Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart...

12
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ulrm20 Lake and Reservoir Management ISSN: 1040-2381 (Print) 2151-5530 (Online) Journal homepage: http://www.tandfonline.com/loi/ulrm20 Transplanting aquatic macrophytes to restore the littoral community of a eutrophic lake after the removal of common carp Joshua M. Knopik & Raymond M. Newman To cite this article: Joshua M. Knopik & Raymond M. Newman (2018): Transplanting aquatic macrophytes to restore the littoral community of a eutrophic lake after the removal of common carp, Lake and Reservoir Management, DOI: 10.1080/10402381.2018.1477885 To link to this article: https://doi.org/10.1080/10402381.2018.1477885 Published online: 19 Sep 2018. Submit your article to this journal Article views: 28 View Crossmark data

Transcript of Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart...

Page 1: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

Full Terms & Conditions of access and use can be found athttp://www.tandfonline.com/action/journalInformation?journalCode=ulrm20

Lake and Reservoir Management

ISSN: 1040-2381 (Print) 2151-5530 (Online) Journal homepage: http://www.tandfonline.com/loi/ulrm20

Transplanting aquatic macrophytes to restore thelittoral community of a eutrophic lake after theremoval of common carp

Joshua M. Knopik & Raymond M. Newman

To cite this article: Joshua M. Knopik & Raymond M. Newman (2018): Transplanting aquaticmacrophytes to restore the littoral community of a eutrophic lake after the removal of common carp,Lake and Reservoir Management, DOI: 10.1080/10402381.2018.1477885

To link to this article: https://doi.org/10.1080/10402381.2018.1477885

Published online: 19 Sep 2018.

Submit your article to this journal

Article views: 28

View Crossmark data

Page 2: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

Transplanting aquatic macrophytes to restore the littoral community of aeutrophic lake after the removal of common carp

Joshua M. Knopika,b and Raymond M. Newmana

aDepartment of Fisheries, Wildlife, and Conservation Biology, University of Minnesota, 2003 Upper Buford Circle, St. Paul, MN 55108;bMinnesota Department of Natural Resources, 1601 Minnesota Drive, Brainerd, MN 56401

ABSTRACTKnopik J, Newman R. 2018. Transplanting aquatic macrophytes to restore the littoral communityof a eutrophic lake after the removal of common carp. Lake Reserve Manage. 34:00–00.

Six native submersed aquatic macrophyte taxa were transplanted to a eutrophic lake (LakeSusan, Minnesota) to promote the growth and expansion of native taxa after the removal ofcommon carp (Cyprinus carpio). Muskgrass (Chara spp.), wild celery (Vallisneria americana), north-ern watermilfoil (Myriophyllum sibiricum), bushy pondweed (Najas flexilis), water stargrass(Heteranthera dubia), and flat-stem pondweed (Potamogeton zosteriformis) were transplanted in aseries of shallow (0.5–1.0 m) and deep (1.0–1.5 m) experimental plots around the lake. Survivaland expansion of plants were measured over 4 yr and compared against environmental factors.Transplantation of whole plants in shallow water was generally successful, but plants in depths�1.4 m failed to persist. Light availability was the most important factor determining success.Water stargrass was the most successful, with high long-term survival and substantial expansion.Wild celery had high survival, but slow and limited expansion. Bushy pondweed had variable sur-vival, but when it survived it generally expanded well. Muskgrass and northern watermilfoil hadpoor survival and expansion. Transplanting whole submersed aquatic macrophytes can help torestore the littoral community in degraded systems, but ecological stressors such as commoncarp should first be addressed. Poor mid-summer water clarity will limit the depth and distribu-tion of successful transplants and taxa that survive. Taxa with large perennial structures such aswater stargrass and wild celery are more likely to establish and persist, but the annual bushypondweed was also able to grow and spread.

KEYWORDSChara; common carp;Heteranthera dubia;macrophyte; Najas flexilis;transplant;Vallisneria americana

Aquatic macrophytes play a significant role inmaintaining water quality and ecosystem health byreducing sediment re-suspension and providinghabitat for aquatic organisms ranging from algae-consuming invertebrates to fish and other wildlife(Horppila and Nurminen 2003, Sondergaard et al.2003, James et al. 2004). A healthy aquatic macro-phyte community consists of a high diversity ofnative taxa (Madsen 1997). High densities ofinvasive common carp (Cyprinus carpio) uprootaquatic macrophytes and stir up sediments (Weberand Brown 2009), encouraging a turbid water statewith a low density of macrophytes (Schrage andDowning 2004, Bajer et al. 2009). Reducing thepopulation of common carp can increase the distri-bution and abundance of the aquatic plant commu-nity (Bajer et al. 2009). However, it can take several

years for aquatic macrophytes to establish in highdensities after fish removal (Hanson and Butler1994), and often the taxa that do establish are non-native invasive taxa (Lauridsen et al. 1994,Lougheed et al. 2004, Baker and Newman 2014).Manipulation of the littoral plant community maybe necessary to promote the establishment of nativevegetation rather than nonnative invasive taxa.

Transplanting can be an effective method forintroducing submersed aquatic macrophytes intowater bodies where few propagules exist (Smartet al. 1998, Lauridsen et al. 2003, Smiley and Dibble2006). The distribution of aquatic macrophytes,and subsequent success of transplanting them, isrelated to a number of environmental factorsincluding light availability (Scheffer 1998), tem-perature (Barko and Smart 1981), water level

CONTACT Raymond M. Newman [email protected]� Copyright by the North American Lake Management Society 2018.

