. Individual one-way ANOVA tests were conducted within each treatment site to investigate the influence of removal method over time on the percentage of the phytoplankton community composed of cyanobacteria. Letter cases in the figure indicate results of the post-hoc Tukey HSD.
","imageTitle":"Percentage of the phytoplankton community composed of cyanobacteria based on month and form of aquatic plant removal
","methods":"Field collection and Enumeration of Cyanobacteria by Microscopy
The study lake (Zmax 14 m, ~24 ha.) is a natural lake of glacial origin located in Pike County, Pennsylvania. Identifying information, including lake name, are not included here per sampling agreement. The vegetation within the drainage basin is primarily forested and the lake has no inlet streams. Routine lake monitoring from a central location on the study lake report a range of summer Secchi depth from 2.5 – 3 m, epilimnetic chlorophyll from 0.42 – 3.4 mg L-1, and epilimnetic total phosphorus from 4.45 – 5.75 mg L-1. The phytoplankton community is dominated by cyanobacteria genera that can produce cyanotoxins (Limnothrix, Aphanizomenon, Dolichospermum).
Curly-leaf Pond Weed (Potamogeton crispus), a submerged perennial, was first identified in the study lake during 2020-2021, composing ~12 acres of the shoreline in 2023. In July 2024, a combination of hand removal and mechanical harvest removed ~95% of P. crispus from the shoreline. Seven acres were treated by mechanical harvest (site MR) and five acres by hand removal (HR) over a two-day period. The mechanical harvester was able to both cut and collect aquatic macrophytes up to 1.3 m below the surface. Hand removal efforts sought to remove all P. crispus, including the roots, but the macrophyte commonly broke mid-stem. A central location within each site, including an area that was not treated (control), was sampled three times over the course of the study period: one week prior to plant removal (June), and 29 (July) and 56 (August) days after removal.
During each sampling event, triplicate sub-surface (0.5 m) water was collected by Van Dorn bottle along a transect, passed through a 153-mm mesh, and stored in 250-mL polycarbonate bottles. Each sample was fixed with a final concentration of 2% Acid Lugol’s and stored in darkness prior to analysis. Samples were concentrated by settling over a 48-hour period after which the remaining ~20 mL was kept for microscopy. A minimum of 300 natural units were identified by light microscopy using a Zeiss Axiovert A1 at 400X magnification using the Utermol method (Paxinos and Mitchell, 2000). Phytoplankton, including cyanobacteria, were identified to genus apart from cells < 5mm diameter that lacked distinctive features, which were grouped as “unidentified nanoplankton.”
Statistical Analysis
All data analysis was conducted in JMP 18.2.2 and the figure was made using R version 4.2.3. Normality and homogeneity of variance were confirmed with a Shapiro Wilk and Levene test, respectively. To meet the assumptions for statistical testing, cyanobacteria abundance and percentage of the community composed of cyanobacteria were log and logit transformed, respectively. To investigate the influence of removal method over time within each site (hand removal, mechanical removal, no removal) a one-way ANOVA with post-hoc Tukey HSD each for cyanobacteria abundance and percentage of the phytoplankton community composed of cyanobacteria. To compare the influence of removal method (hand removal, mechanical removal, no removal) on the percentage of the phytoplankton community composed of cyanobacteria, a one-way ANOVA with post-hoc Tukey HSD was applied for each month after treatment was applied (July, August) with site as the independent variable. Due to significant differences across sites on the abundance of cyanobacteria measured prior to removal method, we did not pursue abundance as a dependent variable for an exploration of the effect of removal method across sites.
","reagents":"","patternDescription":"Despite their evolutionary origins as key aquatic primary producers, dense proliferations, or “blooms” of potentially harmful cyanobacteria are an issue for water quality management in lakes and reservoirs worldwide. The drivers of cyanobacteria dominance and production of toxic secondary metabolites are complex and likely related to environmental conditions associated with global climate change (Paerl et al., 2016). An increased frequency and severity of cyanobacteria blooms are often associated with high surface water temperatures and anthropogenic eutrophication (Kosten et al., 2012; Chapra et al., 2017) Lake managers are now tasked with preventing and responding to cyanobacteria blooms that have been implicated in public health consequences for wildlife, pets, and humans (Backer et al., 2013; Trevino-Garrison et al., 2015; Skafi et al., 2021).
Another threat to freshwater ecosystems is the overgrowth of invasive, submerged aquatic vegetation (Kuiper et al., 2017), which may compromise use of recreational lakes for boating and fishing. Although important to the structure of lake ecosystems as a source of habitat, sediment stability, and nutrient storage (van Donk and van de Bund, 2002; Kovalenko et al., 2010), excess growth of submerged aquatic macrophytes can have negative impacts on water quality when decomposition releases large amounts of phosphorus and consumes dissolved oxygen (Asaeda et al., 2000). There are several methods to manage aquatic macrophytes including removal by either hand or motorized harvesters and chemical treatment with herbicides. Removal of excessive amounts of aquatic macrophytes should be conducted with great caution, as they stabilize the clear water state of shallow lakes (Scheffer et al., 1993). However, it can also be important to balance lake ecosystem health with recreational user preferences.
Aquatic macrophytes may act as natural control agents for cyanobacteria blooms via release of allelopathic compounds (Jasser, 1995), shading, and nutrient competition (Zhou et al., 2017). Field studies that document changes in phytoplankton community structure after removal of aquatic vegetation by various methods are lacking and produce mixed results (Morris et al., 2006; Maredová et al., 2021), especially in lakes that receive a temporally-restricted, rather than continuous, removal of dense stands of aquatic vegetation. We took advantage of lake management action to study the impacts of aquatic plant removal (Potamogeton crispus) by either hand or mechanical harvest on the presence of cyanobacteria. A control was provided by a site in which aquatic plants were undisturbed and present at a low density. We hypothesized that removal of P. crispus, either by hand or mechanical removal, would lead to an increase in cyanobacteria as representatives in the phytoplankton community, with potentially greater impacts on the hand removal site where fragmented plant matter could act as an inadvertent nutrient source. Removal of P. crispus may also enhance cyanobacteria growth due to reduced nutrient competition.
Prior to removal of P. crispus, there was no difference in the percentage of the phytoplankton community composed of cyanobacteria across sites (11% ± 2 SE). However, prior to any initiation of treatment, there were notable differences in the abundance of cyanobacteria by site (F2,3 = 15.41, p = 0.03), with a higher abundance of cyanobacteria in the site designated for mechanical removal relative to that designated for hand removal. Prior to any treatment, the abundance of cyanobacteria at the experimental sites destined for plant removal were not significantly different from the control site.
There was a significant effect of month on the percentage of the community composed of cyanobacteria at both the hand-removal (F2,4 = 24.85, p = 0.0055) and control site (F2,4 = 25.09, p = 0.0054). At the hand-removal site, the percentage of the phytoplankton community composed of cyanobacteria increased over time from 7% to 62%, with significant differences between June, prior to plant removal, and August (p = 0.0048). There was not a significant effect of month on the abundance of cyanobacteria at the hand removal site, suggesting the observed increase in percentage of the phytoplankton community composed of cyanobacteria may result from changes in community structure. It is possible that non-cyanobacteria members of the phytoplankton community did not respond as favorably to conditions associated with hand removal of P. crispus relative to cyanobacteria. Hand removal of P. crispus may have increased the availability of photosynthetic active radiation (PAR) and nutrients available to the phytoplankton, of which cyanobacteria are well-adapted at capitalizing.
In the control site where aquatic plants were undisturbed, there was an initial, although non-significant, decline in the percentage of the community composed of cyanobacteria between pre-treatment conditions in June and July. However, cyanobacteria dominance (%) increased significantly between July and August (p = 0.0047). When considering cyanobacteria abundance at the control site, there was a significant effect of month (F2,4 = 41.75, p = 0.002), where cyanobacteria abundance also increased from July to August (p = 0.002), and the abundance in August was higher than the pre-treatment conditions (p = 0.01). It is worth noting that whereas the cyanobacteria population was kept low between June and July in the control site, there was a positive response of month on non-cyanobacteria members of the phytoplankton community within the same time frame. These results are indicative of the potentially negative allelopathic interactions between P. crispus and cyanobacteria or at least a differential response between the phytoplankton community to the presence of P. crispus.
