The effect of freeze-thaw cycles on phosphorus release...

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Canadian Water Resources Journal / Revue canadiennedes ressources hydriques

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The effect of freeze-thaw cycles on phosphorusrelease from riparian macrophytes in cold regions

Colin J. Whitfield, Nora J. Casson, Rebecca L. North, Jason J. Venkiteswaran,Osama Ahmed, Jeremy Leathers, Katy J. Nugent, Tyler Prentice & Helen M.Baulch

To cite this article: Colin J. Whitfield, Nora J. Casson, Rebecca L. North, Jason J. Venkiteswaran,Osama Ahmed, Jeremy Leathers, Katy J. Nugent, Tyler Prentice & Helen M. Baulch (2019):The effect of freeze-thaw cycles on phosphorus release from riparian macrophytes in coldregions, Canadian Water Resources Journal / Revue canadienne des ressources hydriques, DOI:10.1080/07011784.2018.1558115

To link to this article: https://doi.org/10.1080/07011784.2018.1558115

Published online: 10 Feb 2019.

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The effect of freeze-thaw cycles on phosphorus release from riparianmacrophytes in cold regions

Colin J. Whitfielda, Nora J. Cassonb, Rebecca L. Northc , Jason J. Venkiteswarand , Osama Ahmeda,Jeremy Leathersb, Katy J. Nugenta, Tyler Prenticed and Helen M. Baulcha

aSchool of Environment and Sustainability & Global Institute for Water Security, University of Saskatchewan, Saskatoon, Phone: 306-966-2655; bDepartment of Geography, University of Winnipeg, Winnipeg; cSchool of Natural Resources, University of Missouri,Columbia, MO, USA; dDepartment of Geography and Environmental Studies, Wilfrid Laurier University, Waterloo, ON

ABSTRACTStorage and removal of nutrients by wetlands and riparian areas is an important process in under-standing catchment nutrient fluxes and in helping to mitigate current issues of eutrophication inmany regions. In cold climates, strong seasonality affects natural wetlands and those constructedfor water treatment alike, raising important questions about how ecosystems can be managed tomaximize nutrient retention in the landscape, particularly in light of rapid and ongoing wetlandloss. This study assessed how freeze-thaw cycles (FTCs) affect the release of phosphorus (P) fromcommon riparian macrophytes (Typha spp). The goal was to understand whether the freeze-thawprocesses could drive enhanced nutrient release as has been shown for agricultural residues, butwhich has not previously been assessed in riparian vegetation. Given the rapid expansion ofPhragmites australis in parts of the study area, this study also tested the effects of FTC on P releasefrom Phragmites tissue. A common experimental protocol was used across 11 wetlands in threeregions of Canada. These results demonstrate the potential for FTCs to induce P release frommacrophyte tissue, although this is not observed in all cases. The impact of FTCs on P release wasgreatest and most consistent when samples were collected earlier in the growing season. Releaserates were positively correlated with plant P content. This suggests that the degree of plant senes-cence may play a role in determining the response to FTCs. Typha and Phragmites showed similarresponses to FTCs, suggesting that the importance of this process does not depend on the domin-ant taxon. Sequential FTCs led to further enhancement of P release from macrophyte tissue. Theresults from this study suggest that specific management such as harvesting Typha during thegrowing season, may mitigate the potential for P release due to FTCs.

RESUM�ELe stockage et la s�equestration des nutriments par les zones humides et ripariennes ont des effetsimportants sur les flux de nutriments et doivent être compris si l’on souhaite r�esoudre les probl�emesactuels d’eutrophisation. Dans les climats froids, une forte saisonnalit�e impacte �a la fois les zoneshumides naturelles et celles construites pour le traitement de l’eau. Cela pose des questions impor-tantes sur la façon dont il faut g�erer les �ecosyst�emes pour maximiser leur capacit�e �a retenir les nutri-ments, en particulier dans le contexte o�u la superficie des zones humides diminue rapidement. Cette�etude a �evalu�e comment les cycles de gel-d�egel (CGD) impactent la remobilisation du phosphore (P)par Thypa ssp, un macrophyte riparien commun. Son but �etait de mieux comprendre si le processusde gel-d�egel peut conduire �a une remobilisation accrue des nutriments, comme c’est le cas pour lesr�esidus agricoles. �Etant donn�e l’expansion rapide de Phragmites australis dans certaines portions dusite d’�etude, l’�etude a aussi test�e l’effet des CGD sur la remobilisation du P depuis les tissus dePhragmites. Un protocole exp�erimental commun a �et�e utilis�e sur 11 zones humides dans 3 r�egions duCanada. Nos r�esultats d�emontrent que, dans certains cas, les CGD ont le potentiel de remobiliser le Pdes tissus de macrophytes. L’impact des CGD sur la remobilisation du P �etait plus �elev�e et plussyst�ematique dans les �echantillons pr�elev�es tôt dans la saison de croissance. Les taux de remobilisa-tion �etaient positivement corr�el�es avec la teneur en P des tiges. Cette observation sugg�ere que ledegr�e de s�enescence joue probablement un rôle dans la r�eponse de P au CGD. Typha et Phragmitesont montr�e des r�eponses similaires au CGD, ce qui sugg�ere que le processus de remobilisation ned�epend pas du taxon. Une succession de CGD a provoqu�e une remobilisation accrue du P depuis lestissus de macrophytes. Ces r�esultats sugg�erent que des actions cibl�ees, comme la r�ecolte du Typhadans la saison de croissance, pourraient att�enuer la remobilisation du P par les CGD.

