Factors controlling hyporheic respiration in a desertstream
J.B. J O N E S , jRDepartment of Zoology, Arizona State University, Tempe, AZ 85287, U.S.A.
Present address and address for correspondence: Environmental Sciences Division, Oak Ridge National Laboratory, PO Box2008, Bldg. 1000, Oak Ridge, TN 37831-6335, U.S.A.
SUMMARY
1. Experimental manipulations were performed to detemiine the biological, chemicaland physical attributes that govern sediment respiration in the hyporheic zone ofSycamore Creek, a Sonoran Desert stream.2. Hyporheic respiration per unit volume of sediment was inversely related to diameterof sediment particles, indicating that respiration is affected by availability of substratefor microbial colonization (i.e. sediment surfaces). Respiration rate per unit surface areaon sediments was positively correlated with particle diameter, indicating greatermetabolic activity of microbes on larger sediments.3. Hyporheic respiration was more than twice as high in water collected from thesurface flow than from subsurface flow. Further, hyporheic respiration was highestimmediately foUowing exposure of sediments to surface water and declined over time,presumably due to exhaustion of labile orgaruc matter.4. Microbial activity was stimulated by addition of algal leachate; however, amendmentsof leaf leachate had little effect. Respiration was also elevated with dextrose and leucineamendments, but not with inorganic nitrogen additions, indicating hyporheic respirationis carbon limited.5. Water from the stream surface is probably enriched in labile organic matter derivedfrom algae and stimulates respiration at points of hydrologie downwelling wheresurface water enters hyporheic sediments. The physical structure of sediments furtheraffects metabolism by affecting the area available for microbial attachment.
Introduction
Ecosystem respiration is a basic measure of organicmatter decomposition and energy flow. The overallrate of ecosystem respiration results from complexinteractions between sources of organic matter servingas respiratory substrates and environmental factorslimiting metabolism. Variables influencing respirationin streams include organic matter availability, nutrientsupply, sediment size, temperature and oxygen.Organic matter is variable in its composition andsusceptibility to decomposition (Kaplan & Bott, 1985;Meyer, Edwards & Risley, 1987). Labile forms, suchas monosaccharides and disaccharides are rapidly
degraded, resulting in most of the organic matter poolbeing recalcitrant (Leff & Meyer, 1991). Decompositionis also dependent on nutrient availability (Hynes &Kaushik, 1969; Triska, Sedell & Buckley, 1975); micro-organisms may assimilate required nutrients directlyfrom organic substrates or from the water. Sedimentsize determines surface area available for microbialgrowth and biofilm development (Hargrave, 1972;Peters, Webster & Benfield, 1987), and may also influ-ence interstitial flow rate and thus transport of meta-bolic substrates to organisms.
In Sycamore Creek, a Sonoran Desert stream, nearly
91
92 }.B. Jones
half of total ecosystem respiration occurs in thehyporheic zone (Grimm & Fisher, 1984) and is probablysupported by orgaruc matter derived from benthicalgal production Of>ii6s, Fisher & Grimm, 1995a).Hyporheic respiration is particularly high in areas ofhydrological downwelling where surface water entershyporheic sediments, and decreases downstreamalong subsurface flowpaths (Jones et al., 1995a). Fur-ther, rutrogen limits primary production in SycamoreCreek (Grimm & Fisher, 1986) and may also influencehyporheic respiration.
This research addressed the question of whichfactors might influence respiration rate in thehyporheic zone. A range of biological, chemical andphysical attributes was tested using experimentalmanipulations. Specifically, the relative rates of bioticand abiotic uptake of oxygen, the relative importanceof free-living microbes in interstitial water as opposedto attached microbes in sediments, and the effectsof sediment particle size on respiration rate weredetermined. The water from three subsystems wasalso tested for variability in content of biologicallyavailable organic matter, and determined how rapidlythe amount of readily assimilable organic matter inwater from one subsystem (the stream surface)declined following exposure to hyporheic sediments.The ability of hyporheic microbes to use organic matterfrom two sources, algae and leaves, was tested anddetermined whether respiration was limited by carbonor nitrogen availability.