In July but not August, there was a significant effect of site on the percentage of the community composed of cyanobacteria (F2,3 = 13.27, p = 0.03). A higher percentage of cyanobacteria were observed in the hand and mechanical removal sites relative to the control site where aquatic plants were undisturbed. Approximately one month after treatment, cross-site differences in cyanobacteria dominance (%) were no longer apparent. It may be interpreted that presence of excessive P. crispus had a negative impact on cyanobacteria that was temporarily relieved after removal of the aquatic macrophyte by either hand or mechanical measures. Our methodological approach does not allow us to interpret if this is due to regrowth of P. crispus, decomposition of fragmented plant material, or natural differences in cyanobacteria dominance that may occur within a single ecosystem. We suggest future studies to follow impacts of P. crispus removal through the fall germination period. This work provides a basis for targeted investigations that seek to balance invasive plant management with ecological health.
","references":[{"reference":"Asaeda T, Trung VK, Manatunge J. 2000. Modeling the effects of macrophyte growth and decomposition on the nutrient budget in Shallow Lakes. Aquatic Botany 68: 217-237.
","pubmedId":"","doi":"10.1016/S0304-3770(00)00123-6"},{"reference":"Backer L, Landsberg J, Miller M, Keel K, Taylor T. 2013. Canine Cyanotoxin Poisonings in the United States (1920s–2012): Review of Suspected and Confirmed Cases from Three Data Sources. Toxins 5: 1597-1628.
","pubmedId":"","doi":"10.3390/toxins5091597"},{"reference":"Chapra SC, Boehlert B, Fant C, Bierman VJ, Henderson J, Mills D, et al., Paerl. 2017. Climate Change Impacts on Harmful Algal Blooms in U.S. Freshwaters: A Screening-Level Assessment. Environmental Science & Technology 51: 8933-8943.
","pubmedId":"","doi":"10.1021/acs.est.7b01498"},{"reference":"van Donk E, van de Bund WJ. 2002. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany 72: 261-274.
","pubmedId":"","doi":"10.1016/S0304-3770(01)00205-4"},{"reference":"Jasser I. 1995. The influence of macrophytes on a phytoplankton community in experimental conditions. Hydrobiologia 306: 21-32.
","pubmedId":"","doi":"10.1007/BF00007855"},{"reference":"Kosten S, Huszar VLM, Bécares E, Costa LS, van Donk E, Hansson LA, et al., Scheffer. 2011. Warmer climates boost cyanobacterial dominance in shallow lakes. Global Change Biology 18: 118-126.
","pubmedId":"","doi":"10.1111/j.1365-2486.2011.02488.x"},{"reference":"Kovalenko KE, Dibble ED, Slade JG. 2010. Community effects of invasive macrophyte control: role of invasive plant abundance and habitat complexity. Journal of Applied Ecology 47: 318-328.
","pubmedId":"","doi":"10.1111/j.1365-2664.2009.01768.x"},{"reference":"Kuiper JJ, Verhofstad MJJM, Louwers ELM, Bakker ES, Brederveld RJ, van Gerven LPA, et al., Mooij. 2017. Mowing Submerged Macrophytes in Shallow Lakes with Alternative Stable States: Battling the Good Guys?. Environmental Management 59: 619-634.
","pubmedId":"","doi":"10.1007/s00267-016-0811-2"},{"reference":"Maredová N, Altman J, Kaštovský J. 2021. The effects of macrophytes on the growth of bloom-forming cyanobacteria: Systematic review and experiment. Science of The Total Environment 792: 148413.
","pubmedId":"","doi":"10.1016/j.scitotenv.2021.148413"},{"reference":"Morris K, Bailey PCE, Boon PI, Hughes L. 2006. Effects of plant harvesting and nutrient enrichment on phytoplankton community structure in a shallow urban lake. Hydrobiologia 571: 77-91.
","pubmedId":"","doi":"10.1007/s10750-006-0230-0"},{"reference":"Paerl HW, Gardner WS, Havens KE, Joyner AR, McCarthy MJ, Newell SE, Qin B, Scott JT. 2016. Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients. Harmful Algae 54: 213-222.
","pubmedId":"","doi":"10.1016/j.hal.2015.09.009"},{"reference":"Paxinos R. 2000. A rapid Utermohl method for estimating algal numbers. Journal of Plankton Research 22: 2255-2262.
","pubmedId":"","doi":"10.1093/plankt/22.12.2255"},{"reference":"Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E. 1993. Alternative equilibria in shallow lakes. Trends in Ecology & Evolution 8: 275-279.
","pubmedId":"","doi":"10.1016/0169-5347(93)90254-M"},{"reference":"Skafi M, Vo Duy S, Munoz G, Dinh QT, Simon DF, Juneau P, Sauvé Sb. 2021. Occurrence of microcystins, anabaenopeptins and other cyanotoxins in fish from a freshwater wildlife reserve impacted by harmful cyanobacterial blooms. Toxicon 194: 44-52.
","pubmedId":"","doi":"10.1016/j.toxicon.2021.02.004"},{"reference":"Trevino-Garrison I, DeMent J, Ahmed F, Haines-Lieber P, Langer T, Ménager H, et al., Carney. 2015. Human Illnesses and Animal Deaths Associated with Freshwater Harmful Algal Blooms—Kansas. Toxins 7: 353-366.
","pubmedId":"","doi":"10.3390/toxins7020353"},{"reference":"Zhou Y, Zhou X, Han R, Xu X, Wang G, Liu X, Bi F, Feng D. 2017. Reproduction capacity of Potamogeton crispus fragments and its role in water purification and algae inhibition in eutrophic lakes. Science of The Total Environment 580: 1421-1428.
","pubmedId":"","doi":"10.1016/j.scitotenv.2016.12.108"}],"title":"METHOD OF REMOVAL OF AQUATIC POND WEED VARIABILTY IMPACTS PRESENCE OF POTENTIALLY TOXIGENIC CYANOBACTERIA
","reviews":[{"reviewer":{"displayName":"Keith Fritschie"},"openAcknowledgement":false,"status":{"submitted":true}}],"curatorReviews":[]},{"id":"6a9050dd-c396-4fcc-9d44-fb54b4f2dc1d","decision":"edit","abstract":"Lakes often exist in two alternative stable states: clear waters dominated by submerged aquatic vegetation and turbid states with an abundance of phytoplankton. Management decisions must balance the value of primary producers with recreational use. We monitored the phytoplankton community surrounding removal of invasive Potamogeton crispus, a submerged aquatic perennial. Focus was given to presence of cyanobacteria, which may thrive in the absence of macrophytes by virtue of phosphorus that would otherwise be stored in plant biomass. Results demonstrate that macrophyte removal can lead to an increase in cyanobacteria dominance, with sustained impacts after hand removal.
","acknowledgements":"We are grateful to the lake association members for providing access to the lake and contextual information regarding the lake's history.
","authors":[{"affiliations":["Penn State Berks, Reading, PA, US "],"departments":["Biology"],"credit":["conceptualization","formalAnalysis","methodology","writing_originalDraft"],"email":"sbp20@psu.edu","firstName":"Sarah D","lastName":"Princiotta","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0002-9152-4146"},{"affiliations":["Penn State Schuylkill, Schuylkill Haven, PA, US"],"departments":["Biology"],"credit":["formalAnalysis","dataCuration","methodology","investigation","writing_reviewEditing"],"email":"ostergaardemily0@gmail.com","firstName":"Emily","lastName":"Ostergaard","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["Holy Family University, Philadelphia, PA, US"],"departments":["Biology"],"credit":["conceptualization","formalAnalysis","methodology","investigation","writing_reviewEditing","resources"],"email":"ecarroll2@holyfamily.edu","firstName":"Elizabeth","lastName":"Carroll","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[],"funding":"No funding to report.
","image":{"url":"https://portal.micropublication.org/uploads/e689d99d7dbb8978e802cfaa91cfaf64.JPG"},"imageCaption":"Percentage of the phytoplankton community composed of cyanobacteria in aquatic sites where Potamogeton crispus was removed by hand or mechanically and otherwise left undisturbed (control). The month of June represents pre-treatment conditions. Individual one-way ANOVA tests were conducted within each treatment site to investigate the influence of removal method over time on the percentage of the phytoplankton community composed of cyanobacteria. Letter cases in the figure indicate results of the post-hoc Tukey HSD.