ARTICLE HISTORYReceived 22 December 2017Accepted 24 October 2018

KEYWORDSFreeze-thaw cycles; nutrientrelease; nutrient release;nutrient retention;Phragmites; Typha; wetlands

CONTACT Colin J. Whitfield [email protected]� 2019 Canadian Water Resources Association

CANADIAN WATER RESOURCES JOURNAL / REVUE CANADIENNE DES RESSOURCES HYDRIQUEShttps://doi.org/10.1080/07011784.2018.1558115

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Introduction

Eutrophication is the process of nutrient enrichmentthat leads to changes in ecosystem structure and serv-ices. Eutrophication can be a slow, natural process.However, anthropogenic activities such as mining ofphosphorus (P) bearing minerals for fertilizer, industrialfixation of nitrogen (N) and subsequent application tosoils, animal husbandry practices and use of organic fer-tilizer, and associated agricultural and urban develop-ment has accelerated eutrophication across much of theworld. Cultural eutrophication is now broadly seen asthe most significant threat to freshwater quality(Schindler 2006; Baulch 2013). Wetland and riparianareas at the land-water interface receive water, sedi-ments, and nutrients from up-slope. The combinationof abundant nutrients and access to water facilitate thegrowth of hydrophilic vegetation. Macrophytes thatgrow in these areas, including Typha (cattail) spp. andPhragmites (reed) spp. have a strong ability to retainnutrients (Johnston 1991), so much so that constructedwetlands often use these plants as an affordable and effi-cient method of treating wastewater (Ciria et al. 2005;Rycewicz-Borecki et al. 2017). Both Typha andPhragmites are large, perennial emergent macrophytes,which are considered cosmopolitan taxa, dominant inmany regions and increasing in their dominance(Childers et al. 2003; Zedler and Kercher 2004; Shih andFinkelstein 2008; Olson et al. 2009). Both are consideredas nuisance taxa, or even invasive, and can spread rap-idly, forming large, monospecific stands. Phragmites canoutcompete and displace Typha leading to rapidchanges in emergent macrophytes in some regions fromone ‘nuisance’ taxa to a new one (Findlay et al. 2002).

Complicating matters is the hybridization of thenative Typha latifolia and the introduced Typha angus-tifolia to Typha� glauca. This hybrid often out-com-petes its parent species for wetland space (Kuehn andWhite, 1999; Waters and Shay, 1990, 1992; Tuchmanet al. 2009). Identification of the two species andhybrids is not always simple based on morphometry(Kuehn and White, 1999). Moreover, increasednutrients in wetlands can shift the dominant Typhaspp. (Woo and Zedler 2002), while Typha� glaucainvasion has made nutrient management difficult alongthe coasts of the Laurentian Great Lakes (Angeloniet al. 2006; Tuchman et al. 2009). Phragmitis australissubsp. americanus has also faced an invasive subspecies,Phragmitis australis subsp. australis, as well as potentialhybridization (Meyerson et al. 2010) with associatedeffects on nutrients (Kettenring et al. 2011).

While wetlands are considered hotspots of nutrientcycling and often valued for the ecosystem service of

nutrient removal, they can also serve as temporarystorage or sources of nutrients (Fisher and Acreman2004; Haidary and Nakane 2009; Marton et al. 2015;Cheng and Basu 2017). In northern environments,strong seasonality can impact the transport andcycling of nutrients (Baulch et al. in review); however,remarkably little is known about winter changes innutrient cycling or what drives seasonal variation inchemistry and nutrient retention capacity across mostaquatic ecosystems (Hampton et al. 2017). Winter isoften considered a relatively quiescent period, whenbiological processes slow due to low temperature, andopen water areas are often covered by a significantlayer of ice and snow. This impedes photosynthesisand can contribute to anoxia in shallow systems thatdo not freeze to the bottom (Mathias and Barica1980; Bertilsson et al. 2013; Pernica et al. 2017). Assuch, nutrient removal capacity can be low, andincreased nutrient concentrations may be observed(Catalan 1992; Lawniczak et al. 2016), creating chal-lenges for the use of wetlands to retain nutrients innorthern environments.