Study site
Hyporheic respiration was studied using sedimentsand stream water collected from runs of SycamoreGreek, a Sonoran Desert stream located 34 km north-east of Phoenix, Arizona, USA. Stream flow in Syca-more Creek is lowest in summer (0.01-0.05 m^ 1) andhighest in winter (0.1-2.5 m^ 1). Wetted channel widthof runs averages 5-6 m and mean stream depth is5 cm. The wetted channel is bounded by an activechannel of alluvium that is over 20 m wide (Fisheret al., 1982) which in tum is bordered by a cottonwood-willow riparian zone. Riparian vegetation is set backfrom the wetted stream; consequently the streamreceives full sunlight most of the day, has algal biomassas great as 350 mg chl a m" , and in-stream gross prim-ary production as high as 12 g O2 m"^ day~^ (Gdmm,1987). Substrata in runs consist primarily of sand and
fine gravel with a mean depth to bedrock of 62 cm(Valett, Fisher & Stanley, 1990) and a mean annualrespiration rate of 0.80 mg O21 sediments"' h"^ (Jonesetal, 1995a). Interstitial dissolved organic carbon(IXXT) concentration averages 3.7 mg G 1"' (annualmean; Jones, Fisher & Grimm, in press) and particulateorgaruc carbon (POG) storage ranges from 12 to155 mg CI sediments"^ Qones et al, 1995a). Through-out the year at a depth of 25 cm in the hyporheic zoneof runs, water temperatiu-e is 14-26 °G and dissolvedoxygen 1.3-8.0 mgO2H Qones etal, 1995a). Modalparticle sizes of hyporheic sediments are 1-4.75 mmin diameter and subsurface current velocities throughthe hyporheic zone vary from 0.035 to 1.25 mm s"(Valett et al, 1990).
Methods
The factors governing hyporheic respiration weretested by experimental manipulations using respira-tion chambers incubated in the laboratory. All experi-ments were conducted during summer (1993 and 1994)when metabolic activity associated with hyporheicsediments is high (Jones et al, 1995a). Hyporheic sedi-ments were randomly coUected by trowel from non-weUing zones (no hydrological exchange betweensurface and hyporheic flow) from a depth of 2-17 cmbelow the substrate surface (benthic sediments werescraped away before collecting sediments) and trans-ported to the laboratory at ambient temperature.Sediments stored in the laboratory at 10 °C were usedwithin 4 days of collection. Respiration chambers wereconstructed of clear plastic pipe (32 cm long, 4.4-cminside-diameter) sealed at the ends with rubber stop-pers and plumbed to peristaltic pumps that recircu-Iated water (mean flow rate through sediments inchambers = 0.6 mm s" ; Fig. 1). Chambers were filledwith a 15-cm columr\ of sediment (425 g wet mass)and about 300 ml of unfiltered stream water (unlessotherwise stated, incubation water was from surfaceflow). Initially, chambers were plumbed in-line to areservoir to allow for initial oxygen determination.Water circulated from the reservoir through chambersand then back to the reservoir for 1 h (to allow formixing of water that was initially associated withsediments and newly added incubation water) beforean incubation was initiated (Fig. la). Immediatelybefore starting an incubation, dissolved oxygen con-centration was determined for reservoir water using
Fig. 1 Redrculating respirationchambers used for experimentalmanipulations of hyporheicmetabolism.
a Leeds and Northrup Model 7932 dissolved oxygenmeter. The direction of flow through the chamberswas then immediately changed so that water circulateddirectly from the top of a core through the pump andback to the bottom of the core (Fig. lb), Sedimentswere incubated in the dark for 4 h, after which oxygenconcentration in chambers was determined by openingthe tops of chambers and measuring with an oxygenmeter. Following incubations, the volumes of sedi-ments and water in chambers were determined. Res-piration rate was calculated as uptake of oxygen pervolume of sediment per time.