","imageTitle":"Percentage of the phytoplankton community composed of cyanobacteria based on month and form of aquatic plant removal
","methods":"Field collection and Enumeration of Cyanobacteria by Microscopy
The study lake (Zmax 14 m, ~24 ha.) is a natural lake of glacial origin located in Pike County, Pennsylvania. Identifying information, including lake name, are not included here per sampling agreement. The vegetation within the drainage basin is primarily forested and the lake has no inlet streams. Routine lake monitoring from a central location on the study lake report a range of summer Secchi depth from 2.5 – 3 m, epilimnetic chlorophyll from 0.42 – 3.4 mg L-1, and epilimnetic total phosphorus from 4.45 – 5.75 mg L-1. The phytoplankton community is dominated by cyanobacteria genera that can produce cyanotoxins (Limnothrix, Aphanizomenon, Dolichospermum).
Curly-leaf Pond Weed (Potamogeton crispus), a submerged perennial, was first identified in the study lake during 2020-2021, composing ~12 acres of the shoreline in 2023. In July 2024, a combination of hand removal and mechanical harvest removed ~95% of P. crispus from the shoreline. Seven acres were treated by mechanical harvest and five acres by hand removal over a two-day period. The mechanical harvester was able to both cut and collect aquatic macrophytes up to 1.3 m below the surface. Hand removal efforts sought to remove all P. crispus, including the roots, but the macrophyte commonly broke mid-stem. A central location within each site, including an area that was not treated (control), was sampled three times over the course of the study period: one week prior to plant removal (June), and 29 (July) and 56 (August) days after removal.
During each sampling event, triplicate sub-surface (0.5 m) water was collected by Van Dorn bottle along a transect, passed through a 153-mm mesh, and stored in 250-mL polycarbonate bottles. Each sample was fixed with a final concentration of 2% Acid Lugol’s and stored in darkness prior to analysis. Samples were concentrated by settling over a 48-hour period after which the remaining ~20 mL was kept for microscopy. A minimum of 300 natural units were identified by light microscopy using a Zeiss Axiovert A1 at 400X magnification using the Utermol method (Paxinos and Mitchell, 2000). Phytoplankton, including cyanobacteria, were identified to genus apart from cells < 5mm diameter that lacked distinctive features, which were grouped as “unidentified nanoplankton.”
Statistical Analysis
All data analysis was conducted in JMP 18.2.2 and the figure was made using R version 4.2.3. Normality and homogeneity of variance were confirmed with a Shapiro Wilk and Levene test, respectively. To meet the assumptions for statistical testing, cyanobacteria abundance and percentage of the community composed of cyanobacteria were log and logit transformed, respectively. To investigate the influence of removal method over time within each site (hand removal, mechanical removal, no removal) a one-way ANOVA with post-hoc Tukey HSD each for cyanobacteria abundance and percentage of the phytoplankton community composed of cyanobacteria. To compare the influence of removal method (hand removal, mechanical removal, no removal) on the percentage of the phytoplankton community composed of cyanobacteria, a one-way ANOVA with post-hoc Tukey HSD was applied for each month after treatment was applied (July, August) with site as the independent variable. Due to significant differences across sites on the abundance of cyanobacteria measured prior to removal method, we did not pursue abundance as a dependent variable for an exploration of the effect of removal method across sites.
","reagents":"","patternDescription":"Despite their evolutionary origins as key aquatic primary producers, dense proliferations, or “blooms” of potentially harmful cyanobacteria are an issue for water quality management in lakes and reservoirs worldwide. The drivers of cyanobacteria dominance and production of toxic secondary metabolites are complex and likely related to environmental conditions associated with global climate change (Paerl et al., 2016). An increased frequency and severity of cyanobacteria blooms are often associated with high surface water temperatures and anthropogenic eutrophication (Kosten et al., 2012; Chapra et al., 2017) Lake managers are tasked with preventing and responding to cyanobacteria blooms that have been implicated in public health consequences for wildlife, pets, and humans (Backer et al., 2013; Trevino-Garrison et al., 2015; Skafi et al., 2021).
Another threat to freshwater ecosystems is the overgrowth of invasive, submerged aquatic vegetation (Kuiper et al., 2017), which may compromise use of recreational lakes for boating and fishing. Although important to the structure of lake ecosystems as a source of habitat, sediment stability, and nutrient storage (van Donk and van de Bund, 2002; Kovalenko et al., 2010), excess growth of submerged aquatic macrophytes can have negative impacts on water quality when decomposition releases large amounts of phosphorus and consumes dissolved oxygen (Asaeda et al., 2000). There are several methods to manage aquatic macrophytes including removal by either hand or motorized harvesters and chemical treatment with herbicides. Removal of excessive amounts of aquatic macrophytes should be conducted with great caution, as they stabilize the clear water state of shallow lakes (Scheffer et al., 1993). However, it can also be important to balance lake ecosystem health with recreational user preferences.
Aquatic macrophytes may act as natural control agents for cyanobacteria blooms via release of allelopathic compounds (Jasser, 1995), shading, and nutrient competition (Zhou et al., 2017). Field studies that document changes in phytoplankton community structure after removal of aquatic vegetation by various methods are lacking and produce mixed results (Morris et al., 2006; Maredová et al., 2021), especially in lakes that receive a temporally restricted, rather than continuous, removal of dense stands of aquatic vegetation. We took advantage of lake management action to study the impacts of aquatic plant removal (Potamogeton crispus) by either hand or mechanical harvest on the presence of cyanobacteria. A control was provided by a site in which aquatic plants were undisturbed and present at a low density. We hypothesized that removal of P. crispus, either by hand or mechanical removal, would lead to an increase in cyanobacteria as representatives in the phytoplankton community, with potentially greater impacts on the hand removal site where fragmented plant matter could act as an inadvertent nutrient source. Removal of P. crispus may also enhance cyanobacteria growth due to reduced nutrient competition.
Prior to removal of P. crispus, there were no differences in the percentage of the phytoplankton community composed of cyanobacteria across sites (11% ± 2 SE). However, prior to any initiation of treatment, there were notable differences in the abundance of cyanobacteria by site (F2,3 = 15.41, p = 0.03), with a higher abundance of cyanobacteria in the site designated for mechanical removal relative to that designated for hand removal. Additionally, the abundance of cyanobacteria at the experimental sites destined for plant removal were not significantly different from the control site.
There was a significant effect of month on the percentage of the community composed of cyanobacteria at both the hand-removal (F2,4 = 24.85, p = 0.0055) and control site (F2,4 = 25.09, p = 0.0054). At the hand-removal site, the percentage of the phytoplankton community composed of cyanobacteria increased over time from 7% to 62%, with significant differences between June, prior to plant removal, and August (p = 0.0048). There was not a significant effect of month on the abundance of cyanobacteria at the hand removal site, suggesting the observed increase in percentage of the phytoplankton community composed of cyanobacteria may result from changes in community structure. It is possible that non-cyanobacteria members of the phytoplankton community did not respond as favorably to conditions associated with hand removal of P. crispus relative to cyanobacteria. Hand removal of P. crispus may have increased the availability of photosynthetic active radiation (PAR) and nutrients available to the phytoplankton, of which cyanobacteria are well-adapted at capitalizing.
In the control site where aquatic plants were undisturbed, there was an initial, although non-significant, decline in the percentage of the community composed of cyanobacteria between pre-treatment conditions in June and July. However, cyanobacteria dominance (%) increased significantly between July and August (p = 0.0047). When considering cyanobacteria abundance at the control site, there was a significant effect of month (F2,4 = 41.75, p = 0.002), where cyanobacteria abundance also increased from July to August (p = 0.002), and the abundance in August was higher than the pre-treatment conditions (p = 0.01). It is worth noting that whereas the cyanobacteria population was kept low between June and July in the control site, there was a positive response of month on non-cyanobacteria members of the phytoplankton community within the same time frame. These results are indicative of the potentially negative allelopathic interactions between P. crispus and cyanobacteria or at least a differential response between the phytoplankton community to the presence of P. crispus.
In July but not August, there was a significant effect of site on the percentage of the community composed of cyanobacteria (F2,3 = 13.27, p = 0.03). A higher percentage of cyanobacteria were observed in the hand and mechanical removal sites relative to the control site where aquatic plants were undisturbed. Approximately one month after treatment, cross-site differences in cyanobacteria dominance (%) were no longer apparent. It may be interpreted that presence of excessive P. crispus had a negative impact on cyanobacteria that was temporarily relieved after removal of the aquatic macrophyte by either hand or mechanical measures. Our methodological approach does not allow us to interpret if this is due to regrowth of P. crispus, decomposition of fragmented plant material, or natural differences in cyanobacteria dominance that may occur within a single ecosystem. We suggest future studies to follow impacts of P. crispus removal through the fall germination period. This work provides a basis for targeted investigations that seek to balance invasive plant management with ecological health.