One major driver of these changes may be due tothe seasonality of macrophyte growth. Macrophytescan both store and release large masses of nutrients(Murkin et al. 1989). They often reach peak biomassin mid or late summer (Murkin et al. 1989; Asaedaet al. 2002; Grosshans 2014). Seasonal changes in Pstorage also occur. For example, Typha spp. tend tohave peak tissue P concentrations around the time ofpeak biomass in summer, then tissue content declinesin fall as P is translocated to roots. In cold-temperateregions, there is evidence that tissue P can furtherdecline in winter, with median tissue P contentdeclining by half from fall to a minima in spring(Grosshans 2014).

The decomposition of macrophyte tissue is knownto occur in several stages. Rapid P release is oftenassociated with leaching from the tissue over periodsfrom hours to days, followed by microbial coloniza-tion facilitating continued, albeit slower nutrientrelease, and finally the slow release of more refractorystructural materials (Webster and Benfield 1986). Insome cases, particularly for N, short-term immobiliza-tion can also occur (Webster and Benfield 1986). It ispoorly known how freeze-thaw cycles (FTCs) mayimpact the release of P from macrophyte tissue inwetlands. There is clear evidence that FTCs canimpact nutrient release from vegetation (e.g.,Roberson et al. 2007), including agricultural residues(Timmons et al. 1970; Elliott 2013; Lozier et al. 2017),catch crops (Liu et al. 2013), and natural terrestrial

2 C. J. WHITFIELD ET AL.

vegetation (White 1973). Cell expansion and lysingduring freezing is the likely mechanism. MultipleFTCs can lead to greater nutrient mobilization than asingle FTC (Bechmann et al. 2005; Liu et al. 2013),though plant species plays an important role (Lozieret al. 2017). Nutrient-rich crop residues are associatedwith higher rates of release (Elliott 2013); however,little is known about the impact of FTCs on wetlandnutrient cycling or how FTCs affect the capacity ofriparian vegetation to retain nutrients.

In cold continental regions of North Americawhere wetland macrophytes can experience repeatedFTCs for notable portions of the year (e.g., Ontario),and in cold semi-arid areas where runoff is predom-inantly generated from snowmelt (e.g., Canadian prai-ries), nutrient release from wetland and riparianplants during thaw may influence aquatic nutrientexport. This is an important consideration in agricul-tural settings where riparian buffer zones are used tomitigate nutrient release into freshwaters (Sharpleyet al. 2015). This study assesses how freezing andthawing of plant tissue affects nutrient release fromaquatic macrophytes collected from riparian areas indifferent regions of Canada, with the prediction thatFTCs induce higher rates of P release from Typhaspp., a taxa found across all sites. Noting the rapidexpansion of the invasive Phragmites australis subsp.australis and replacement of Typha spp. with thehybrid Typha� glauca and P. australis in Ontario(Wilcox et al. 2003), freeze-thaw induced nutrientrelease from this plant was also investigated. Thisstudy aimed to determine whether factors includingdifferences in P concentrations in plant tissues(Findlay et al. 2002; Rycewicz-Borecki et al. 2017), thepresence of standing water, and the number and sea-sonal timing of FTCs are associated with differencesin freeze-thaw induced P release rates.

Methods

Study sites

Study sites were selected on the basis of landownerpermission and presence of the vegetation types ofinterest. Eleven wetlands featuring emergent macro-phytes (Typha spp., Phragmites australis) weresampled in three Canadian provinces (Table 1). InOntario (ON), four suburban wetlands in the LaurelCreek watershed, City of Waterloo, were selected fortheir Typha and Phragmites communities. Here Typhawere all Typha� glauca as per Smith (1986) andKuehn and White (1999). Phragmites were identifiedas Phragmites australis subsp australis as perSaltonstall et al. (2004). All sites are on the WaterlooMoraine or adjacent till plains (Bajc et al. 2014; Vealeet al. 2014) and have little to no standing water. InManitoba (MB), two riparian wetlands adjacent tostreams and two seasonally-stagnant drainage ditcheswere selected within the city of Winnipeg, all ofwhich are dominated by Typha� glauca and arelocated on clayey glaciolacustrine deposits (Matileet al. 2000). In Saskatchewan (SK), three Typha latifo-lia dominated wetlands in a semi-arid agriculturalregion featuring relatively flat topography to thesouthwest of the city of Saskatoon were investigated.

Field sampling

Each site was sampled in fall of 2016. Sites in ONand MB were sampled prior to snowfall, while SKsites were sampled in mid-October following a transi-ent snowfall event. Repeat sampling during winterand the following summer was conducted at one ofthe SK sites (Table 1). At each wetland, three (repli-cate) quadrats (1m2) were placed haphazardly andused to demarcate the areas for vegetation extraction.Where both macrophyte species were present, three

Table 1. Study site locations, land use, sampling dates, total dissolved phosphorous (TDP) concentrations in surface waters dur-ing site visits, and mean annual and October minimum air temperature. Sites for which there was no standing water at time ofsampling are denoted by NSW.