LAKE AND RESERVOIR MANAGEMENThttps://doi.org/10.1080/10402381.2018.1477885

Page 3: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

fluctuation (Fleming et al. 2012), sediment structureand fertility (Barko and Smart 1986, Doyle 2001),and timing of transplants (Vanderbosch andGalatowitsch 2011). It has also been shown that pro-tection from herbivores and wave energy can beimportant for transplanting aquatic macrophytes(Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al. 1996,Lauridsen et al. 2003) to protect plants, but thesestructures can pose a recreation hazard and increasecost to littoral restoration projects. Stands of float-ing-leaf macrophytes (e.g., water lily stands) mayalso provide wave energy reduction and protectionfor transplanted macrophytes until establishment.

Although transplanting submersed macro-phytes as a means for littoral community restor-ation has been shown to be successful, themajority of the case studies were done in reser-voirs in southern latitudes of the United States orin more temperate climates of Europe (Doyleet al. 1997, Lauridsen et al. 2003, Dick et al.2004a, 2004b, Fleming et al. 2011). Few examplesfrom natural lakes in northern North Americaexist (Storch et al. 1986). Quantifying the growthand expansion of the transplants, along withenvironmental variables related to submergedmacrophyte growth such as depth, light intensity,sediment texture, timing of transplanting, soilorganic matter, and available nitrogen, may help

further define the most important factors thatcan lead to success in future transplanting.

The objective of our study was to determine iftransplantation can be used to establish new sub-mersed macrophyte species after carp removal ina continental-climate Minnesota lake. In addition,we wanted to compare the environmental varia-bles that may affect the survival and colonizationrate, and determine if floating-leaf stands couldprovide protection from wave activity to enhancetransplant success.

Methods

Site description

Lake Susan is a natural, eutrophic lake in CarverCounty, Minnesota, USA. The oval lake (shore-line development ¼ 1.15) has a surface area of36 ha, a mean fetch of 600 m (390–850 m), andmaximum depth of 5.2 m (Fig. 1). Lake Susanhad low summer Secchi depths (0.6 m), fewaquatic macrophyte taxa in very low abundance,and a high abundance of common carp (Bajerand Sorensen 2012, 2015). Using under-ice sein-ing in the winter of 2009, approximately 78% ofthe carp were removed from the lake (carp stand-ing stock reduced from 307 kg/ha to 65 kg/ha) inan attempt to determine if removal of carp wouldenhance water clarity and improve the nativeplant community (Bajer and Sorensen 2015).

Figure 1. Locations of transplant plots in Lake Susan. Each plot contained 5 sites with 1 species planted at each site.

2 J. M. KNOPIK AND R. M. NEWMAN

Page 4: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

Transplant plot methodology

It was suspected there were few viable aquaticplant propagules in the benthos, due to sustainedhigh carp densities for decades. Starting in 2010,6 native submersed aquatic taxa were trans-planted from nearby Lake Ann, Carver County,Minnesota, into Lake Susan to promote thegrowth and expansion of native plants. Thesource lake (Lake Ann) is located about 3 kmupstream of Lake Susan. It is within the samewatershed and had good water clarity (summerSecchi depths of 2.5–4 m) and high species rich-ness (25 submersed, emergent, and floating-leaf species).

Transplant selection criteria considerationsincluded that all species were native toMinnesota, expected to have high likelihood ofsuccess as determined by Smart et al. (1996), inadequate abundance in the source lake, and notalready found in Lake Susan. The 6 species weremuskgrass (Chara spp.), wild celery (Vallisnariaamericana), northern watermilfoil (Myriophyllumsibiricum), bushy pondweed (Najas flexilis), waterstargrass (Heteranthera dubia), and flat-stempondweed (Potamogeton zosteriformis). Waterstargrass was transplanted in only shallow plots(<1 m) and flat-stem pondweed was transplantedin only deeper plots (�1.4 m), matching theirdistribution in the source lake.

Transplants were collected from Lake Ann bysnorkeling and wading in 0.5–1.5 m depths. Asmall garden spade was used to dig up the sedi-ment around the roots of mature plants; care wastaken to not damage roots and rhizomes and toensure only the preselected species were collected.The roots were gently rinsed of sediment andwhole plants were placed in a large cooler withlike taxa and lake water, stored at room tempera-ture overnight, and transplanted into Lake Susanthe next day.

Transplant plots were located away from devel-oped areas and locations were recorded by GPS.

Each plot contained 5 transplant sites, spaced 2m apart, and marked with a small labeled PVCpipe pushed into the substrate to aid future mon-itoring. One species was randomly selected to betransplanted at each site, where 10 individualplant stems were planted within a 0.25 m2 area.Existing vegetation, if present, was removed byhand prior to transplanting. Bare roots wereplaced in a small hand-dug hole (approximately5 cm deep) and a 10 cm steel sod staple was usedto hold the roots in place, which were then cov-ered with sediment. Muskgrass, which lacks roots,was transplanted as a cluster approximately500 cm3 (1 cluster was considered 1 stem) andheld to the substrate with a sod staple. Sedimentat transplant sites tended to be sandy with amean bulk density of 1.26 g/mL±0.09 SE (Table 1)and mean organic matter of 1.66%±0.25 SE(Knopik 2014).