","references":[{"reference":"Asaeda T, Trung VK, Manatunge J. 2000. Modeling the effects of macrophyte growth and decomposition on the nutrient budget in Shallow Lakes. Aquatic Botany 68: 217-237.
","pubmedId":"","doi":"10.1016/S0304-3770(00)00123-6"},{"reference":"Backer L, Landsberg J, Miller M, Keel K, Taylor T. 2013. Canine Cyanotoxin Poisonings in the United States (1920s–2012): Review of Suspected and Confirmed Cases from Three Data Sources. Toxins 5: 1597-1628.
","pubmedId":"","doi":"10.3390/toxins5091597"},{"reference":"Chapra SC, Boehlert B, Fant C, Bierman VJ, Henderson J, Mills D, et al., Paerl. 2017. Climate Change Impacts on Harmful Algal Blooms in U.S. Freshwaters: A Screening-Level Assessment. Environmental Science & Technology 51: 8933-8943.
","pubmedId":"","doi":"10.1021/acs.est.7b01498"},{"reference":"van Donk E, van de Bund WJ. 2002. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany 72: 261-274.
","pubmedId":"","doi":"10.1016/S0304-3770(01)00205-4"},{"reference":"Jasser I. 1995. The influence of macrophytes on a phytoplankton community in experimental conditions. Hydrobiologia 306: 21-32.
","pubmedId":"","doi":"10.1007/BF00007855"},{"reference":"Kosten S, Huszar VLM, Bécares E, Costa LS, van Donk E, Hansson LA, et al., Scheffer. 2011. Warmer climates boost cyanobacterial dominance in shallow lakes. Global Change Biology 18: 118-126.
","pubmedId":"","doi":"10.1111/j.1365-2486.2011.02488.x"},{"reference":"Kovalenko KE, Dibble ED, Slade JG. 2010. Community effects of invasive macrophyte control: role of invasive plant abundance and habitat complexity. Journal of Applied Ecology 47: 318-328.
","pubmedId":"","doi":"10.1111/j.1365-2664.2009.01768.x"},{"reference":"Kuiper JJ, Verhofstad MJJM, Louwers ELM, Bakker ES, Brederveld RJ, van Gerven LPA, et al., Mooij. 2017. Mowing Submerged Macrophytes in Shallow Lakes with Alternative Stable States: Battling the Good Guys?. Environmental Management 59: 619-634.
","pubmedId":"","doi":"10.1007/s00267-016-0811-2"},{"reference":"Maredová N, Altman J, Kaštovský J. 2021. The effects of macrophytes on the growth of bloom-forming cyanobacteria: Systematic review and experiment. Science of The Total Environment 792: 148413.
","pubmedId":"","doi":"10.1016/j.scitotenv.2021.148413"},{"reference":"Morris K, Bailey PCE, Boon PI, Hughes L. 2006. Effects of plant harvesting and nutrient enrichment on phytoplankton community structure in a shallow urban lake. Hydrobiologia 571: 77-91.
","pubmedId":"","doi":"10.1007/s10750-006-0230-0"},{"reference":"Paerl HW, Gardner WS, Havens KE, Joyner AR, McCarthy MJ, Newell SE, Qin B, Scott JT. 2016. Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients. Harmful Algae 54: 213-222.
","pubmedId":"","doi":"10.1016/j.hal.2015.09.009"},{"reference":"Paxinos R. 2000. A rapid Utermohl method for estimating algal numbers. Journal of Plankton Research 22: 2255-2262.
","pubmedId":"","doi":"10.1093/plankt/22.12.2255"},{"reference":"Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E. 1993. Alternative equilibria in shallow lakes. Trends in Ecology & Evolution 8: 275-279.
","pubmedId":"","doi":"10.1016/0169-5347(93)90254-M"},{"reference":"Skafi M, Vo Duy S, Munoz G, Dinh QT, Simon DF, Juneau P, Sauvé Sb. 2021. Occurrence of microcystins, anabaenopeptins and other cyanotoxins in fish from a freshwater wildlife reserve impacted by harmful cyanobacterial blooms. Toxicon 194: 44-52.
","pubmedId":"","doi":"10.1016/j.toxicon.2021.02.004"},{"reference":"Trevino-Garrison I, DeMent J, Ahmed F, Haines-Lieber P, Langer T, Ménager H, et al., Carney. 2015. Human Illnesses and Animal Deaths Associated with Freshwater Harmful Algal Blooms—Kansas. Toxins 7: 353-366.
","pubmedId":"","doi":"10.3390/toxins7020353"},{"reference":"Zhou Y, Zhou X, Han R, Xu X, Wang G, Liu X, Bi F, Feng D. 2017. Reproduction capacity of Potamogeton crispus fragments and its role in water purification and algae inhibition in eutrophic lakes. Science of The Total Environment 580: 1421-1428.
","pubmedId":"","doi":"10.1016/j.scitotenv.2016.12.108"}],"title":"Method of Removal of Aquatic Pond Weed Variability Impacts Presence of Potentially Toxigenic Cyanobacteria
","reviews":[],"curatorReviews":[]},{"id":"6d8708e3-5e32-4c30-9346-185034974ae5","decision":"publish","abstract":"Lakes often exist in two alternative stable states: clear waters dominated by submerged aquatic vegetation and turbid states with an abundance of phytoplankton. Management decisions must balance the value of primary producers with recreational use. We monitored the phytoplankton community surrounding removal of invasive Potamogeton crispus, a submerged aquatic perennial. Focus was given to presence of cyanobacteria, which may thrive in the absence of macrophytes by virtue of phosphorus that would otherwise be stored in plant biomass. Results demonstrate that macrophyte removal can lead to an increase in cyanobacteria dominance, with sustained impacts after hand removal.
","acknowledgements":"We are grateful to the lake association members for providing access to the lake and contextual information regarding the lake's history.
","authors":[{"affiliations":["Penn State Berks, Reading, PA, US "],"departments":["Biology"],"credit":["conceptualization","formalAnalysis","methodology","writing_originalDraft"],"email":"sbp20@psu.edu","firstName":"Sarah D","lastName":"Princiotta","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0002-9152-4146"},{"affiliations":["Penn State Schuylkill, Schuylkill Haven, PA, US"],"departments":["Biology"],"credit":["formalAnalysis","dataCuration","methodology","investigation","writing_reviewEditing"],"email":"ostergaardemily0@gmail.com","firstName":"Emily","lastName":"Ostergaard","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["Holy Family University, Philadelphia, PA, US"],"departments":["Biology"],"credit":["conceptualization","formalAnalysis","methodology","investigation","writing_reviewEditing","resources"],"email":"ecarroll2@holyfamily.edu","firstName":"Elizabeth","lastName":"Carroll","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[],"funding":"No funding to report.
","image":{"url":"https://portal.micropublication.org/uploads/e689d99d7dbb8978e802cfaa91cfaf64.JPG"},"imageCaption":"Percentage of the phytoplankton community composed of cyanobacteria in aquatic sites where Potamogeton crispus was removed by hand or mechanically and otherwise left undisturbed (control). The month of June represents pre-treatment conditions. Individual one-way ANOVA tests were conducted within each treatment site to investigate the influence of removal method over time on the percentage of the phytoplankton community composed of cyanobacteria. Letter cases in the figure indicate results of the post-hoc Tukey HSD.
","imageTitle":"Percentage of the phytoplankton community composed of cyanobacteria based on month and form of aquatic plant removal
","methods":"Field collection and Enumeration of Cyanobacteria by Microscopy
The study lake (Zmax 14 m, ~24 ha.) is a natural lake of glacial origin located in Pike County, Pennsylvania. Identifying information, including lake name, are not included here per sampling agreement. The vegetation within the drainage basin is primarily forested and the lake has no inlet streams. Routine lake monitoring from a central location on the study lake report a range of summer Secchi depth from 2.5 – 3 m, epilimnetic chlorophyll from 0.42 – 3.4 mg L-1, and epilimnetic total phosphorus from 4.45 – 5.75 mg L-1. The phytoplankton community is dominated by cyanobacteria genera that can produce cyanotoxins (Limnothrix, Aphanizomenon, Dolichospermum).