Site Province Latitude Longitude Land use Date TDP (mg L–1) Annual (�C)October

minimum (�C)DD MB 49.89 –97.03 Urban 10-06-2016 0.26 3.0 –0.5OC MB 49.91 –97.21 Urban 10-14-2016 0.53 3.0 –0.5OMD MB 49.88 –97.19 Urban 09-29-2016 0.35 3.0 –0.5TC MB 49.89 –97.23 Urban 10-14-2016 0.13 3.0 –0.5BW ON 43.48 –80.56 Suburban 10-07-2016 NSW 7.0 2.9CF ON 43.47 –80.57 Suburban 10-28-2016 NSW 7.0 2.9CW ON 43.47 –80.56 Suburban 11-02-2016 NSW 7.0 2.9LBE ON 43.47 –80.58 Suburban 10-18-2016 NSW 7.0 2.9KR SK 51.96 –107.02 Agricultural 10-15-2016 0.02 3.3 –1.4WF SK 51.97 –106.93 Agricultural 10-15-2016 (fall), 11-25-2017

(winter), 07-17-2017 (summer)0.4 3.3 –1.4

WSA SK 51.91 –106.96 Agricultural 10-15-2016 0.08 3.3 –1.4

CANADIAN WATER RESOURCES JOURNAL / REVUE CANADIENNE DES RESSOURCES HYDRIQUES 3

quadrats were used for each type. Plant density wasdetermined by counting standing plants in the quad-rat and a minimum of 25 Typha or Phragmites wereremoved from each quadrat by cutting the plant fromits base (soil or sediment). The vegetation was trans-ported back to the laboratory and stored at 4 �C. Abulk surface water sample was collected for nutrientanalyses in HDPE bottles, filtered (0.45 mm), andstored at 4 �C until analysis.

Laboratory analysis

Experimental treatment. The base of each plant wascut to length (0.15m) to standardize the plant mater-ial being used in the experiment to that most likely tobe submerged and undergo freezing (preliminary test-ing indicated that P release for different plant parts,including leaves, exposed to FTC was similar, whilework by Grosshans (2014) on the distribution of P inabove-ground biomass also supports such anapproach), and excess material discarded. Five Typhafrom each quadrat were placed in 1 L HDPE bottlesand randomly assigned to a wet control (WC) or wettreatment (WT) replicate. Phragmites were treated inthe same way, except that more than five plants weretypically used owing to smaller mass of individualplants. Wet weight of biomass was measured for eachreplicate and 700mL MilliQ water (approximately40mL per g dry biomass on average) was added toeach bottle to cover the plant material. Bottles wereagitated at low speed (80 rpm) using an orbital shakerfor 1 hr, to simulate plant movement in a field setting(e.g. wind, water). The WT samples were placed inthe freezer at –20 �C or –40 �C for 24 hr and thenthawed for approximately 48 hr at room temperature.The WC samples were stored in the refrigerator(4 �C), until near the end of the thaw, when theywere removed to bring both sample treatments toroom temperature. At the conclusion of the FTC,both WT and WC were shaken (as above) and a smallvolume of water was withdrawn for analysis. At theconclusion of all FTCs, plants were oven-dried at60 �C for 48 hr and weighed for dry tissue mass; wetand dry biomass weights were used to calculate plantmoisture content (% dry weight) at each site at thetime of sampling.

Additional analyses were conducted on the samplesfrom the ON sites. The three ON sites featuringTypha (BW, CF, CW) were subjected to two add-itional FTCs, where both WC and WT were stored at4 �C until initiation of the subsequent FTC (withinapproximately one week of start of initial FTC). Aknown volume of water was withdrawn after each

FTC; the water volume in the bottle at each samplingjuncture was used to normalize the data (describedbelow). Because the macrophytes harvested in ONwere growing in locations with no standing water, theexperimental protocol was repeated under dry condi-tions. The plants from these dry sites (termed drytreatment; DT) were placed in bottles without anywater, frozen for 24 hr and thawed as above. The drycontrol (DC) replicates were left in the fridge (4 �C)for the duration of experiment. At the conclusion ofthe FTC, 700mL of MilliQ water was added to bothDC and DT. The samples were shaken as above and asmall, known volume of water withdrawn for analysis.

Chemical analyses. Bulk surface water samples andexperimental samples were filtered through 0.45 mmnon-sterile nylon syringe-tip filters. Total dissolvedphosphorus (TDP) was analyzed colorimetricallyusing a SmartChem 170 (Westco Scientific InstrumentsInc., now Unity Scientific Inc.) as per EPA Method365.1 (O’Dell 1993).

Dried biomass was analyzed for P content follow-ing Hutchinson et al. (1999). Briefly, a subsample(0.2 g) was ground (mortar and pestle), dissolved in2.5mL 6N HNO3 overnight at room temperature inPyrex tubes, heated to 100 �C for 8 hr, cooled, andfiltered (Whatman No. 42, 2.5 mm nominal pore size).Samples were then diluted to 50mL with MilliQ waterand analyzed colorimetrically, as above.

