Downloaded by guest on September 24, 2021 www.pnas.org/cgi/doi/10.1073/pnas.1617454114 Marzadri Alessandra scaling in processes N subsurface and surface of Role a hsaayi eel htN N that two . reveals in zone analysis zone column benthic–water hyporheic–benthic This the the to from streams N shifts headwater and in of size source conditions. primary climatic and stream the and that , show cover, We land morphology, sizes, N N N controlling of tions in water zones and benthic, column near- zone), the (hyporheic of sediment roles streambed relative surface the of oxide understanding nitrous been limited Our gas have cation. greenhouse rivers, potent the and (N of streams sources as as reported 2017 such 16, March environments, approved and Riverine Switzerland, Lausanne, Lausanne, 2016) Federale 20, Polytechnique October Ecole review , for of (received Laboratory Rinaldo, Andrea by Edited and 46556; IN ieienetworks riverine processes natural and N activity on human of effect and the datasets quantifies hydromorphological thus, and N chemical accessible riverine scaling widely of the predictions understanding facilitates By N zone. of nature column benthic–water and the zone, N benthic–hyporheic lower the the within production from results ugs htgoa msin rmrvrn ewrspresented networks riverine from emissions the global that to suggest pre- reach with associated individual N uncertainty of the the dictions N to addition from In for network. ranging river responsible scales processes of at of parameterization production biogeochemical lack inadequate dominant a and of the data because field challenging is large high-resolution emissions a these for quantifying that responsible N understood of is is proportion denitrification it Although mediated (9). microbially rate the and exchange temperature, gas depend hydrodynamics, air–water stream that 8), dynamics (6, equilibrium with evasion, N streams on diffusive headwater through from N sphere size produced The system rivers. of to irrespective (6), transformation zones biogeochemical distinct of inter- two reflecting boundary the that ronments, upper suggests at understanding the is N Current riverine and zone zone. sat- sediment hyporheic benthic mainly fluvial and material The the water streambed found (7). between of be water band face can stream the flora of is and latter urated the the of fauna region 6), aquatic ecological (4, both the is where zone and streambed, anoxic benthic streams the of and Whereas zones inter- (2) near-subsurface) rivers. sediment–water (i.e., bulk-oxic (i.e., hyporheic and benthic both face) both within of has (3–5) occur Denitrification environments to (1). observed destruction ozone been stratospheric for (N ble oxide nitrous and (NO (N nitrate where tion, R N etrfrEoyruisRsac,Uiest fIao os,I 83702; ID Boise, Idaho, of University Research, Ecohydraulics for Center 2 2 msinpotentials emission O 2 msin rmsrasadrvr olwd fdifferent of worldwide rivers and streams from emissions O 2 )t h topeemil i irbal eitddenitrifi- mediated microbially via mainly atmosphere the to O) 2 ,wihcntttstemjrt fErhsatmosphere, Earth’s of majority the constitutes which ), dnie shtpt fmcoilymdae denitrifica- mediated microbially of been hotspots have rivers, as and streams identified as such environments, iverine 2 2 production. 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A.M., and the and M.M.D. wrote measurements; J.L.T. data; and analyzed protocols J.L.T. sampling and synoptic lished M.M.D. research; performed A.B. and t rv h ovrino oue ogse.Ti nlssshows analysis This gasses. to solutes N of that conversion activ- the biogeochemical drive and availability ity solute microbial whereas to 15–17), (5, reactants of delivery assemblagesanddeterminesresidencetimesforreactionstooccur the controls pro- N Hydrodynamics biogeochemical for and responsible model hydrodynamics Our cesses primary upscale globally. the networks to riverine identifies methodology their to a and processes proposing reach-scale rivers thereby and zones, streams hyporheic of characteristics biogeochemical N model, a consequent the and activities rivers anthropogenic and streams N for on account processes riverine natural that the cli- and improve models at to emissions change needed occurring is quantify mate relationship processes best scaling upscale This to scale. to reach network single us scal- a a allows of within identification that the is relationship works, which ing previous factor, in key the elusive A among been zones. has scale hyporheic reach and benthic, the column, uncertainty at water reactions occurring This biogeochemical interactions of complex 12–14). dependence on the (6, from part underestimated in Change results likely Climate on are Panel Intergovernmental report recent most the in otiuinfo h ae oun(,1,1) easmdthat assumed We 18). 