Curly-leaf Pond Weed (Potamogeton crispus), a submerged perennial, was first identified in the study lake during 2020-2021, composing ~12 acres of the shoreline in 2023. In July 2024, a combination of hand removal and mechanical harvest removed ~95% of P. crispus from the shoreline. Seven acres were treated by mechanical harvest and five acres by hand removal over a two-day period. The mechanical harvester was able to both cut and collect aquatic macrophytes up to 1.3 m below the surface. Hand removal efforts sought to remove all P. crispus, including the roots, but the macrophyte commonly broke mid-stem. A central location within each site, including an area that was not treated (control), was sampled three times over the course of the study period: one week prior to plant removal (June), and 29 (July) and 56 (August) days after removal.
During each sampling event, triplicate sub-surface (0.5 m) water was collected by Van Dorn bottle along a transect, passed through a 153-mm mesh, and stored in 250-mL polycarbonate bottles. Each sample was fixed with a final concentration of 2% Acid Lugol’s and stored in darkness prior to analysis. Samples were concentrated by settling over a 48-hour period after which the remaining ~20 mL was kept for microscopy. A minimum of 300 natural units were identified by light microscopy using a Zeiss Axiovert A1 at 400X magnification using the Utermol method (Paxinos and Mitchell, 2000). Phytoplankton, including cyanobacteria, were identified to genus apart from cells < 5mm diameter that lacked distinctive features, which were grouped as “unidentified nanoplankton.”
Statistical Analysis
All data analysis was conducted in JMP 18.2.2 and the figure was made using R version 4.2.3. Normality and homogeneity of variance were confirmed with a Shapiro Wilk and Levene test, respectively. To meet the assumptions for statistical testing, cyanobacteria abundance and percentage of the community composed of cyanobacteria were log and logit transformed, respectively. To investigate the influence of removal method over time within each site (hand removal, mechanical removal, no removal) a one-way ANOVA with post-hoc Tukey HSD each for cyanobacteria abundance and percentage of the phytoplankton community composed of cyanobacteria. To compare the influence of removal method (hand removal, mechanical removal, no removal) on the percentage of the phytoplankton community composed of cyanobacteria, a one-way ANOVA with post-hoc Tukey HSD was applied for each month after treatment was applied (July, August) with site as the independent variable. Due to significant differences across sites on the abundance of cyanobacteria measured prior to removal method, we did not pursue abundance as a dependent variable for an exploration of the effect of removal method across sites.
","reagents":"","patternDescription":"Despite their evolutionary origins as key aquatic primary producers, dense proliferations, or “blooms” of potentially harmful cyanobacteria are an issue for water quality management in lakes and reservoirs worldwide. The drivers of cyanobacteria dominance and production of toxic secondary metabolites are complex and likely related to environmental conditions associated with global climate change (Paerl et al., 2016). An increased frequency and severity of cyanobacteria blooms are often associated with high surface water temperatures and anthropogenic eutrophication (Kosten et al., 2012; Chapra et al., 2017) Lake managers are tasked with preventing and responding to cyanobacteria blooms that have been implicated in public health consequences for wildlife, pets, and humans (Backer et al., 2013; Trevino-Garrison et al., 2015; Skafi et al., 2021).
Another threat to freshwater ecosystems is the overgrowth of invasive, submerged aquatic vegetation (Kuiper et al., 2017), which may compromise use of recreational lakes for boating and fishing. Although important to the structure of lake ecosystems as a source of habitat, sediment stability, and nutrient storage (van Donk and van de Bund, 2002; Kovalenko et al., 2010), excess growth of submerged aquatic macrophytes can have negative impacts on water quality when decomposition releases large amounts of phosphorus and consumes dissolved oxygen (Asaeda et al., 2000). There are several methods to manage aquatic macrophytes including removal by either hand or motorized harvesters and chemical treatment with herbicides. Removal of excessive amounts of aquatic macrophytes should be conducted with great caution, as they stabilize the clear water state of shallow lakes (Scheffer et al., 1993). However, it can also be important to balance lake ecosystem health with recreational user preferences.
Aquatic macrophytes may act as natural control agents for cyanobacteria blooms via release of allelopathic compounds (Jasser, 1995), shading, and nutrient competition (Zhou et al., 2017). Field studies that document changes in phytoplankton community structure after removal of aquatic vegetation by various methods are lacking and produce mixed results (Morris et al., 2006; Maredová et al., 2021), especially in lakes that receive a temporally restricted, rather than continuous, removal of dense stands of aquatic vegetation. We took advantage of lake management action to study the impacts of aquatic plant removal (Potamogeton crispus) by either hand or mechanical harvest on the presence of cyanobacteria. A control was provided by a site in which aquatic plants were undisturbed and present at a low density. We hypothesized that removal of P. crispus, either by hand or mechanical removal, would lead to an increase in cyanobacteria as representatives in the phytoplankton community, with potentially greater impacts on the hand removal site where fragmented plant matter could act as an inadvertent nutrient source. Removal of P. crispus may also enhance cyanobacteria growth due to reduced nutrient competition.
Prior to removal of P. crispus, there were no differences in the percentage of the phytoplankton community composed of cyanobacteria across sites (11% ± 2 SE). However, prior to any initiation of treatment, there were notable differences in the abundance of cyanobacteria by site (F2,3 = 15.41, p = 0.03), with a higher abundance of cyanobacteria in the site designated for mechanical removal relative to that designated for hand removal. Additionally, the abundance of cyanobacteria at the experimental sites destined for plant removal were not significantly different from the control site.
There was a significant effect of month on the percentage of the community composed of cyanobacteria at both the hand-removal (F2,4 = 24.85, p = 0.0055) and control site (F2,4 = 25.09, p = 0.0054). At the hand-removal site, the percentage of the phytoplankton community composed of cyanobacteria increased over time from 7% to 62%, with significant differences between June, prior to plant removal, and August (p = 0.0048). There was not a significant effect of month on the abundance of cyanobacteria at the hand removal site, suggesting the observed increase in percentage of the phytoplankton community composed of cyanobacteria may result from changes in community structure. It is possible that non-cyanobacteria members of the phytoplankton community did not respond as favorably to conditions associated with hand removal of P. crispus relative to cyanobacteria. Hand removal of P. crispus may have increased the availability of photosynthetic active radiation (PAR) and nutrients available to the phytoplankton, of which cyanobacteria are well-adapted at capitalizing.
In the control site where aquatic plants were undisturbed, there was an initial, although non-significant, decline in the percentage of the community composed of cyanobacteria between pre-treatment conditions in June and July. However, cyanobacteria dominance (%) increased significantly between July and August (p = 0.0047). When considering cyanobacteria abundance at the control site, there was a significant effect of month (F2,4 = 41.75, p = 0.002), where cyanobacteria abundance also increased from July to August (p = 0.002), and the abundance in August was higher than the pre-treatment conditions (p = 0.01). It is worth noting that whereas the cyanobacteria population was kept low between June and July in the control site, there was a positive response of month on non-cyanobacteria members of the phytoplankton community within the same time frame. These results are indicative of the potentially negative allelopathic interactions between P. crispus and cyanobacteria or at least a differential response between the phytoplankton community to the presence of P. crispus.
In July but not August, there was a significant effect of site on the percentage of the community composed of cyanobacteria (F2,3 = 13.27, p = 0.03). A higher percentage of cyanobacteria were observed in the hand and mechanical removal sites relative to the control site where aquatic plants were undisturbed. Approximately one month after treatment, cross-site differences in cyanobacteria dominance (%) were no longer apparent. It may be interpreted that presence of excessive P. crispus had a negative impact on cyanobacteria that was temporarily relieved after removal of the aquatic macrophyte by either hand or mechanical measures. Our methodological approach does not allow us to interpret if this is due to regrowth of P. crispus, decomposition of fragmented plant material, or natural differences in cyanobacteria dominance that may occur within a single ecosystem. We suggest future studies to follow impacts of P. crispus removal through the fall germination period. This work provides a basis for targeted investigations that seek to balance invasive plant management with ecological health.
","references":[{"reference":"Asaeda T, Trung VK, Manatunge J. 2000. Modeling the effects of macrophyte growth and decomposition on the nutrient budget in Shallow Lakes. Aquatic Botany 68: 217-237.