Shallow plots

Twelve plots of 5 taxa (muskgrass, water star-grass, northern watermilfoil, bushy pondweed,and wild celery) were transplanted at shallow(0.5–0.75 m depth) locations distributed aroundthe lake on 1 August 2010. Six plots were plantedshoreward of lily stands (protected), and 6 plotswere open to wave action (open) to evaluatewhether stands of floating-leaf species, whitewater lily (Nymphea odorata), yellow waterlily(Nuphar variegata), and water lotus (Nelumbolutea), provided adequate wave protection.Transplant plot locations were distributed aroundthe undeveloped stretches of shorelines to min-imize human interference and to maximizepotential for lake-wide colonization. One“protected” plot and 1 “open” plot were locatednear each other in an attempt to have similarfetch, shading, and substrate characteristics(Fig. 1).

Table 1. Summary of mean (±1 SE) sediment bulk density, mean percentorganic matter, and mean total nitrogen in soil samples taken July 2011.

Open (Shallow) Protected (Shallow) Combined (Shallow) Deep

Density (g/mL) 1.31 ± 0.09 1.21 ± 0.08 1.26 ± 0.09 0.72 ± 0.04Organic (%) 1.63 ± 0.40 1.68 ± 0.20 1.66 ± 0.25 1.94 ± 0.33Total N mg/g 0.0036 ± 0.0005 0.0039 ± 0.0010 0.0037 ± 0.0006 0.0053 ± 0.0004

LAKE AND RESERVOIR MANAGEMENT 3

Page 5: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

Deeper plots

Transplant success in deeper water was tested at 4additional plots (2 plots on the east side and 2 onthe west side of the lake). The plants were trans-planted in depths ranging from 1.2 m to 1.6 m on22 July 2010 (Fig. 1). The 5 species transplantedwere muskgrass, flat-stem pondweed, northernwatermilfoil, bushy pondweed, and wild celery.

Six additional deeper plots were transplanted on24 June 2011 using the same 5 taxa listed above todetermine if earlier planting improved the successof the deeper transplants. The transplanting wastimed to allow the plants at least 3–4 weeks toestablish in Lake Susan before Secchi transparencydropped below the transplanting depth of 1.6 m.

Plot assessment

Transplants were assessed at each site for survivaland area of coverage during the growing season.Survival was based on the presence of any stems ofthe transplanted taxa growing within 1 m of thetransplant site post and expressed as the propor-tion of sites with transplants present. Expansion ofcoverage at the transplant sites was measured tofurther understand if the transplanted taxa wouldexpand coverage within the littoral zone. Coveragewas calculated by measuring the area of homogen-ous growth (cm2) as well as the area of presence.The area of homogenous growth was defined as thearea in which approximately �90% of the plantswere made up of the transplanted taxa (Fig. 2). Alarge area of homogenous growth would indicatemonotypic stand development of the taxa. The area

of presence was defined as the area in which thespecies was present, but not necessarily dominant(Fig. 2). A large area of presence would indicate thetaxon is colonizing the littoral area as part of amore heterogeneous plant community. Mean areaof presence and homogenous growth were calcu-lated based on sites where plants were present(zeros were not included) to indicate expansionwhere plants survived. The summer maximummean area for each taxa was summarized per year.Shallow transplants were assessed every 3–4 weeksduring the summers of 2010 through 2013, andonce in 2014. Deep transplants were assessed aboutevery 4 weeks during the growing seasons of 2010and 2011, twice in 2012, and once in 2013.

To monitor natural recruitment of aquatic mac-rophytes after carp removal, point-intercept sur-veys were conducted in the summers of 2009–2014to determine the frequency of occurrence of taxapresent. Following methods outlined by Madsen(1999), GIS software was used to generate 146 sur-vey points in a 50 m systematic square grid acrossthe lake. A GPS was used to navigate a boat within5 m of each point. At each point, depth wasrecorded and vegetation was sampled with aweighted double-headed rake (0.33 m wide)attached to a rope, tossed into the lake, anddragged along the lake bottom for approximately 3m to cover 1 m2. Vegetation on the rake was identi-fied to species level and frequency of occurrencewas determined for the points sampled within thelittoral zone (�4.6 m depth). Borman et al. (2014)was used as the taxonomic authority.

Environmental variables

In situ limnological variables were measured at0.5 m depth intervals in the water column at thedeepest part of the lake biweekly between Apriland October. Water temperature (C) and dis-solved oxygen (mg/L) were measured with a YSI50B electronic meter. Photosynthetically activeradiation (PAR) was measured with a LI-COR189 digital meter and LI-192 quantum sensor.The depth at which surface PAR declined to 5%was used to compare PAR among years. Secchidepth was recorded to the nearest 0.1 m. PARwas also measured in August 2011 at 0.1 m inter-vals at 2 sites per plot, and PAR attenuation was

Figure 2. Example of plant growth assessment with area ofpresence and homogenous area of growth indicated. This sitewas planted with wild celery (Vallisneria americana).

4 J. M. KNOPIK AND R. M. NEWMAN

Page 6: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

compared between shallow open, shallow pro-tected, and deep plots.

In August 2011, a sediment sample was collectedwith a 5 cm diameter PVC core tube at each end ofthe transplant plots, resulting in 2 samples per plot(�8 m apart). The top 10 cm of sediment was sub-sampled and analyzed for sediment bulk density,organic matter, and total nitrogen.

Bulk density (g/mL) was determined from a10mL subsample of homogenized sediment. Thepercent organic matter was determined by com-busting the sample for 4 h at 550 C. Ammonium-Nwas measured in the pore water centrifuged from a50mL subsample of homogenized sediment usingan ammonia electrode (Orion model 9512). Theexchangeable ammonium-N was extracted fromthe remaining subsample with a 2 molar KCL solu-tion (Keeney and Nelson 1982), then measuredwith the ammonia electrode. The pore water nitro-gen and exchangeable nitrogen were combined formacrophyte-available N.