Biotic activity associated with surfaces of hyporheicsediments was studied by testing the rate of abioticvs. biotic oxygen uptake and respiration rate of free-living organisms in stream water vs. biota attachedto sediments. The effects of particle diameter andsediment surface-area on respiration was also exam-ined, with the assumption that surface area of sedimentand therefore space available for microbial coloniza-tion is inversely related to particle diameter. Abiotic vs.biotic uptake of oxygen was determined by incubatingsediments with and without mercuric chloride(100 mg HgCl21"^; n = 8 poisoned, n = 8 control cham-bers). Total hyporheic respiration was partitioned intothat by organisms associated with sediments andorganisms free-living in stream water using chamberscontaining sediments plus stream water and chamberswith stream water only (M = 8 sediments + water,tt = 8 water only). The respiration rate of free-livingorganisms, initially measured as |XgO2 I HjO"' h""', wascalculated with respect to sediment volume as theproduct of respiration rate per volume of water andsediment porosity (porosity determined as volume ofinterstitial water in a known volume of sediments).
Respiration rate of sediment-associated microbes wascalculated as the difference between respiration ratesin chambers containing sediments plus water andchambers containing only water. The effect of sedimentparticle size on metabolism was tested by incubatingsediments of three different size classes (sedimentswet sieved, size classes ^ 0.053-1, 1-2, 2-4.75 mm,tt = 12 chambere per size class). Respiration rate wasexpressed with respect to both volume of sedimentsand surface area of particles. Particle surface area fora size class was estimated as the product of numberof particles occupying a given volume (assumingparticles are spheres) and sphere-surface area (thediameter of all particles within a size class wasassumed to be the mean for that class, i.e. 0.53, 1.5,3.38 mm).
Two experiments were conducted to examine spatialvariability of labile organic matter in water fromdifferent subsystems and how rapidly labile organicmatter in water from one subsystem, the stream sur-face, is respired when exposed to sediments (analogousto surface water downwelling into the hyporheiczone). In the first experiment, differences in labileorganic-matter content of water from different subsys-tems were assessed with chambers filled with watercollected from the surface, hyporheic and parafluvial(the part of the active channel without surface water;Holmes, Fisher & Grimm, 1994) zones. Hyporheic andparafluvial water was collected from mini-piezometersinserted to a depth of 25 cm. Piezometers were 9-mm(internal diameter) polyethylene tubes with perfora-tions near the tip of the tube covered with 300-)imNitex® mesh. Ten piezometers were randomly locatedin the hyporheic and parafluvial zones (five piezo-meters per subsystem) and 41 of water drawn from
94 J.B. Jones
each to collect 20 1 of hyporheic and 20 I of parafluvialwater. In the second experiment, it was determinedwhether the amount of labile organic matter in surface-stream water declined following exposure tohyporheic sediments by repeatedly incubating thesame sediments and stream water {n ^ 24 incubationstotal, eight chambers X three consecutive incubations);in other words, for a given chamber, the stream waterand sediments used in incubations were not changed.The total exposure time of stream water to sedimentswas 47 h and each of the three incubation periodslasted 4 h. In between incubation periods the directingof flow through chambers was altered so that chamberswere plumbed in-line to the reservoir; the directing offlow was changed between incubations to maintainoxic conditions within chambers.
Finally, three experiments testing (i) the ability ofhyporheic organisms to use specific sources of organicmatter, and (ii) organic carbon and (iii) nitrogen limita-tion of respiration were conducted using enrichmentassays. The ability of hyporheic microbes to use differ-ent sources of orgaruc matter was determined byamending stream water with leachates from algae{Cladophora glomerata) and cotton wood {Populusfremon-tii) leaves. Leachates were produced by maceratingleaves and algae in a blender, or a mortar and pestle,respectively, followed by filtration (Whatman GF/Fglass fibre filters). EXXT concentration of leachatewas measured by high-tennperature oxidation on aShimadzu Model 5000 Total Organic Carbon Analyzerand an appropriate volume was added to incubationwater to produce a concentration of 5 mg C 1"* ofleachate-amended water in chambers (n = 20 control,20 leaf, 20 algal). Carbon and nitrogen limitation wereassessed with amendments of labile organic carbon,using dextrose and leucine (5 mg C H amended; n =12 control, 14 dextrose, 14 leucine chambers), and
inorganic rutrogen, using ammonium (NH4CI) andnitrate (NaNO3; 5 mg N T amended; n = 20 control,19 ammonium, 20 nitrate chambers), respectively.