","pubmedId":"","doi":"10.1016/S0304-3770(00)00123-6"},{"reference":"Backer L, Landsberg J, Miller M, Keel K, Taylor T. 2013. Canine Cyanotoxin Poisonings in the United States (1920s–2012): Review of Suspected and Confirmed Cases from Three Data Sources. Toxins 5: 1597-1628.
","pubmedId":"","doi":"10.3390/toxins5091597"},{"reference":"Chapra SC, Boehlert B, Fant C, Bierman VJ, Henderson J, Mills D, et al., Paerl. 2017. Climate Change Impacts on Harmful Algal Blooms in U.S. Freshwaters: A Screening-Level Assessment. Environmental Science & Technology 51: 8933-8943.
","pubmedId":"","doi":"10.1021/acs.est.7b01498"},{"reference":"van Donk E, van de Bund WJ. 2002. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany 72: 261-274.
","pubmedId":"","doi":"10.1016/S0304-3770(01)00205-4"},{"reference":"Jasser I. 1995. The influence of macrophytes on a phytoplankton community in experimental conditions. Hydrobiologia 306: 21-32.
","pubmedId":"","doi":"10.1007/BF00007855"},{"reference":"Kosten S, Huszar VLM, Bécares E, Costa LS, van Donk E, Hansson LA, et al., Scheffer. 2011. Warmer climates boost cyanobacterial dominance in shallow lakes. Global Change Biology 18: 118-126.
","pubmedId":"","doi":"10.1111/j.1365-2486.2011.02488.x"},{"reference":"Kovalenko KE, Dibble ED, Slade JG. 2010. Community effects of invasive macrophyte control: role of invasive plant abundance and habitat complexity. Journal of Applied Ecology 47: 318-328.
","pubmedId":"","doi":"10.1111/j.1365-2664.2009.01768.x"},{"reference":"Kuiper JJ, Verhofstad MJJM, Louwers ELM, Bakker ES, Brederveld RJ, van Gerven LPA, et al., Mooij. 2017. Mowing Submerged Macrophytes in Shallow Lakes with Alternative Stable States: Battling the Good Guys?. Environmental Management 59: 619-634.
","pubmedId":"","doi":"10.1007/s00267-016-0811-2"},{"reference":"Maredová N, Altman J, Kaštovský J. 2021. The effects of macrophytes on the growth of bloom-forming cyanobacteria: Systematic review and experiment. Science of The Total Environment 792: 148413.
","pubmedId":"","doi":"10.1016/j.scitotenv.2021.148413"},{"reference":"Morris K, Bailey PCE, Boon PI, Hughes L. 2006. Effects of plant harvesting and nutrient enrichment on phytoplankton community structure in a shallow urban lake. Hydrobiologia 571: 77-91.
","pubmedId":"","doi":"10.1007/s10750-006-0230-0"},{"reference":"Paerl HW, Gardner WS, Havens KE, Joyner AR, McCarthy MJ, Newell SE, Qin B, Scott JT. 2016. Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients. Harmful Algae 54: 213-222.
","pubmedId":"","doi":"10.1016/j.hal.2015.09.009"},{"reference":"Paxinos R. 2000. A rapid Utermohl method for estimating algal numbers. Journal of Plankton Research 22: 2255-2262.
","pubmedId":"","doi":"10.1093/plankt/22.12.2255"},{"reference":"Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E. 1993. Alternative equilibria in shallow lakes. Trends in Ecology & Evolution 8: 275-279.
","pubmedId":"","doi":"10.1016/0169-5347(93)90254-M"},{"reference":"Skafi M, Vo Duy S, Munoz G, Dinh QT, Simon DF, Juneau P, Sauvé Sb. 2021. Occurrence of microcystins, anabaenopeptins and other cyanotoxins in fish from a freshwater wildlife reserve impacted by harmful cyanobacterial blooms. Toxicon 194: 44-52.
","pubmedId":"","doi":"10.1016/j.toxicon.2021.02.004"},{"reference":"Trevino-Garrison I, DeMent J, Ahmed F, Haines-Lieber P, Langer T, Ménager H, et al., Carney. 2015. Human Illnesses and Animal Deaths Associated with Freshwater Harmful Algal Blooms—Kansas. Toxins 7: 353-366.
","pubmedId":"","doi":"10.3390/toxins7020353"},{"reference":"Zhou Y, Zhou X, Han R, Xu X, Wang G, Liu X, Bi F, Feng D. 2017. Reproduction capacity of Potamogeton crispus fragments and its role in water purification and algae inhibition in eutrophic lakes. Science of The Total Environment 580: 1421-1428.
","pubmedId":"","doi":"10.1016/j.scitotenv.2016.12.108"}],"title":"Method of Removal of Aquatic Pond Weed Variably Impacts Presence of Potentially Toxic Cyanobacteria
","reviews":[],"curatorReviews":[]}]}},"species":{"species":[{"value":"acer saccharum","label":"Acer saccharum","imageSrc":"","imageAlt":"","mod":"TreeGenes","modLink":"https://treegenesdb.org","linkVariable":""},{"value":"achillea millefolium","label":"Achillea millefolium","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"acinetobacter baylyi","label":"Acinetobacter baylyi","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"actinobacteria bacterium","label":"Actinobacteria bacterium","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"adelges tsugae","label":"Adelges tsugae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"adenocaulon chilense","label":"Adenocaulon chilense","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"aedes japonicus","label":"Aedes japonicus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"aegorhinus vitulus","label":"Aegorhinus vitulus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"alaimidae","label":"Alaimidae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"allobates femoralis","label":"Allobates femoralis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"alnus glutinosa","label":"Alnus glutinosa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"alosa aestivalis","label":"Alosa aestivalis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"alosa pseudoharengus","label":"Alosa pseudoharengus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"alternaria alternata","label":"Alternaria alternata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"amynthas agrestis","label":"Amynthas Agrestis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ancylostoma caninum","label":"Ancylostoma caninum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ancylostoma ceylanicum","label":"Ancylostoma ceylanicum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anemone multifida","label":"Anemone multifida","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anguilla rostrata","label":"Anguilla rostrata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anisakis simplex","label":"Anisakis simplex","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anomala albopilosa","label":"Anomala albopilosa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anthomyiidae sp","label":"Anthomyiidae sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anthomyiidae sp","label":"Anthomyiidae sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"arabidopsis","label":"Arabidopsis","imageSrc":"arabidopsis.png","imageAlt":"Arabidopsis graphic by Zoe Zorn CC BY 4.0","mod":"TAIR","modLink":"https://arabidopsis.org","linkVariable":""},{"value":"architeuthis dux","label":"Architeuthis dux","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"arion vulgaris","label":"Arion vulgaris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"armeria","label":"Armeria","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"artemia","label":"Artemia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"arthrobacter sp.","label":"Arthrobacter sp.","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ascaridia","label":"Ascaridia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ascaridia galli","label":"Ascaridia galli","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"asparagopsis taxiformis","label":"Asparagopsis taxiformis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"astatotilapia burtoni","label":"Astatotilapia burtoni","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"avena sativa","label":"Avena sativa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"aves","label":"Aves","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus","label":"Bacillus (firmicutes)","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus cereus","label":"Bacillus cereus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus mycoides","label":"Bacillus mycoides","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus subtilis","label":"Bacillus subtilis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus thuringiensis","label":"Bacillus thuringiensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus toyonensis","label":"Bacillus toyonensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus wiedmannii","label":"Bacillus wiedmannii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacteria","label":"Bacteria","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacteriophage","label":"Bacteriophage","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bactrocera","label":"Bactrocera sp.","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"batrachospermum gelatinosum","label":"Batrachospermum gelatinosum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"betula lenta","label":"Betula lenta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"betula nigra","label":"Betula nigra","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bombus dahlbohmii","label":"Bombus dahlbohmii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bombus terrestris","label":"Bombus terrestris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bombyx mori","label":"Bombyx mori","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bos taurus","label":"Bos Taurus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"brachygobius doriae","label":"Brachygobius doriae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"brassica oleracea","label":"Brassica oleracea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"brassica rapa","label":"Brassica rapa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"brugia malayi","label":"Brugia malayi","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"burkholderia thailandensis","label":"Burkholderia thailandensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"buttiauxella","label":"Buttiauxella","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"caenorhabditis brenneri","label":"Caenorhabditis brenneri","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"caenorhabditis briggsae","label":"Caenorhabditis briggsae","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"c. elegans","label":"Caenorhabditis elegans","imageSrc":"c-elegans.jpg","imageAlt":"C. elegans graphic by Zoe Zorn CC BY 4.0","mod":"WormBase","modLink":"https://wormbase.org","linkVariable":""},{"value":"caenorhabditis inopinata","label":"Caenorhabditis inopinata","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"caenorhabditis japonica","label":"Caenorhabditis japonica","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"caenorhabditis nigoni","label":"Caenorhabditis nigoni","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"caenorhabditis remanei","label":"Caenorhabditis remanei","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"caenorhabditis tropicalis","label":"Caenorhabditis tropicalis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"calidifontibacillus","label":"Calidifontibacillus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"calidifontibacillus erzuremensis","label":"Calidifontibacillus erzuremensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"calliphora sp","label":"Calliphora sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"caltha sagittata","label":"Caltha sagittata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cambarus latimanus","label":"Cambarus latimanus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"candida albicans","label":"Candida albicans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"canis familiaris","label":"Canis familiaris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cannabis sativa","label":"Cannabis sativa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"caretta