The potential influence of fetch and wind direc-tion was tested by comparing transplant survivalby year among plots with similar fetch/direction.Summer prevailing wind direction is from theWSW (NOAA 2012), so plots along the northernand eastern shoreline (with higher fetch/direction)were in one group, and plots along the southernand western shoreline were in the other group(Fig. 1).

Statistical analysis

Statistical analyses were completed using R statis-tical software version 2.13.1 (R DevelopmentCore Team 2011) and Microsoft Excel. Survivalwas evaluated separately from expansion. Single-factor ANOVA analysis was used to compare sur-vival to year and fetch. For expansion analysis,only sites with surviving plants were analyzed toassess expansion in the sites where the taxa sur-vived. Single-factor ANOVA analysis of expan-sion was performed separately for shallow sitesand deep sites, with homogenous area, and againwith area of presence. A single-factor ANOVAwas conducted for each taxa to compare meanarea of presence for open vs. protected sites.

Results

Shallow transplant plots

By the end of the first growing season (2010),100% of the water stargrass, wild celery, andbushy pondweed sites contained viable plants,and 92% of northern watermilfoil sites and 58%of muskgrass sites contained viable plants (Fig.3). Survival over the 5 yr decreased (P¼ 0.005),especially after 2012. By 2014, bushy pondweed,water stargrass, and wild celery were found in atleast 40% of sites, but northern watermilfoil wasfound at only 10% of sites and muskgrass wasnot found (Fig. 3).

None of the transplanted taxa grew into sizablemonotypic stands as measured by the homogen-ous area of growth (Fig. 4). Across all years,water stargrass in 2011 had the largest meanhomogenous area of 3.1 m2 (Fig. 4). During theinitial (2010) growing season, no plants expandedbeyond the original planting area of 0.25 m2 foreither homogenous area (Fig. 4) or area of pres-ence (Fig. 5).

There was wide variation between taxa in themean area of presence. Comparing across allyears, water stargrass generally had the greatestarea of presence, ranging from 89.6 m2 ± 24.8 SEin 2011 to 11.1 m2 ± 9.0 SE in 2014 (Fig. 5).Bushy pondweed also had large but more variedareas of presence, ranging from 124.1 m2 ± 61.2SE in 2011 to 2.33 m2 ± 1.8 SE in 2014. Wild cel-ery had slower, but consistent increases in area ofpresence, ranging from 1.4 m2 ± 0.3 SE in 2011 to5.6 m2 ± 5.1 SE in 2014. Northern watermilfoilshowed an initial increase of area of presence to18.9 m2 ± 12.2 SE in 2011, but it was not foundin 2013 and only 0.49 m2 ± 0.48 SE of coveragein 2014. Muskgrass had highly varied areas ofpresence ranging from less than 1.0 m2 in 2011to 8.1 m2 ± 5.3 SE in 2012, but it was not foundat all in 2014.

Fetch did not influence transplant survival asthere was no difference in survival by site loca-tion (P¼ 0.60). There was also no difference insurvival between open and protected sites(P¼ 0.67; Fig. 3). Between open and protectedsites, there was no difference in homogenous area(P¼ 0.928; Fig. 4) nor area of presence(P¼ 0.097; Fig. 5), and no individual taxa showed

LAKE AND RESERVOIR MANAGEMENT 5

Page 7: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

a difference in homogenous area or area of pres-ence between open and protected. There washigh variation in expansion among open andprotected sites between years and taxa. Forexample, in 2012 the area of coverage in pro-tected sites containing bushy pondweed andwater stargrass increased in both homogenousarea (Fig. 4) and area of presence (Fig. 5).

However, the opposite was true for northernwatermilfoil. Comparing both survival and thearea of presence there appeared to be 2 generalcategories (Fig. 6): taxa that survived and/orexpanded well (wild celery, water stargrass,bushy pondweed), and taxa that had lowersurvival and expansion (muskgrass, northernwatermilfoil).

0%10%20%30%40%50%60%70%80%90%

100%

Bushypondweed

Muskgrass Northernmilfoil

Waterstargrass

Wild celery

Site

swith

plan

ts

20102011201220132014

0%

20%

40%

60%

80%

100%

2010 2011 2012 2013 2014

Site

s with

pla

nts

open Protected

Figure 3. Survival of plant taxa in shallow plots by year (top) and overall survival by protection treatment (bottom).

0.00

0.01

0.10

1.00

10.00

201

0

201

1

201

2

201

3

201

4

201

0

201

1

201

2

201

3

201

4

201

0

201

1

201

2

201

3

201

4

201

0

201

1

201

2

201

3

201

4

201

0

201

1

201

2

201

3

201

4

Muskgrass N. Milfoil Bushy

Pondweed

Wild Celery Water

Stargrass

Are

a (m

2 )

Figure 4. Mean homogenous area of growth at open (hollow)and protected (stippled) sites by year of transplant in shallowplots. Initial planted area (indicated by dashed line) was 0.25m2. Note area axis is in logarithmic scale of base 10. Error barsare ±1 SE.