Data analysis

All P concentration data were converted to P releasenormalized to the volume of water in each samplebottle and the dry biomass of plant tissue in order toaccount for site and species differences:

TDP mg g–1� � ¼ TDP mg L

–1� ��Volume Lð ÞDry biomass gð Þ (1)

All calculations, statistical tests (agricolae package,de Mendiburu 2016), and graphics development(ggplot2 package, Wickham 2009) were performed inR (R core team 2016). A non-parametric ANOVAwith blocking and post-hoc tests (Friedman test) wasused to test for significant differences betweentreatments. A Kruskal-Wallis test was used to test forsignificant differences among seasons at a single site.A Spearman rank correlation test was used to assessthe relationship between TDP release and plant Pcontent. An alpha value of 0.05 was used for all tests.


Results

Overall, P release from Typha collected in fall wassomewhat enhanced by the experimental wet freeze-thaw treatment, although this response varied byregion. When blocking by site, the difference betweencontrol (median across all sites ¼ 4.13x10�3mg g�1)and treatment (median ¼ 9.54x10�3mg g�1) sampleswas not significant (p¼ 0.21). The ON sites demon-strated a consistent, strong response to the freeze-thaw treatment, while the response at the MB and SKsites was mixed. Several sites (e.g., WF, KR, TC) dem-onstrated considerable variability in TDP release(Figure 1). At the ON sites, where there was nostanding water, there were significant pair-wise differ-ences between all treatments (DC, DT, WC, WT;p¼ 0.03); both the wet (median ¼ 5.96x10�3mg g�1)and dry (median ¼ 4.38x10�3mg g�1) treatmentsreleased significantly more TDP compared with theirrespective controls (WC median ¼ 2.43x10�3mg g�1;DC median ¼ 2.99x10�3mg g�1; Figure 2).

The effect of the wet freeze-thaw treatment was con-sistent across species (Typha and Phragmites) at the ONsites. When blocking by site and species in this region,WT samples released significantly more TDP than didWC samples (p¼ 0.01; Figure 3). There was no signifi-cant difference in the TDP release rate per gram of tis-sue, even given the morphological differences betweenthe two species (Typha median ¼ 5.96x10�3mg g�1;

Phragmites median ¼ 3.75x10�3mg g�1; p¼ 0.32;Figure 3). In the experiment where Typha from the ONsites were exposed to multiple FTCs, there was signifi-cantly more TDP released with each subsequent freez-ing and thawing (p¼ 0.050; Figure 4). Notably, theincrease from FTC two to three was generally lowerthan from FTC one to two (Figure 4).

Given the more muted response of sites located incolder and more northerly regions, the timing of sam-pling and the P content of Typha tissue were consid-ered as possible factors contributing to the rate ofTDP release following FTCs. Moisture content, usedhere as a proxy for the initial condition of the planttissue, was similar among the samples collected in thefall, for each species (Table 2). For one of the SK sites(WF), Typha were sampled in October, November,and again the following July (Table 1). There wasgreater variability in the TDP released from plant tis-sue collected in fall (October, November), than insummer (July) when moisture content of the tissuewas much higher. Plant tissue collected in fall mayhave lower propensity for nutrient release, but thisresult was not significant (p¼ 0.06; Figure 5). Therewas a strong, significant correlation between plant Pcontent and TDP release following wet freeze-thawtreatment (r¼ 0.84, p< 0.01; Figure 6), but no clearsignal that plant P content was driven by region,given that there was considerable variability in plantP within regions.

Figure 1. Total dissolved phosphorus (TDP) release normalized to Typha dry tissue mass undergoing wet control (WC) and wetfreeze-thaw (WT) treatments (WF fall sampling only). Site names are in headings (full description in Table 1) and shading denotesprovince of collection.


Discussion

Freeze-thaw induced phosphorus releasefrom Typha

Macrophytes are an important, yet temporary site ofnutrient storage (Boyd 1970). Nutrient release frommacrophyte tissue is classically described in three phases,starting with rapid leaching, then microbial colonizationand slower release, and finally, slow breakdown of more

refractory tissues (Webster and Benfield 1986). Theresults of this study suggest that FTCs can also influenceP release from macrophyte tissue. The freeze-thaw pro-cess accelerates nutrient release within both Typha andPhragmites, although it was not observed at all sitesacross the three study regions. These results build on thegrowing body of evidence from cold regions demonstrat-ing the importance of FTCs to the release of nutrientsfrom plant material (Timmons et al. 1970; White 1973;

Figure 2. Total dissolved phosphorus (TDP) release normalized to Typha dry tissue mass undergoing dry control (DC), dry treatment(DT), wet control (WC) and wet freeze-thaw (WT) treatments for the ON sites only (site names in headings).