caretta","label":"Caretta caretta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cassiopea xamachana","label":"Cassiopea xamachana","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"caulobacter vibrioides","label":"Caulobacter vibrioides","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cephalopods","label":"Cephalopoda","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cerastium arvense","label":"Cerastium arvense","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ceriodaphnia","label":"Ceriodaphnia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ceroglossus suturalis","label":"Ceroglossus suturalis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chaetoceros","label":"Chaetoceros","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chamaecrista fasciculata","label":"Chamaecrista fasciculata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chilicola chalcidiformis","label":"Chilicola chalcidiformis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chitinimonas","label":"Chitinimonas","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chlamydomonas reinhardtii","label":"Chlamydomonas reinhardtii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chromobacterium","label":"Chromobacterium","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chrysemys picta","label":"Chrysemys picta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chrysoperla rufilabris","label":"Chrysoperla rufilabris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"citrus","label":"Citrus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"clavibacter sp.","label":"Clavibacter sp.","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"colinus virginianus","label":"Colinus virginianus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"crassostrea virginica","label":"Crassostrea virginica","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"crithidia fasciculata","label":"Crithidia fasciculata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cutibacterium acnes","label":"Cutibacterium acnes","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cyanobacteria","label":"Cyanobacteria","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"daphnia","label":"Daphnia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"daphnia pulex","label":"Daphnia pulex","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"diabrotica virgifera","label":"Diabrotica virgifera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"diabrotica virgifera virgifera virus 1","label":"Diabrotica virgifera virgifera virus 1","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"d. discoideum","label":"Dictyostelium discoideum","imageSrc":"dicty.png","imageAlt":"D. discoideum","mod":"dictyBase","modLink":"http://dictybase.org","linkVariable":""},{"value":"diptera","label":"Diptera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"dotocryptus bellicosus","label":"Dotocryptus bellicosus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"drechmeria coniospora","label":"Drechmeria coniospora","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"drosophila","label":"Drosophila","imageSrc":"drosophila.png","imageAlt":"Drosophila graphic by Zoe Zorn CC BY 4.0","mod":"FlyBase","modLink":"https://flybase.org/doi/","linkVariable":"doi"},{"value":"dryopteris campyloptera","label":"Dryopteris campyloptera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"dryopteris expansa","label":"Dryopteris expansa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"dryopteris intermedia","label":"Dryopteris intermedia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"dugesia dorotocephala","label":"Dugesia dorotocephala","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"elasmobranchii","label":"Elasmobranchii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"embryophyta","label":"Embryophyta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"enoploteuthis chunii","label":"Enoploteuthis chunii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"enterobacter aerogenes","label":"Enterobacter aerogenes","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"enterococcus raffinosus","label":"Enterococcus raffinosus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"epichloë coenophiala","label":"Epichloë coenophiala","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"equus caballus","label":"Equus caballus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"erigeron sp","label":"Erigeron sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"eristalis","label":"Eristalis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"eruca vesicaria","label":"Eruca vesicaria","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"erwinia carotovora","label":"Erwinia carotovora","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"erythronium americanum","label":"Erythronium americanum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"escherichia coli","label":"Escherichia coli","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"eukaryota","label":"Eukaryotes","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"felis catus","label":"Felis catus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"francisella novicida","label":"Francisella novicida","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"francisella tularensis","label":"Francisella tularensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"fraxinus americana","label":"Fraxinus americana","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"fucus distichus","label":"Fucus distichus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"fungi","label":"Fungi","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"gasteropelecus sp.","label":"Gasteropelecus sp.","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"geranium sp","label":"Geranium sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"girardia","label":"Girardia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"glaucomys volans","label":"Glaucomys volans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"glycine max","label":"Glycine max","imageSrc":"","imageAlt":"","mod":"Soybase","modLink":"https://soybase.org","linkVariable":""},{"value":"glyptemys insculpta","label":"Glyptemys insculpta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"gossypium hirsutum","label":"Gossypium hirsutum","imageSrc":"","imageAlt":"","mod":"CottonGen","modLink":"https://www.cottongen.org/","linkVariable":""},{"value":"gromphadorhina portentosa","label":"Gromphadorhina portentosa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"gryllodes sigillatus","label":"Gryllodes sigillatus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"haliotis rufescens","label":"Haliotis rufescens","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"hepacivirus hominis","label":"Hepatitis C Virus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"herpes simplex virus type 1","label":"Herpes simplex virus type 1","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"human","label":"Human","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"human coronavirus oc43","label":"Human coronavirus OC43","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"hydra vulgaris","label":"Hydra vulgaris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"hydropsyche sp","label":"Hydropsyche sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"hymenoptera","label":"Hymenoptera","imageSrc":"","imageAlt":"","mod":"Hymenoptera Genome Database","modLink":"https://hymenoptera.elsiklab.missouri.edu/","linkVariable":""},{"value":"hypochaeris radicata","label":"Hypochaeris radicata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"hypodynerus vespiformis","label":"Hypodynerus vespiformis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"iflaviridae","label":"Iflaviridae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"iflavuris","label":"Iflavirus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ipomoea hederacea","label":"Ipomoea hederacea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ischnomera","label":"Ischnomera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ischnomera ruficollis","label":"Ischnomera ruficollis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"julidochromis marlieri","label":"Julidochromis marlieri","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"juniperus virginiana","label":"Juniperus virginiana","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"kluyveromyces marxianus","label":"Kluyveromyces marxianus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"l. casei","label":"L. casei","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lacticaseibacillus casei","label":"Lacticaseibacillus casei","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"larentiinae sp","label":"Larentiinae sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"laurus nobilis","label":"Laurus nobilis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lepidoptera","label":"Lepidoptera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"leucanthemum vulgare","label":"Leucanthemum vulgare","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"linepithema humile","label":"Linepithema humile","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"liometopum occidentale","label":"Liometopum occidentale","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lolium arundinaceum","label":"Lolium arundinaceum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lumbriculus variegatus","label":"Lumbriculus variegatus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lumbricus terrestris","label":"Lumbricus terrestris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lupinus polyphyllus","label":"Lupinus polyphyllus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lycorma delicatula","label":"Lycorma delicatula","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lynx rufus","label":"Lynx rufus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"magnaporthe oryzae","label":"Magnaporthe oryzae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"mammalia","label":"Mammalia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"manihot esculenta","label":"Manihot esculenta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"medicago lupulina","label":"Medicago lupulina","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"meloidogyne","label":"Meloidogyne","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"mimus polyglottos","label":"Mimus polyglottos","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bryophyta","label":"Mosses","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"mouse","label":"Mouse","imageSrc":"","imageAlt":"","mod":"MGI","modLink":"https://informatics.jax.org","linkVariable":""},{"value":"m. minutoides","label":"Mus minutoides","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"mycobacterium smegmatis","label":"Mycobacterium smegmatis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"nakaseomyces glabratus","label":"Nakaseomyces glabratus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"nauphoeta cinerea","label":"Nauphoeta cinerea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"neurospora","label":"Neurospora","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"n. benthamiana","label":"Nicotiana benthamiana","imageSrc":"","imageAlt":"","mod":"Solgenomics Network","modLink":"https://solgenomics.net/organism/Nicotiana_benthamiana/genome","linkVariable":""},{"value":"nicotiana tabacum","label":"Nicotiana tabacum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"noctuidae","label":"Noctuidae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"noctuidae