0.00

0.01

0.10

1.00

10.00

100.00

1000.00

201

0

201

1

201

2

201

3

201

4

201

0

201

1

201

2

201

3

201

4

201

0

201

1

201

2

201

3

201

4

201

0

201

1

201

2

201

3

201

4

201

0

201

1

201

2

201

3

201

4

Muskgrass N. Milfoil Bushy

Pondweed

Wild Celery Water

Stargrass

Are

a (m

2 )

Figure 5. The mean area of presence of plants at open (hol-low) and protected (stippled) sites by year of transplant inshallow plots. Initial area planted (indicated by dashed line)was 0.25 m2. Note area axis is in logarithmic scale of base 10.Error bars are ±1 SE.

6 J. M. KNOPIK AND R. M. NEWMAN

Page 8: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

Deeper transplant plots

Plants transplanted in 2010 at deeper depths(1.4 m) generally failed to establish. The plants alllooked dead 1mo after planting. Evaluation of theseplots after 1 yr found a few individual stems of flat-stem pondweed at 3 of the 4 sites, and 1 wild cel-ery plant at 1 site. None of the transplanted taxawere found growing near any of the sites in 2012.

The earlier timing of deep transplants in 2011showed better initial results compared to the laterplantings of 2010. Many of the flat-stem pondweedand northern watermilfoil plants showed some ini-tial growth and development of adventitious roots.Flat-stem pondweed and wild celery both had a 67%survival, with at least 1 plant found in 4 of the 6 sitesin August 2011. However, the average homogenousarea and area of presence (0.01 m2 and 0.05 m2,respectively) was less than 0.25 m2, the initial areaplanted. A few individual plants survived, but mostof them failed. After 1mo, bushy pondweed wasfound growing in only 1 site. Muskgrass survived innone of the sites. Overwinter survival was poor andassessments in spring 2012 found only a single ros-ette of wild celery growing at 2 locations (33% of thesites). Subsequent assessments in 2012 and 2013failed to locate any surviving deep transplants.

Environmental factors

Temperature and dissolved oxygen profiles indi-cate the lake typically became stratified in June

and remained so throughout the summer. Athermocline generally formed below 2 m and thehypolimnion became hypoxic (� 2mg/L) below3.5 m (Knopik 2014, Bajer and Sorenson 2015).

There was an increase in clarity during springand early summer (May–Jun) 2010 and 2011,after the removal of carp in 2009. However, theincreased clarity did not persist for the durationof the summer as Secchi depth and subsurfacePAR declined around mid-July (Fig. 7). PAR at1.5 m was usually <5% of surface light by earlyAugust, with the exception of 2010 and 2012when PAR at 1.5 m was <5% in early and mid-June, respectively (Fig. 7). This decrease in claritywas driven by increased chlorophyll a (Bajer andSorenson 2015). There was no difference in PAR(P> 0.05) just above the sediment in shallow sitesbetween open (1.8%± 0.4 SE) and protected(2.1%± 0.3 SE) sites, nor between deep transplantlocations (1.6%± 0.3 SE) when measured inAugust 2011.

The available sediment N varied little among sam-pling locations, with a mean of 0.0037mg/g±0.001SE (Table 1), and no difference in available sedimentN between protected and open sites, or deepsites (P¼ 0.13).

Lake-wide plant surveys

In 2008, prior to carp removal, only 2 submersedtaxa were reported from Lake Susan, coontail

Flatstem Pondweed

Wild Celery

Muskgrass

N. watermilfoil

BushyPondweed

WaterStargrass

0%

10%

20%

30%

40%

50%

60%

70%

80%

90%

100%

0 20 40 60 80 100 120

Mea

n Su

rviv

al

Area of Presence (m2)

Figure 6. Comparison of mean survival and area of presence for taxa in shallow plots during the 2011 growing season.

LAKE AND RESERVOIR MANAGEMENT 7

Page 9: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

(Ceratophyllum demersum) and Eurasian water-milfoil (Myriophyllum spicatum) (Bajer andSorensen 2015). In 2009, after carp removal, 5additional submersed taxa were found: Canadawaterweed (Elodea canadensis), curlyleaf(Potamogeton crispus), narrow leaf (P. pusillus),sago (Stukenia pectinata), and horned pondweed(Zannichellia palustris). After this initial appear-ance of new taxa, all but 2 of the 6 new taxa thatappeared in surveys, Illinois pondweed (P. illi-noensis) and white water buttercup (Ranunculusaquatilis), were transplants. By 2014, 4 of thetransplanted taxa (bushy pondweed, water star-grass, wild celery, and flatstem) were found inpoint intercept surveys near the areas where theywere transplanted. Transplanted taxa accountedfor the remaining increase in taxa diversity.

Plant frequency of occurrence increased from40% in 2009 to almost 60% in 2010 andremained above 45% in 2011 but declined to 30%in 2012 and subsequent years. The number ofsubmersed plants per point also declined from an

average of �1.27 in 2009, 2010, and 2011 to0.56 ± 0.14 in 2012 and subsequent years. Themaximum depth of plant occurrence decreasedfrom �3.1 m in 2009–2011 to 2.0 m in 2012 withpoor water clarity, but increased to 2.9 m in 2013and 2014.