Figure 3. Total dissolved phosphorus (TDP) release normalized to Typha or Phragmites dry tissue mass undergoing wet control(WC) and wet freeze-thaw (WT) treatments (ON sites only).


Bechmann et al. 2005; Roberson et al. 2007; Elliott 2013;Lozier et al. 2017). The second sequential FTC resultedin an increase in TDP concentrations relative to the ini-tial, but the increase in TDP following the third sequen-tial FTC was only marginally higher than the releasefollowing the second. Consecutive FTC’s impact on Pconcentrations are varied in the literature, with resultsranging from significant increase along a logarithmicscale with the number of FTCs, up to six freezing cycles(Bechmann et al. 2005), to P increase only after the initialFTC (Riddle and Bergstr€om 2013). In much of theCanadian Prairie provinces, wetlands are frozen fornearly half the year, with many shallow wetlands freezingto the bottom, and only the deep pothole wetlands main-tain liquid water under the ice. Emergent tissue is likelyto undergo many FTCs annually, and even tissue that is

underwater or in shallow sediments can be susceptible toat least one FTC.

Seasonality of nutrient dynamics within Typha

Freeze-thaw induced nutrient release from plant tissueis thought to be caused by cell lysis (White 1973).Thus, the observed difference among sites may relateto the state of the plant tissue and its nutrient con-centrations, which dictate the maximum rate ofrelease. In samples from SK, healthy, turgid tissuessampled in summer show the greatest susceptibility toFTC induced release and the highest nutrient content,prior to fall reallocation of nutrients. While themonthly differences were not statistically significant(p¼ 0.06), the marginally lower TDP release in thecooler months suggests a potential dependence on tis-sue nutrient content and availability. The significantrelationship between TDP release and Typha P con-tent (Figure 6) provides further support of this con-cept. These explanations could account for theobserved spatial differences in susceptibility to FTC.The prairie (MB and SK) sites demonstrated greatervariability in TDP release, indicating that macrophytescould be at different stages of senescence and/ortranslocation. Samples from ON showed a consistentresponse to freeze-thaw cycling. This is the mostsoutherly of the sites, where the seasonal reallocationof nutrients to the roots is likely to occur later. Incontrast, the SK sites had been subject to a short

Figure 4. Total dissolved phosphorus (TDP) release for sequential wet freeze-thaw (WT) treatments normalized to Typha dry tis-sue mass (ON sites bearing Typha only).

Table 2. Average moisture content of Phragmites and Typhatissue at time of sampling for each study site.Site Date Species Moisture content (% dry weight)

DD 10-06-2016 Typha 393OC 10-14-2016 Typha 416OMD 09-29-2016 Typha 203TC 10-14-2016 Typha 359BW 10-07-2016 Phragmites 36.9BW 10-07-2016 Typha 186CF 10-28-2016 Phragmites 73.4CF 10-28-2016 Typha 259CW 11-02-2016 Typha 216LBE 10-18-2016 Phragmites 39.7KR 10-15-2016 Typha 466WF 10-15-2016 Typha 316WF 11-25-2017 Typha 368WF 07-17-2017 Typha 1.08x103

WSA 10-15-2016 Typha 427


snowfall prior to the fall sampling, and MB sites expe-rienced several sub-zero nights.

In conjunction with tissue health, allocation of Pbetween above-ground plant tissue and roots couldexplain the observed temporal and spatial differences.The representation of tissue P concentrations in the baseof the plants only, may not fully represent changes in Pconcentrations. At the end of the growing season, P is

typically stored in below-ground plant roots (Adhikariet al. 2011). In the Canadian prairies, large amounts of Pmay already be allocated to the roots when FTC occur.This study targeted above-ground biomass on the prin-ciple that soil will insulate below-ground biomass forparts of the year, and therefore, these results do notaccount for P loss from roots due to FTC. Sedimentnutrient concentrations, which can be correlated with

Figure 5. Total dissolved phosphorus (TDP) release (normalized to dry tissue mass) from Typha collected from one site in SK(WF) during different seasons. Data shown are TDP release after one wet freeze-thaw (WT) cycle.

Figure 6: Total dissolved phosphorous (TDP) release from Typha undergoing a wet freeze-thaw treatment relative to total TyphaP content (both normalized to dry tissue mass).


water column and plant tissue P concentrations(Adhikari et al. 2011), were not measured.

Will increasing Phragmites relative to Typhayield higher nutrient release from freeze-thaw cycles?