12, (4, the column of water increase the the from by compensated contribution partially only to contri- is streams hyporheic which the from bution, of reduction downstream systematic the moving of because reduce rivers area benthic– N unit because the per emerge, within limits sions two production These zone. by N column caused lower water the is and potential interface, emission benthic–hyporheic the within tion N two N upper between the bounded potentials: is worldwide network river uhrcnrbtos ...... n ...dsge eerh .. D.T., A.M., research; designed J.L.T. and A.B., D.T., M.M.D., A.M., contributions: Author owo orsodnesol eadesd mi:[email protected]. Email: addressed. be work. should this correspondence to whom To equally contributed J.L.T. and A.B., D.T., M.M.D., A.M., sn edl vial ec-cl igohmclmeasure- data. hydromorphological biogeochemical and reach-scale ments available conditions, climatic readily and using types, land-use biomes, among wide, river- N governing quantify factors anal- scaling N This primary in rivers. ine the in zones reveals column benthic also water N and ysis and of benthic hyporheic source the to primary the streams the from that and shifts size production stream and river on N that show We Significance 2 ee eietf n en hssaiglwb ikn,through linking, by law scaling this define and identify we Here, msinfo hs systems. these from emission O 2 rdcinprui fsra/ie ufc rafo the from area surface stream/river of unit per production O 2 msin.Fnly tpoie rdcieto to tool predictive a provides it Finally, emissions. 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ENVIRONMENTAL SCIENCES ammonium entering via , or other routes, is quickly The work of Ocampo et al. (15) suggested interpreting NO3 nitrified, such that in-stream processes (i.e., hyporheic zone, ben- transport and transformation within a using a thic, and ) are the primary source of N2O emissions, Damkohler¨ number, which is the ratio of a characteristic resi- whereas direct N2O contribution, which may enter the streams dence time, with importance (28) that has been documented by from groundwater or terrestrial origin, is negligible (6). several empirical (5, 16, 17) and numerical (29, 30) investiga- We unveiled this scaling and developed our model by analyz- tions, to the characteristic time of the pertinent biogeochemi- ing available N2O emission data and hydromorphological param- cal reaction. Recent investigations also proposed this approach eters of 12 headwater streams in the Kalamazoo River (Michi- to interpret hyporheic processes (31, 32), and they adapted it gan) watershed (19, 20) and 16 headwater streams associated to quantify the hyporheic biogeochemical response at both bed- with the second Lotic Intersite Nitrogen eXperiment (LINXII) form (33) and reach (34) scales. Here, we capitalized on these Study (6, 10, 11). These data allow us to parse the relative roles advances to depict the observed scaling effect on N2O emis- of the benthic and hyporheic zones in N2O emissions and con- sions across riverine networks (Fig. 1), and we parameterized strain them between two limits: upper- and lower-bound models. the transformation efficiency of dissolved NO3 to gaseous N2O We then validated the scaling law and the identified upper- and in terms of two Damkohler¨ numbers (Materials and Methods and lower-bound models with data that we collected during synoptic SI Text). In headwater streams that are typically small and shal- sampling campaigns along the Tippecanoe River (Indiana) and low, microbially mediated denitrification occurs mainly within Manistee River (Michigan) watersheds and data available in the the benthic–hyporheic zone (35). Headwater stream hydrody- literature collected in a midsized United Kingdom river (21, 22) namics at and within the streambed (hyporheic flows) is the main (Swale-Ouse River), six large river networks in Africa (23) (Athi– factor controlling the flux of dissolved nutrients to