Discussion

Transplanting was successful in establishingplants in the lake. All of the transplanted taxaplanted in shallow sites were found in the lakeafter 1 yr, 4 of the taxa persisted at transplantsites through 2014, and 4 expanded enough to befound in point-intercept surveys (bushy pond-weed, water stargrass, wild celery, and flat stem).Natural recruitment was not found to be themain factor in increasing the submersed speciesdiversity in Lake Susan beyond the year aftercarp removal, as only 2 taxa naturally recruited(Illinois pondweed and white water buttercup)after 2010. Natural recruitment appeared to

0

0.5

1

1.5

2

2.5

3

3.5

4

4.5

5

01-May 21-May 10-Jun 30-Jun 20-Jul 09-Aug 29-Aug

Dept

h (m

)2009

2010

2011

2012

2013

0

0.5

1

1.5

2

2.5

3

3.5

4

4.5

5

01-May 21-May 10-Jun 30-Jun 20-Jul 09-Aug 29-Aug

Dept

h (m

)

2009

2010

2011

2012

2013

Figure 7. Lake Susan Secchi depth by year (top), and depth of 5% PAR by year (bottom).

8 J. M. KNOPIK AND R. M. NEWMAN

Page 10: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

respond quickly to carp removal, which suggeststhat waiting a year or two before transplantingwill allow for strategic addition of new taxa. Thetransplants failed to persist at deeper (>1.4 m)sites; only a few stems of flat-stem pondweed andwild celery were found in the year after plantingand these did not further persist, although flat-stem did appear in a later point-intercept survey.Transplants should be monitored for severalyears after planting to assess establishment andexpansion. Few studies have reported assessmentsbeyond the first year after transplanting (Storchet al. 1986, Lauridsen et al. 2003).

Light availability was an important factor insurvival of taxa, illustrated by the success of trans-plants at shallow locations vs. the failure at deeperlocations and the reduced survival and expansionin 2012 when clarity was especially poor. By earlyAugust of most years, PAR was generally �5% ofsurface light at 1.5 m depth. Madsen (1991) foundthat, although light compensation point variedbetween species, an average of 7% surface PARwas needed for most species to survive. The earlyand persistent low water clarity during 2012 likelyinhibited establishment of the deep transplantsfrom 2011 and suppressed and reduced the expan-sion of the shallow transplants. The depth of 5%surface PAR in 2012 was less than 1.25 m fromearly June and was 0.5 m for most of the summer.In addition to reducing transplant success, thelake-wide abundance of plants was reduced in2012 and the maximum depth of plant occurrencewas reduced to 2 m. Transplant survival in 2012was decreased for all taxa; bushy pondweed,muskgrass, and water stargrass showed a reboundin survival in 2013 with better clarity. The betterpersistence of flat-stem pondweed and wild celeryat deeper sites may be due to their lower lightcompensation points. Wild celery plants provided5% of surface light were able to produce tubers(Kimber et al. 1995), however, plants did not sur-vive at 2% of surface light. Still, the poor waterclarity and low light penetration in Lake Susanmay explain the lower than expected area of pres-ence of wild celery in shallow sites.

Water stargrass and wild celery, both withlarge perennial structures, exhibited the highestsurvival in this study. Taxa with large vegetativestructures have larger carbohydrate reserves,

which allows for faster initial growth and carbo-hydrate levels generally sufficient to overwinter(Madsen 1991). Perennial submersed macro-phytes often produce twice as many vegetativepropagules than seeds, and vegetative propagulesare generally better at overwintering than seeds(Madsen 1991). Taxa with annual life historytraits such as muskgrass and flat-stem pondweedgenerally had lower survival (Fig. 6). The primarymeans of overwintering by annual plants isthrough the production of seeds or spores.Although annuals were noted as having lowersurvival rates, seed production can be a bettermeans of broadcasting propagules greater distan-ces (Madsen 1991). This explains why bushypondweed, with variable survival, can be consid-ered successful; where it did survive, it grew andexpanded well. Northern watermilfoil, however,did not fit the pattern of either perennial orannual groups in our study.

Factors influencing expansion were not clear.Taxa using fragmentation strategies, such aswater stargrass and bushy pondweed, had thegreatest area of presence (Fig. 5). Water stargrasshad good survival and most sites had high expan-sion. The use of runners by water stargrass likelyled to increased expansion and success, as notedby Smart et al. (1996). Wild celery had very goodoverwinter survival each year, but less expansionof coverage. The slow rate of expansion in wildcelery was unexpected as it has both a large rhi-zome and the use of runners. Smart et al. (1998)also noted that wild celery generally expandedrapidly. Low Secchi transparency and PAR pene-tration may have limited wild celery expansion inour study as none of the transplanted taxa devel-oped large dense homogenous stands. When wildcelery transplants expanded beyond their originalplanted areas, they generally grew in scatteredlow-density clusters.

Managers should anticipate the possible effectsof year-to-year variability in water clarity (Jameset al. 2004). Additional actions, such as alumtreatment, may be needed to maintain clarity andtruly restore the submersed plant community. Allof the taxa we transplanted may do well in lakeswith good summer-long water clarity, but inlakes with lower clarity, bushy pondweed, waterstargrass, and wild celery may be the best choices.

LAKE AND RESERVOIR MANAGEMENT 9

Page 11: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

Maximum successful transplanting depth will beinfluenced by minimum summer clarity andextreme years should be anticipated.

Protection by floating-leaf stands did not sig-nificantly affect the outcomes of transplantingduring this study. This may have been becausethe study lake was small, with a maximum fetchof only 850 m. There was also no apparent effectof fetch or wind direction on survival. During a2009 pilot study, wire fence barriers wereinstalled around 2 of 4 trial transplant plots.There was no significant difference betweenfenced and unfenced plots after 1 yr (Knopik2014). Protective barriers may not have been asbeneficial on Lake Susan once the carp abun-dance was greatly reduced and there were fewbenthivorous fish to uproot plants. The densityof other macro-herbivores such as waterfowl ormuskrats was not quantified, although personalobservation indicated very low abundance ofeach, which is consistent with similar suburbanarea lakes. Lakes with uncontrolled herbivores orlarge fetches may need protective exclosures to beeffective (e.g., Smart et al. 1998, Lauridsen et al.2003, Fleming et al. 2011).