Despite evidence that Phragmites and Typha can differin their nutrient content and rates of decompositionand nutrient release (Murkin et al. 1989; McJannet et al.1995; Wrubleski et al. 1997; Gingerich and Anderson2011), significant differences in freeze-thaw mediated Prelease across taxa were not observed when normalizedto dry mass. Dual use in wastewater treatment plantsdemonstrates that both taxa are equivalently effective inremoving P, though significant differences in Nremoval were observed (Juwarkar et al. 1995). These P-specific results may not fully demonstrate the impactexpansion of Phragmites will have on Canadian wet-lands. Given gross differences in morphology, it issomewhat surprising that the response to FTC would beso similar between Typha and Phragmites. Of course,the potential for differences in the density and biomassof stands of the two taxa must be considered. In the cur-rent study, there were few sites with both species pre-sent, but initial comparison (of per area biomass to0.15m above soil at these sites) suggests Phragmites bio-mass was approximately twice that of Typha. Whilefreeze-thaw susceptibility does not appear to differ sig-nificantly among taxa per unit biomass, differences intheir biomass, tissue nutrient concentrations (McJannetet al. 1995), and decomposition rates (Murkin et al.1989; Findlay et al. 2002; Gingerich and Anderson2011) may have important impacts on nutrient cycling,particularly when one taxon (typically Phragmites),replaces the other, as observed recently in many parts ofOntario (Wilcox et al. 2003). In coastal areas of theLaurentian Great Lakes, declines in water levels havepromoted non-native Typha� glauca and Phragmitesestablishment (Tulbure et al. 2007; Lishawa et al. 2010)with potential for changing water quality (Mitch andWang 2000).

What are the implications of changingclimate conditions?

Changing winter conditions are expected to affect theduration of winter and frequency of FTCs, withregionally varied effects anticipated (Hayhoe et al.1992; Baker and Ruschy 1995; Bourque et al. 2005).There is predicted to be an increasing number andintensity of soil FTCs in Canada during the next 50

to 100 years (Henry 2008). Winter, while widely con-sidered a quiescent period, is one where nutrientcycling clearly differs from summer. Low autotrophicactivity is expected (Murkin et al. 1989; Hamptonet al. 2017; Pernica et al. 2017), but other changes arealso likely to be important. For example, limited mac-roinvertebrate activity and even freezing at lower tem-peratures (Frisbie and Lee 1997; Danks 2007), maydecrease decomposition rates (Brinson et al. 1981;Cummins et al. 1989). Although, high macroinverte-brate biomass (Engel 1985) may at least partially com-pensate for these differences in some ecosystems.Freeze-thaw cycles and ice-disruption of plants willhave further impacts. These winter changes overlaycurrent wet-dry cycles, which vary regionally and willvary through time. The response of Typha to FTCsconducted in submerged conditions was slightly, butstatistically significantly greater than FTCs conductedin dry conditions. This may suggest that changes tothe water regime of the ecosystem may interact withthe frequency of FTCs to determine P release frommacrophyte tissue. Where severity or duration ofdrought results in drier plant tissue, P release duringFTCs may be promoted by this prior enhanced break-down of plant tissue. Ultimately, a process-basedunderstanding of current nutrient cycles and controlsis required to allow us to anticipate change, particu-larly for taxa and processes important to amelioratingcurrent issues of degraded water quality. Whilechanging FTCs are one driver of change in wetlandsand riparian areas, understanding the interaction ofmany factors including changing water levels, taxa,and management is required to understand futurechanges in nutrient cycling and retention capacity.

Potential impacts of freeze-thaw release of Pon nutrient loading to water bodies

The three-fold increase in P release from submergedtissues suggests a potentially important impact ofFTCs on P release from two macrophyte taxa. Giventhe often slow degradation of tissues from these mac-rophytes (Findlay et al. 2002), this could represent animportant short-term acceleration of nutrient release.Although, it may not alter the total mass of P releasedfrom these macrophytes over time — only the speedand timing at which it is released. These results indi-cate that freeze-thaw induced release could stimulatea potentially important pulse of nutrient release(Figure S1), particularly from plants with high P con-tent. This pulse would occur at a time when bioticuptake processes are expected to be minimal due to


low winter temperatures and light (Catalan 1992;Hampton et al. 2017). These FTCs also occur during(and prior to) a period when nutrients can be highlysusceptible to transport — spring snowmelt (Baulchet al. in review). Of course, the importance of FTCsto nutrient release will depend on a suite of factorsincluding whether tissues are submerged (and suscep-tible to leaching) or emergent (and subject to tissuebreakdown during drying). The P content of the planttissue is also a factor, which will depend on biomasscondition, nutrient concentrations at a site, and thenumber of FTCs. In many ways, this study is a proof-of-concept, demonstrating that similar to terrestrialenvironments (Timmons et al. 1970; White 1973;Bechmann et al. 2005; Roberson et al. 2007; Elliott2013; Lozier et al. 2017), FTCs can stimulate nutrientrelease from macrophyte tissues. These experimentalmethods, which use submerged fresh plant tissue,reflect the potential for FTCs to affect the early leach-ing stage of nutrient release. While these results couldrepresent an upper limit to TDP release, due to theslow, mechanical agitation of samples, it is also pos-sible that inclusion of a broader range of plant tissue(beyond the base of the plants) and tissues higher inP content could yield TDP release above the levelsreported herein. More work is required to understandeffects of different parts of the plant (i.e., leaves,roots), and at different stages of decomposition. Forexample, there is a need to better understand thepotential impacts of FTCs in spring on the morerefractory tissues present following months of decom-position, and how winter changes in microbial com-munity may interact to affect decomposition offreezing-affected tissues. Physical damage associatedwith freezing is likely to be important in other ways,such as affecting the distribution of macrophytes(Renman 1989). Ecosystem-scale monitoring com-bined with experimental work and measurement ofkey nutrient pools, including macrophyte tissuesthrough winter, is required. This will allow for a bet-ter understanding of winter changes in nutrient con-centrations, nutrient cycling, and the impacts ofinterannual variability in winter conditions on wet-land and riparian ecosystems.