Differences in oxygen-uptake rate between poisonedand control treatments, and between chambers withsediments plus stream water and stream water onlywere assessed with f-tests (SYSTAT inc.; Wilkinson,1990). Effects of sediment size and surface-water expo-sure-time to hyporheic sediments on respiration rateswere analysed by linear regression. Data from thesediment-size experiment were log-log transformedto achieve linearity (Hargrave, 1972). The effect of
assuming the diameter of all particles within a sizeclass (sediment-size experiment) was the mean forthat class was examined by varying assumed particlesize and reanalysing with linear regression. Particleswere assumed to be the minimum, mean and max-imum diameters of size-class intervals (e.g. for the0.053-1 mm size class, 0.053, 0.53, 1 mm) and allcomparisons between size classes were assessed(except cases in which particle diameter for two sizeclasses were equal; twenty-one comparisons in total).The influence of subsystem origin of stream water,leaf and algal leachate amendments, and carbon andrutrogen amendments were tested with one-wayANOVA (WUkinson, 1990).
Results
Nearly all change (86%) of dissolved oxygen concen-tration in incubation chambers was biotic. Oxygenuptake in chambers poisoned with mercuric chloridewas only 42 ig O2 1 sediments"^ h"^ compared with306 p,g O21 sediments"^ h" in controls (i.e. chamberswithout mercuric chloride; P < 0.001). Nearly allrespiration was from biota associated with sedi-ments. Respiration in chambers without hyporheicsediments was 90 \ig O21 H20^^ h"^ equivalent to27 ig O21 sediments'^ h~ (voltune H2O per volumesediments = 0.30), which was only 9% of total metabol-ism. Further, respiration rate was inversely related todiameter of sediment particles. Respiration rate perunit volume of sediments increased nearly 1.5 timeswith an 84% reduction in particle diameter (logY = 2.7-0.23 X logX, r = 0.22, P < 0.01; Fig. 2a). In contrast,however, respiration expressed in terms of sedimentsurface-area was more than 4-fold greater on sedi-ments with a mean particle-diameter of 3.4 mm com-pared with 0.5 mm (logY = 2.2 + 0.77 X logX, r =0.76, P < 0.001; Fig. 2b). Assuming all particles withina size class were the mean diameter in size had littleeffect on the relationship between respiration persediment surface area and particle diameter. In twentyout of twenty-one comparisons in which assumedparticle diameter was varied, the relationship betweenarea specific respiration rate and particle size wassignificantly greater than zero (P < 0.05; range ofslopes = 0.65-0.91).
The amount of biologically available organic matterin stream water was variable between subsystems ofSycamore Creek. Respiration of sediments incubated
Fig. 2 Relationship between hyporheic respiration per unitvolume of sediments (a) and surface area on sediments (b) andsediment-particle diameter.
with surface water was more than twice as high assediments incubated with hyporheic or parafluvialwater (Fig. 3; P < 0.001). Furthermore, hyporheic res-piration was greatest immediately following exposureof sediments to surface water and declined withresidence time (Fig. 4). Respiration rate decreased 56%from 303 g O2 I sediments"' h~' at the time of initialexposure of surface water to hyporheic sediments, to131 |ig O21 sediments"' h"' after 43 h of contact (Y =303--4.0 xX,r^ = 0.39; P < 0.01).