Further research is needed to provide greaterunderstanding of the factors that predict expan-sion and colonization of plants in the littoralzone. More focus on the timing of transplantingmay be beneficial for increasing the successfulnessof transplanting in deeper areas. Earlier plantingmay allow more time to overcome transplantshock and adapt to the available light conditions.Size of plant or perennial structure can influenceplant health and ability to withstand transplantshock (Zimmerman et al. 1995), however this vari-able was not measured during our study.

Our study showed that transplanting sub-mersed aquatic macrophytes can be successful asa means of restoring the littoral community innorthern climates. However, before an aquaticmacrophyte restoration is attempted, the eco-logical stressors that prohibit the natural recruit-ment of macrophytes, the population of carp inour case, need to first be addressed (Smart et al.2005). Success should be evaluated over severalyears as success during the initial year of trans-planting did not ensure long-term establishment.Sustained water clarity throughout the growing

season is needed to maximize the survival andexpansion of transplants and the depth of suc-cessful transplants.

Acknowledgments

This research was funded by the Riley Purgatory BluffCreek Watershed District with additional support from theUSDA National Institute of Food and Agriculture, Hatchgrant MIN-41-074. We thank James Johnson, Ajay Jones,Jonathan JaKa, Holly Sigler, and Teran Smith for assistancewith data collection and Dr. Peter W. Sorensen, Dr. DavidBiesboer, Dr. Przemek Bajer, and the watershed district forsharing data, lab, and field resources. Drs. SusanGalatowitsch and Peter Sorensen provided helpful input onearly versions of this manuscript. Comments by thereviewers and Associate Editor helped us improvethe manuscript.

References

Bajer PG, Sorenson PW. 2012. Using boat electrofishing toestimate the abundance of invasive common carp insmall Midwestern lakes. N Am J Fish Manage.32:817–822. doi:10.1080/02755947.2012.690822.

Bajer PG, Sorensen PW. 2015. Effects of common carp onphosphorus concentrations, water clarity, and vegetationdensity: a whole system experiment in a thermally strati-fied lake. Hydrobiologia. 746:303–311. doi:10.1007/s10750-014-1937-y.

Bajer PG, Sullivan G, Sorenson PW. 2009. Effects of a rap-idly increasing population of common carp on vegetationcover and waterfowl in a recently restored Midwesternshallow lake. Hydrobiologia. 632:235–245. doi:10.1007/s10750-009-9844-3.

Baker LA, Newman RM. 2014. Managing the biological, eco-nomic, and social aspects of sustainability of lake ecosys-tems. In: Ajuha S, editor. Comprehensive water quality andpurification Volume 4. Amsterdam: Elsevier. p. 76–86.

Barko JW, Smart RM. 1981. Comparative influences of lightand temperature on the growth and metabolism ofselected submersed freshwater macrophytes. EcolMonogr. 51:219–235. doi:10.2307/2937264.

Barko JW, Smart RM. 1986. Sediment related mechanismsof growth limitation in submerged macrophytes. Ecology.67:1328–1340. doi:10.2307/1938689.

Borman S, Korth R, Temte J. 2014. Through the lookingglass: a field guide to aquatic plants. 2nd ed. WisconsinLakes Partnership, Stevens Point, WI.

Dick GO, Smart RM, Gilliland ER. 2004a. Aquatic vegeta-tion restoration in Arcadia Lake, Oklahoma: a case study.ERDC/EL TR-04-7. Lewisville Aquatic EcosystemResearch Facility. Lewisville (TX): U.S. Army EngineerResearch and Development Center.

Dick GO, Smart RM, Smith JK. 2004b. Aquatic vegetationrestoration in Cooper Lake, Texas: a case study. ERDC/

10 J. M. KNOPIK AND R. M. NEWMAN

Page 12: Transplanting aquatic macrophytes to restore the littoral community … · 2018. 9. 28. · (Smart et al. 1996). Previous studies have used bar-riers such as wire mesh (Smart et al.

EL TR-04-5. Lewisville Aquatic Ecosystem ResearchFacility. Lewisville (TX): U.S. Army Engineer Researchand Development Center.

Doyle RD 2001. Effects of waves on the early growth ofVallisneria americana. Freshwat Biol. 46:389–397.doi:10.1046/j.1365-2427.2001.00668.x.

Doyle RD, Smart RM, Guest C, Bickel K. 1997.Establishment of native aquatic plants for fish habitat:test plantings in two north Texas reservoirs. Lake ReservManage. 13:259–269. doi:10.1080/07438149709354317.

Fleming JP, Madsen JD, Dibble ED. 2011. Macrophyte re-establishment for fish habitat in Little Bear CreekReservoir, Alabama, USA. J Freshwat Ecol. 26:105–114.doi:10.1080/02705060.2011.553925.

Fleming JP, Madsen JD, Dibble ED. 2012. Development of aGIS model to enhance macrophyte re-establishment projects.Appl Geogr. 32:629–635. doi:10.1016/j.apgeog.2011.07.013.

Hanson M, Butler M. 1994. Responses of plankton, turbid-ity, and macrophytes to biomanipulation in a shallowprairie lake. Can J Fish Aquat Sci. 51:1180–1188.doi:10.1139/f94-117.