Conclusions

This research demonstrates that FTCs are an import-ant factor that may result in rapid nutrient releasefrom riparian vegetation to adjacent water bodies.The effect of FTCs is, however, mediated by factorsincluding plant condition and seasonality, site

nutrient characteristics, the frequency of FTCs, andthe presence of standing water. The results of thisstudy, spanning different regions of Canada, includingthe Lake Winnipeg and Lake Erie catchments, maysuggest the more southern sites seem more susceptibleto FTCs. However, more work is required to under-stand the interplay of seasonality, plant growth andsenescence, invasive species/hybrids, and FTCs to bet-ter understand how FTCs will impact nutrient cyclingin wetland ecosystems as a whole. Phosphorus lossduring winter from plant tissues has been previouslydocumented (Grosshans 2014), suggesting that insome ecosystems, a potentially large pool is mobilizedin this season. Given the long winters in these studyareas, the importance of this potential short-termpulse of nutrient release may be muted at an ecosys-tem scale, if slower decomposition processes continuethrough winter, and if P release rates from macro-phytes are decreased due to the earlier nutrient loss.

Phosphorus removal via plant harvesting has beenthe subject of considerable management interest(Mart�ın and Fern�andez 1992; Grosshans et al. 2014).This work concurs with past work which suggeststhat harvesting during the growing season will maxi-mize nutrient removal (Mart�ın and Fern�andez 1992;Grosshans 2014) associated with peak tissue nutrientconcentrations and prevent re-release associated withleaching, decomposition, or FTCs. The net effect maystill be positive, as within agricultural fields, themajority of P released from cover crops and wheat isretained within the field (Lozier et al. 2017).However, macrophyte winter harvest may be themore sustainable option when multiple ecosystemservices are considered because winter harvesting isexpected to minimize impacts on the ecosystem andkey taxa within it (Cicek et al. 2006). Winter is aperiod of low biotic nutrient uptake, where manyplant tissues are dormant. Decomposition of senescedtissues can require periods of months to years(Brinson et al. 1981; Findlay et al. 2002). These resultssuggest that the P release from macrophyte tissuescan be accelerated by tissue freezing and thawing.Many winter changes may affect wetland nutrientcycling in cold climates, but FTC can alter the rate ofnutrient release from tissue, and interact with otherclimate-related changes in wetland ecosystems andriparian zones.

Acknowledgements

Research was conducted as part of the LinkedUndergraduate Experiments on Nutrients (LUGNuts;Casson et al. 2018). Funding was provided by NSERC


Discovery Grant to HMB, NSERC Discovery Grant to NJC,faculty start-up (U of S) to CJW, faculty start-up (MU) toRLN, a Laurier Institute for Water Science ResearchScholarship (TP, JJV), and the Global Institute for WaterSecurity. We also thank MU undergraduate studentMatthew Sauer who contributed to the data discussion,Carlie Elliott and Kim Gilmour for assisting with analysesat the U of S, and two anonymous reviewers for helpfulsuggestions on improvements to the manuscript.

Author contributions

The study was designed by HMB, NJC, RLN, JJV and CJW. OA,JL, KN and TP conducted the data collection and compilation.CJW led the data analysis, with contributions from NJC. HMB,NJC, RLN, JJV and CJW wrote the manuscript. All authorsreviewed and provided comments on the final manuscript.

ORCID

Rebecca L. North http://orcid.org/0000-0003-3762-5939Jason J. Venkiteswaran http://orcid.org/0000-0002-6574-7071

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AbstractIntroductionMethodsStudy sitesField samplingLaboratory analysisExperimental treatmentChemical analyses

Data analysis

ResultsDiscussionFreeze-thaw induced phosphorus release from TyphaSeasonality of nutrient dynamics within TyphaWill increasing Phragmites relative to Typha yield higher nutrient release from freeze-thaw cycles?

What are the implications of changing climate conditions?Potential impacts of freeze-thaw release of P on nutrient loading to water bodiesConclusionsAcknowledgementsAuthor contributionsReferences

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