the microbial Galana–Sabaki, Betsiboka, Congo, Rianila, Tana, and Zambezi), assemblages that control biogeochemical transformations (Fig. and a large tidal river (24, 25) (Hudson River in New York) (6, 2). Therefore, the Damkohler¨ number for the benthic–hyporheic 10, 19–25) (descriptions of these streams are in Tables S1, S2, zone is defined as the ratio between the median hyporheic res- and S3). These streams are more than 400 testing reaches with idence time (τ50), which is an index of the time that stream contrasting land use land cover (LULC), biomes, climatic condi- water spends within the hyporheic sediment, and the charac- tions, morphology, and size (Table S4). teristic time of denitrification (τD ), τD = 1/kD , where kD is the denitrification reaction rate (evaluated as the ratio between the Results and Discussion denitrification uptake rate, vfden , and the mean flow depth, Y0: Analysis of average flux of N2O emissions per unit area, F N2O kD = vfden /Y0): DaDHZ = τ50/τD (zone 1 in Fig. 2) (36). How- (micrograms N per square meter per hour), from the study ever, as stream size increases, the ratio of hyporheic to sur- reaches of all of 417 analyzed streams and rivers to the atmo- face flow declines, which reduces the relative contribution of sphere shows that F N2O systematically decreases with system hyporheic zone to biogeochemical transformations (zone 2 in size (as width) along a gradient from headwater streams to rivers Fig. 2). In rivers, therefore, water column transformations com- (Fig. 1) of contrasting river networks (e.g., US streams and bined with benthic processes at the sediment–water interface African rivers) and within the same networks (e.g., Manistee dominate denitrification, overwhelming the benthic–hyporheic and Tippecanoe, with channel widths that span <1 to >50 m) contribution (zone 3 in Fig. 2). This behavior requires a differ- (Table S2). Using this analysis, streams and rivers can be clas- ent metric to describe the relevant timescale of N2O production. sified in three zones according to the gradient of reduction in We identify this metric with the time of turbulent vertical mix- emissions shown in Fig. 1. Zone 1, which includes small streams ing, tm , which is the average time for any neutrally buoyant par- with widths (W ) that are less than 10 m (4), shows a very steep ticle to sweep through the entire water column because of tur- reduction of emissions with stream size. Zone 2, which includes bulence. Thus, we introduce a unique Damkohler¨ number for streams with 10

Fig. 1. Nitrous oxide emissions from the analyzed streams and rivers. Average N2O emissions (FN2O) per unit area as a function of the mean system width (W) for the analyzed streams and rivers. Zone delineation is based on FN2O changes with stream/river size (fast change with size for zone 1, low change with size for zone 2, and no change with size for zone 3). This division is consistent with the classification proposed by the Forest Prac- tice Code (26), Buffington and Montgomery (27), and Peterson et al. (4). Error bars represents the SE (±SE) of the mean stream width and average flux of N2O.

2 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1617454114 Marzadri et al. Downloaded by guest on September 24, 2021 Downloaded by guest on September 24, 2021 azdie al. et Marzadri a eacutdfrwt nAreislk eainhpwhen relationship N Arrhenius-like temperature an the water with of quantifying for effect the accounted whereas be N scale, can of that reach scaling the expect biogeochemical at of We tion and use advective 3). the the because Fig. both scale, the in larger at applicable and line globally watershed are solid laws power dimensionless (red N two these lower bound) the from (lower provides production tial zone the benthic both whereas the in zones, only occurring benthic and processes Fig. hyporheic by in the caused N streams line upper headwater solid from the (black as law identify power following data 3): River the Kalamazoo and define Study and LINXII the combine we Thus, with scaling similar watershed a River shows Kalamazoo 20) the (19, in that zone provided benthic–hyporheic the relationships above the FDIN to Methods and predictability (Materials confers 36) (34, dimen- ogy proposed the and in biochemistry accounted conditions via are LULC climatic framework that , sionless effects and of and size, regardless 3) stream (Fig. scales morphology, log stream five type, data than experimental with more patterns, benthic scaling ranging the similar within have processes They governing zone. influence processes also law lines hydromorphological exchange Study power orange that hyporheic LINXII The and suggest experimental the red and 2). with by data Fig. regression shown by in 3 obtained 1 Fig. are in (zone contribu- reported streams zone relationships hyporheic headwater the in of symbols), tion importance orange emissions relative 3, total (Fig. the zones the stating hyporheic than and lower benthic headwater magnitude sym- both (6). of red from 3, order these sites (Fig. one Study groundwa- zone are from benthic LINXII bols) the Furthermore, the only contributions from at Text ). emissions negligible Measured column (SI deemed were water 34) systems with asso- (6, and associated former latter one ter the the indirect with and zones, denitrification the direct hyporheic with and ciated benthic the from xldn hs sdi hi eiain(IXISuy 16 N worldwide), Study, Therefore, 400 streams). (LINXII 12 than derivation River, their (more Kalamazoo in reaches and used streams, study those all excluding with erality (ANCOVA) covariance of from [analysis different 3 statistically Fig. not in is analysis line which orange line), the dashed green 3, F ∗ 0 N skon h aeaayi ple oN to applied analysis same The known. is 2 F O value 1 = .55 0 = τ .068 × 2 50 u from flux O 10 ikdt temhdalcadmorphol- and hydraulic stream to linked −7 FDIN < 2 msinptnil(pe bound) (upper potential emission O (Da F crit 0 DHZ , 4 = k D F ) 0.43 and , .259 ∗ N and Da 2 and .W ettergen- their test We O. and τ DHZ .Ti linkage This Text). SI 50 r 2 with , msinpoten- emission O 2 P 0 = for Da 0 = hc we which .48, DHZ F 2 k .796 u from flux O D 2 ∗ produc- O N ikdto linked 2 captures > (Fig. O 0.05]. 2 O n re ie)aentsgicnl ifrn,w te ohdtst with N datasets quantifies orange both [F fitted (dashed law we relationships power different, significantly two a not these are Because lines) green line. and green the by shown with scale [ line streams regress- dashed power orange their the and r symbols, as orange shown in is are ion HZ) + of zones, contribution both (combined zone benthic–hyporheic [F the these line from of solid Emissions regression 0.75]. red law the power with the shown symbols; is red data with shown is N streams Study of production the from ing n Damk tion i.3. Fig. watersheds the of streams headwater the of all for (FDIN valid load nitrogen law inorganic of of function flux prod- mass riverine the total as a and computed the within be can of 1 4A) uct and zone 3 in Figs. (compare streams network headwater from emissions 2 = = 6 n h aaao ie (Michigan; River Kalamazoo the and 16) 4.Eisosfo h eti–yohi oeo h Kalamazoo the of zone benthic–hyporheic the from Emissions 0.54]. F ∗ N iesols u fN of flux Dimensionless he ubr(Da number ohler ¨ 2 rvddb h pe-on oe a oe sa as model law power upper-bound the by provided O 2 msin rmheadwaters. from emissions O Da ∗ N DHZ 2 O Da = 1.55 DHZ bakln nFg ) efudti power this found We 3). Fig. in line (black yohi oag)znsa ore fN of sources and as (red), zones benthic (orange) hyporheic blue), importance (light relative column water the the of and indicates rivers and arrows streams of N Size of magnitude size. increas- stream of zones ing three within biogeochemical and transformations hydrodynamics of role tive 2. Fig. DHZ [F × 2 ∗ 10 ihnol h eti oeo h LINXII the of zone benthic the only within O nteLNI td (n Study LINXII the in ) N 2 −7 2 (F O O (Da = ocpulmdldsrbn h rela- the describing model Conceptual ∗ 9.83 ∗ N DHZ N 2 2 )a ucino h denitrifica- the of function a as O) F O ) × 0.43 ∗ 2 = N msin e ntae from area unit per emissions O n 10 2 , 1.91 = O r −8 2 NSEryEdition Early PNAS = 2 streams. 12) = (Da 2.15 × 8 lc ie,which line], black 0.48; = DHZ 10 × ubro streams, of number −8 ) 0.41 10 (Da −7 , F r DHZ ∗ (Da 2 N = 2 ) 0.57 result- O DHZ 4 as 0.54] | 2 O. , ) f6 of 3 0.46 r 2 0 = , )