Horppila J, Nurminen L. 2003. Effects of submerged macro-phytes on sediment resuspension and internal phosphorusloading in Lake Hiidenvesi (southern Finland). Water Res.37:4468–4474. doi:10.1016/S0043-1354(03)00405-6.

James WF, Best EP, Barko JW. 2004. Sediment resuspensionand light attenuation in Peoria Lake: can macrophytesimprove water quality in this shallow system? Hydrobiologia.515:193–201. doi:10.1023/B:HYDR.0000027328.00153.b2.

Keeney DR, Nelson DW. 1982. Nitrogen–inorganic forms.In: Page AL et al., editor. Methods of soil analysis: part 2,chemical and microbiological properties. 2nd ed.Madison (WI): American Society of Agronomy and SoilScience Society of America. p. 643–698.

Knopik JM 2014. Aquatic macrophyte response to carpremoval and the success of transplanting aquatic macro-phytes to restore the littoral community. MS thesis.University of Minnesota: Minneapolis (MN).

Lauridsen TL, Jeppesen E, Sodergaard M. 1994.Colonization and succession of submerged macrophytesin shallow Lake Vaeng during the first five years follow-ing fish manipulation. Hydrobiologia. 275:233–242.doi:10.1007/BF00026714.

Lauridsen TL, Sandsten H, Moller PH. 2003. The restor-ation of a shallow lake by introducing Potamogeton spp.:the impact of waterfowl grazing. Lakes Reserv ResManage. 8:177–187. doi:10.1111/j.1440-1770.2003.00224.x.

Lougheed VL, Theysmeyer TS, Smith T, Chow-Fraser P.2004. Carp exclusion, food-web interactions, and the res-toration of Cootes Paradise Marsh. J Great Lakes Res.30:44–57. doi:10.1016/S0380-1330(04)70328-7.

Madsen JD 1991. Resource allocation at the individual plantlevel. Aquat Bot. 41:67–86. doi:10.1016/0304-3770(91)90039-8.

Madsen JD 1997. Methods for management of nonindige-nous aquatic plants. Assessment and Management ofPlant Invasions. SectionIII:145–171. doi:10.1007/978-1-4612-1926-2_13.

Madsen JD 1999. Point intercept and line intercept methodsfor aquatic plant management. Vicksburg (MS): US ArmyEngineer Research and Development Center, Aquatic PlantControl Technical Note (TN APCRP-M1-02).

NOAA. 2012. Local climate data, Minneapolis, Minnesota,May and June 2012. https://www.ncdc.noaa.gov/IPS/lcd/lcd.html. Asheville (NC): National Climate Data Center.

R Development Core Team. 2011. R: a language and envir-onment for statistical computing. Vienna, Austria: RFoundation for Statistical Computing. ISBN 3-900051-07-0 URL http://www.R-project.org.

Scheffer M 1998. Ecology of shallow lakes. New York (NY):Chapman and Hall.

Schrage LJ, Downing JA. 2004. Pathways of increased waterclarity after fish removal from Ventura Marsh; a shallow,eutrophic wetland. Hydrobiologia. 511:215–231.doi:10.1023/B:HYDR.0000014065.82229.c2.

Smart RM, Dick GO, Doyle RD. 1998. Techniques forestablishing native aquatic plants. J Aquat Plant Manage.36:44–49.

Smart RM, Dick GO, Snow JR. 2005. Update to the propa-gation and establishment of aquatic plants handbook.ERDC/EL TR-05-4. Lewisville Aquatic EcosystemResearch Facility. Lewisville (TX): U.S. Army EngineerResearch and Development Center.

Smart RM, Doyle RD, Madsen JD, Dick GO. 1996.Establishing native submersed aquatic plant communitiesfor fish habitat. Am Fish Soc Symposium. 16:347–356.

Smiley PC, Dibble ED. 2006. Evaluating the feasibility ofplanting aquatic plants in shallow lakes in the Mississippidelta. J Aquat Plant Manage. 44:73–80.

Sondergaard M, Jensen J, Jeppesen E. 2003. Role of sedi-ment and internal loading of phosphorus in shallowlakes. Hydrobiologia. 506(1–3):135–145. doi:10.1023/B:HYDR.0000008611.12704.dd.

Sponberg AF, Lodge DM. 2005. Seasonal below ground her-bivory and a density refuge from waterfowl herbivory forVallisneria americana. Ecology. 86:2127–2134.doi:10.1890/04-1335.

Storch TA, Winter JD, Neff C. 1986. The employment ofmacrophyte transplanting techniques to establishPotamogeton amplifolius beds in Chautauqua Lake, NewYork. Lake Reserv Manage. 2:263–266. doi:10.1080/07438148609354640.

Vanderbosch DA, Galatowitsch SM. 2011. Factors affectingthe establishment of Schoenoplectus tabernaemontani(C.C Gmel.) Palla in urban lakeshore restorations.Wetlands Ecol Manage. 19:35–45. doi:10.1007/s11273-010-9198-7.

Weber MJ, Brown ML. 2009. Effects of common carp onaquatic ecosystems 80 years after “Carp as a Dominant”:ecological insights for fisheries management. Rev FishSci. 17:524–537. doi:10.1080/10641260903189243.

Zimmerman RC, Reguzzoni JL, Alberte RS. 1995. Eelgrass(Zostera marina L.) transplants in San Francisco Bay: roleof light availability on metabolism, growth, and survival.Aquat Bot. 51:67–86. doi:10.1016/0304-3770(95)00472-C.

LAKE AND RESERVOIR MANAGEMENT 11