sp","label":"Noctuidae sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"nothobranchius furzeri","label":"Nothobranchius furzeri","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"onchocerca volvulus","label":"Onchocerca volvulus","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"orconectes virilis","label":"Orconectes virilis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ormia ochracea","label":"Ormia ochracea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"o. sativa","label":"Oryza sativa","imageSrc":"","imageAlt":"","mod":"Gramene","modLink":"https://www.gramene.org/","linkVariable":""},{"value":"other","label":"Other","imageSrc":"","imageAlt":"","mod":null,"modLink":null,"linkVariable":null},{"value":"oxalis enneaphylla","label":"Oxalis enneaphylla","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"paenarthrobacter nicotinovorans","label":"Paenarthrobacter nicotinovorans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"paenarthrobacter nicotinovorans","label":"Paenarthrobacter nicotinovorans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pantoea","label":"Pantoea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pantoea agglomerans","label":"Pantoea agglomerans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"papaver sp","label":"Papaver sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"paramecium bursaria","label":"Paramecium bursaria","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"partitiviridae","label":"Partitiviridae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pelodiscus sinensis","label":"Pelodiscus sinensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"perezia recurvata","label":"Perezia recurvata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"petromyzon marinus","label":"Petromyzon marinus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"photinus pyralis","label":"Photinus pyralis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"photinus pyralis associated partiti-like virus","label":"Photinus pyralis associated partiti-like virus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"photinus pyralis iflavirus 1","label":"Photinus pyralis iflavirus 1","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"physcomitrium patens","label":"Physcomitrium patens","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pinus strobus","label":"Pinus strobus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pinus taeda","label":"Pinus taeda","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"platycheirus","label":"Platycheirus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"plectus sambesii","label":"Plectus sambesii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pogonomyrmex occidentalis","label":"Pogonomyrmex occidentalis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"poncirus trifoliata","label":"Poncirus trifoliata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"populus deltoides","label":"Populus deltoides","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"potato virus y","label":"Potato virus Y","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"primula magellanica","label":"Primula magellanica","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pristionchus pacificus","label":"Pristionchus pacificus","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"prunus persica","label":"Prunus persica","imageSrc":"","imageAlt":"","mod":"Genome Database for Rosaceae","modLink":"https://www.rosaceae.org/","linkVariable":""},{"value":"psalmopoeus iriminia","label":"Psalmopoeus iriminia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudanabaena sp.","label":"Pseudanabaena sp.","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudomonas","label":"Pseudomonas","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudomonas aeruginosa","label":"Pseudomonas aeruginosa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudomonas glycinae","label":"Pseudomonas glycinae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudomonas putida","label":"Pseudomonas putida","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudomonas syringae","label":"Pseudomonas syringae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pterophyllum scalare","label":"Pterophyllum scalare","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"python regius","label":"Python regius","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"quercus macrocarpa","label":"Quercus macrocarpa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ralstonia solanacearum","label":"Ralstonia solanacearum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ranitomeya imitator","label":"Ranitomeya imitator","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ranunculus peduncularis","label":"Ranunculus peduncularis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"rat","label":"Rat","imageSrc":"","imageAlt":"","mod":"RGD","modLink":"https://rgd.mcw.edu","linkVariable":""},{"value":"rheinheimera","label":"Rheinheimera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ribes rubrum","label":"Ribes rubrum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"sars-cov-2","label":"SARS-CoV-2","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"s. cerevisiae","label":"Saccharomyces cerevisiae","imageSrc":"yeast.png","imageAlt":"Yeast graphic by Zoe Zorn CC BY 4.0","mod":"SGD","modLink":"https://yeastgenome.org","linkVariable":""},{"value":"saccharomyces paradoxus","label":"Saccharomyces paradoxus ","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"s. uvarum","label":"Saccharomyces uvarum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"schistosoma","label":"Schistosoma","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"schizosaccharomyces japonicus","label":"Schizosaccharomyces japonicus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"s. pombe","label":"Schizosaccharomyces pombe","imageSrc":"pombe.png","imageAlt":"Pombe graphic by Zoe Zorn © Caltech","mod":"PomBase","modLink":"https://www.pombase.org/reference/PMID:","linkVariable":"pmId"},{"value":"schmidtea mediterranea","label":"Schmidtea mediterranea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"senecio sp","label":"Senecio sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"simocephalus","label":"Simocephalus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"siraitia grosvenorii","label":"Siraitia grosvenorii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"solanum lycopersicum","label":"Solanum lycopersicum","imageSrc":"","imageAlt":"","mod":"Solgenomics Network","modLink":"https://solgenomics.net/organism/1/view/","linkVariable":""},{"value":"sorghum","label":"Sorghum","imageSrc":"","imageAlt":"","mod":"SorghumBase","modLink":"https://www.sorghumbase.org","linkVariable":""},{"value":"spiroplasma eriocheiris","label":"Spiroplasma eriocheiris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"staphylococcus aureus","label":"Staphylococcus aureus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"staphylococcus epidermidis","label":"Staphylococcus epidermidis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"steinernema carpocapsae","label":"Steinernema carpocapsae","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"https://wormbase.org","linkVariable":""},{"value":"steinernema hermaphroditum","label":"Steinernema hermaphroditum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"stenotrophomonas geniculata","label":"Stenotrophomonas geniculata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"streptococcus gordonii ","label":"Streptococcus gordonii ","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"streptococcus mutans","label":"Streptococcus mutans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":" streptococcus pneumoniae","label":"Streptococcus pneumoniae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"s. purpuratus","label":"Strongylocentrotus purpuratus","imageSrc":"","imageAlt":"","mod":"Echinobase","modLink":"https://www.echinobase.org","linkVariable":""},{"value":"strongyloides ratti","label":"Strongyloides ratti","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"sulfolobus","label":"Sulfolobus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"symphoricarpos albus","label":"Symphoricarpos albus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"syncirsodes","label":"Syncirsodes","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"synechococcus elongatus","label":"Synechococcus elongatus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"syrphidae","label":"Syrphidae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tarantobelus jeffdanielsi","label":"Tarantobelus jeffdanielsi","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"taraxacum officinale","label":"Taraxacum officinale","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tatochila theodice","label":"Tatochila theodice","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tetrahymena","label":"Tetrahymena","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tetramorium immigrans","label":"Tetramorium immigrans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tomato brown rugose fruit virus","label":"ToBRFV","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"trachemys scripta","label":"Trachemys scripta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tribolium castaneum","label":"Tribolium castaneum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"trichoptera","label":"Trichoptera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"trichuris muris","label":"Trichuris muris","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"trifolium repens","label":"Trifolium repens","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"trypoxylus dichotomus","label":"Trypoxylus dichotomus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tsuga canadensis","label":"Tsuga canadensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ulva expansa","label":"Ulva expansa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"universal","label":"Universal","imageSrc":"","imageAlt":"","mod":null,"modLink":null,"linkVariable":null},{"value":"vargula hilgendorfii","label":"Vargula hilgendorfii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"vespula vulgaris","label":"Vespula vulgaris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"virus","label":"Virus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"watasenia scintillans","label":"Watasenia scintillans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"wolbachia pipientis","label":"Wolbachia pipientis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"xenopus","label":"Xenopus","imageSrc":"xenopus.png","imageAlt":"Xenopus graphic by Zoe Zorn CC BY 4.0","mod":"XenBase","modLink":"https://xenbase.org","linkVariable":""},{"value":"xenorhabdus griffiniae","label":"Xenorhabdus griffiniae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"yramea cytheris","label":"Yramea cytheris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"zaprionus indianus","label":"Zaprionus indianus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"zea mays","label":"Zea mays","imageSrc":"","imageAlt":"","mod":"MaizeGDB","modLink":"https://www.maizegdb.org","linkVariable":""},{"value":"zebrafish","label":"Zebrafish","imageSrc":"zebrafish.png","imageAlt":"Zebrafish graphic by Zoe Zorn CC BY 4.0","mod":"ZFIN","modLink":"https://zfin.org","linkVariable":""}]}},"pageContext":{"id":"5591acdb-f50b-49d9-b2fd-e22fb3e6f873","citedBy":[],"parsedCsv":{"csvHeader":[],"csvData":[]}}}, "staticQueryHashes": ["2114697108"]}