ENVIRONMENTAL SCIENCES ∗ Fig. 4. Dimensionless flux of N2O(F N2O) as a function of the two Damkohler¨ numbers, reflecting processes occurring within the benthic–hyporheic zone and the water column. None of the streams (circles), shown colored by reach width with the width increasing from green to yellow, were used in deriving ∗ the upper (black lines) and lower bounds (red lines) in A, C, and E. A, C, and E consider the scaling of F N2O as a function of DaDHZ for zones 1–3, respectively. Black lines represent the scaling obtained in Fig. 3 by fitting the power law to the LINXII Study and Kalamazoo River data [n = number of streams, n = ∗ −7 0.43 28; F N2O = 1.55 × 10 (DaDHZ ) ]. Red lines represent the scaling obtained by fitting the power law to the LINXII Study data (n = 16) considering only ∗ −8 0.57 benthic emissions (red line in Fig. 3) [F N2O = 1.91 × 10 (DaDHZ ) ], and blue lines represent the fitting of the power law with all of the data shown. B, ∗ D, and F show the scaling of F N2O as a function of DaDS for zones 1–3 (n = 91, 66, and 247, respectively). The blue continuous lines represent the fitting of a power law with all of the data shown by circles in the graph.

analyzed in this study regardless of biomes, LULC, or climatic explicitly for hyporheic downwelling fluxes that control the conditions (in Fig. 4A, notice the higher r 2 of 0.59 when applied amount of reactants delivered to the sediment. These fluxes for all studied headwater streams without including those used depend on the same hydromorphological parameters that char- to derive the upper-bound power law relationship in Fig. 3). The acterize τ50, and thus, we implicitly, although partially, account regression of a power law to all of the available data (blue line for downwelling fluxes via τ50, because there is an inverse rela- in Fig. 4A) is also not statistically different (ANCOVA analy- tionship between τ50 and mean hyporheic downwelling flux. sis Fvalue = 0.0 < Fcrit = 3.89 and P = 1 > 0.05) from the upper- As stream/river size increases, the relative contribution of the bound power law (black lines in Figs. 3 and 4A) and maintains the hyporheic zone to N2O emissions in relation to the benthos and same r 2. Thus, we suggest that the upper-bound power law could water column declines; consequently, our conceptual model pre- F ∗ be widely applicable to streams across the globe because of the dicts a decline in dimensionless emissions, N2O (compare breath of our data. Some unexplained variance is likely caused Fig. 4 A, C, and E). Notice that colors of the symbols in Fig. 4 by N O originating from groundwater and terrestrial sources vary from green to yellow as the width of the system increases 2 from streams to rivers. The coefficient of determination of the or nitrification/denitrification of groundwater NH4. Our model upper-bound power law model, which includes both benthic and assumed that the main source of N O resulted from transforma- 2 hyporheic zones (in Fig. 4, the black lines are the same as in Fig. tions of dissolved inorganic nitrogen (NO3 plus NH4) present 3), declines moving from headwater streams (Fig. 4A, r 2 = 0.59) in the stream without distinguishing the source of dissolved 2 inorganic nitrogen (e.g., groundwater, runoff, or atmospheric to intermediate systems (Fig. 4C, r = 0.28) and rivers (Fig. 4E, 2 deposition). As such, we may partially account for NH4 of r = 0). This decrease suggests a shift in processes controlling 2 groundwater origin if nitrification occurs within the stream via N2O production. When the data are fitted, r rises again, but transformation in the water column, benthic, or hyporheic zone. the resulting regression curves, shown in blue in Fig. 4 C and Another potential source of error is that we do not account E, increasingly deviate from the power law model of zone 1

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on impact may ate streams the headwater of Thus, contribution contribution column dominates. the benthic–water and rivers, declines, to zone hyporheic transition streams as contrast, oeuei xoe otedntiyn niomn stemedian the is environment denitrifying the (τ to time residence exposed hyporheic is molecule process. biogeochemical the this to control according mainly network that riverine environments the riverine along changes zones denitrifying the of lation reac- biogeochemical rate reaction the denitrification, denitrification of of time time the characteristic is the the tion For model, reaction. this biogeochemical the of of purpose water time and characteristic hyporheic, the (benthic, and zones column) denitrifying the within time residence Damk a N of flux dimensionless The Methods and Materials scale. global the human at quantify change help climate to on management impact water and among water LULC, feedback climate, needed and the use provides it land Consequently, biogeochemical outcomes. influences in climate changing changes how or watershed-scale management used as be such with can ments, value framework N dimensionless the quantify the Thus, to scaling equation. by Arrhenius-type accounted an also N be on effects can temperature Water land quality. climate water and fore, of regime, because transport and change sediment use, may extraction, which water (46), change, and through ogy activ- forcing human natural of and impact This ity the zone, zone). quantifies riparian hyporheic actively the framework also (e.g., and scaling reach column, water the stream/river the of zone, the benthic role of the linking parts and different constraining considering and by morphology models N conceptual stream controlling of in improvement predict morphology to to contribute river of (12) role Storage the Subsurface and N reach-scale hyporheic Exchange network-scale with works in quantify them and models, include define to headwater research relationships, for small need these in a is common there Consequently, plane- are (27). and streams which step-pool, (34), cascade, morphologies for available bed mod- currently These not are information. hyporheic els space hydromorphological robust in to requires both linked which approach This models network, ammonium, (45). river time and the read- through and throughout nitrate and distributed quantify (44) of be to morphology can measurements one stream available allow of ily analyses laws system scaling mation Our Text). chan- N (SI and slope, width) velocity, depth, nel flow mean morphology, stream and temperature reach- stream NO accessible (i.e., through measurements conditions geochemical scale climatic and (Q types, streams LULC headwater from m N scales quantify across to environments worldwide applied ocn loicue UC im,adciai odtos hrfr,the Therefore, conditions. climatic This sedi- and shape. biome, and and Damk LULC, type discharge bed-form includes affect both also change on forcing 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ENVIRONMENTAL SCIENCES tm between the characteristic time controlling hyporheic residence time and Da = , [2] DS τ the characteristic time controlling the denitrification process: D τ50 where the median residence time in the hyporheic zone, τ50, is replaced by DaDHZ = . [1] τD tm, stating a shift from hyporheic- to water column-dominated N2O pro- duction. When DaDS < 1 (tm < τD), the timescale for the vertical mixing is Values of DaDHZ < 1 suggest that the system is limited by the denitrification less than that of denitrification; therefore, the production of N2O is chiefly rate (i.e., low kD) or short residence time (small τ50). Conversely, DaDHZ > 1 controlled by microbial activity. In contrast, when Da > 1 (t > τ ), the suggests high denitrification efficiency (high kD) or long residence time DS m D production of N O is controlled by hydrodynamics, which determines solute (large τ50) (zone 1 in Fig. 2). 2 As stream size increases, the ratio of hyporheic to surface flow declines mixing throughout the water column, thereby influencing the contact time in favor of a gradual contribution of the benthic–water column in control- with microbial denitrifiers carried by suspended particles. ling denitrification (zone 2 in Fig. 2). Rivers are turbulent systems in which All data reported in the paper are reported in SI Text. dissolved solutes and particles are vertically mixed throughout the water col- umn (47), thus requiring a different metric to describe the relevant timescale ACKNOWLEDGMENTS. This research is supported by National Science Foun- of N2O production. We identify this metric with the time of turbulent verti- dation Awards 1344661 and 1344602 and by the European Communities 7th cal mixing, tm, which is the average time for any neutrally buoyant particle Framework Programme under Grant Agreement 603629-ENV-2013-6.2.1- to sweep through the entire water column because of turbulence (details on Globaqua. Any opinions, conclusions, or recommendations expressed in this the calculation of tm are in SI Text). Thus, we introduce a unique Damkohler¨ material are those of the authors and do not necessarily reflect the views of number for rivers as follows: the supporting agencies.

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