Micro-organisms from the hyporheic zone of Syca-more Creek readily use algae-derived organic matter.Respiration increased 160% from a background rateof 523 [J-g O2 1 sediments"' h"' in non-amended streamwater to 835 ^g O2 1 sediments"' h"' when algal-leach-ate water was added (P < 0.05; Fig. 5a). In contrast,respiration rate was not significantly elevated withamendment of leaf leachate (P. 0.05). Further,hyporheic respiration rate increased more than 2-fold with monosaccharide (dextrose) and amino acid(leucine) amendments (P < 0,001; Fig. 5c), but was not
Surface Hyporheic ParattuviaiSubsystem origin of water
Fig. 3 Respiration rate (mean ± SE) of hyporheic sedimentsincubated with stream water from three subsystems. Barshaving the same letter designation have meansindistinguishable by Tukey's multiple comparison (a= 0.05).
500 n
400 -
300 -
200 -
100 -
P<0.01
"Tr-ie
—I—
24 420 6 12 18 24 30 36Water residence time in sediments (h)
Fig. 4 Relationship between respiration and residence time ofsurface stream water in hypoiheic sediments.
affected by addition of inorganic nitrogen (P =0.05; Fig. 5b).
Discussion
Biofilms and sediment surfaces
The large amount of hyporheic respiration associatedwith sediments (91%) in Sycamore Creek is typical of
96 J.B. Jones
100 -
Control Leucine
Fig. 5 Respiration rate (mean ± SE) of hyporheic sedimentswith amendments of (a) leaf and algal leachate, (b) nitrogenand (c) carbon. Bars having the same letter designation havemeans indistinguishable by Tukey's multiple comparison (a=0.05).
stream metabolism and results from microbial biofilmson particle surfaces (Lock et al, 1984; Jones & Lock,1989). Respiration rate was not only dramaticallydifferent in chambers with and without sediments,but also responded to particle size (Fig. 2). For a givenvolume of hyporheic sediments, small sediments havemore surface area available for microbial attachmentand biofilm formation than large particles, and con-sequently have greater microbial activity. Hargrave(1972) speculated that there is a simple and basicrelationship between sediment respiration-rate andparticle surface-area (with a slope coefficient of -1)and that other environmental attributes modify theinteraction between the two (i.e. change the y-inter-cept). For organic particles, however, the relationship
between respiration and particle size is more variableas detritus tends to be less spherical and also serve asrespiratory substrates (Tank, Webster & Benfield, 1993).
In the hyporheic zone of Sycamore Creek therelationship between respiration and surface areaavailable for colonization is not as simple as speculatedby Hargrave (1972). If respiration is solely a functionof particle surface area then respiration should beconstant on an areal basis. One explanation for higherrespiration per unit particle surface area on largersediments is that larger substrata may allow for higherflux rate of metabolic substrates. If microbial densitiesare equal on particles of varying sizes the presentresults suggest that microbes on larger particles havea higher respiration rate. Large sediments have largerinterstitial spaces (assuming size of sediments is uni-form), resulting in more uniform subsurface flow ofwater and flux of dissolved or small-particulateorgaruc substrates to biofilms which may stimulatemetabolism. Alternatively, particle size affects epilithiccommuruty composition and development, which intum may influence metabolism (King & Cummins,1989; Ward etal, 1990; Fiebig & Marxsen, 1992). Ifthe biofilm community is better developed on largersubstrata, a greater density of micro-organisms mayresult in a higher respiration rate per unit surface area.In either case, respiration per area of stream bedincreases with small particles and the metabolic rateper unit surface area of substrate declines.
Biological availability of organic matter in surface andsubsurface water
Jones et al. (1995a) hypothesized that organic matterderived from benthic algal production supportshyporheic respiration (algae-derived organic-matterhypothesis). In support, hyporheic respiration in Syca-more Creek was correlated with chlorophyll a (Joneset ai, 1995a). The present results further support thishypothesis. Sediment respiration was greatest whenincubated with water from the stream surface, whichis presumably enriched in organic matter derived frombenthic algal production. Extrapolating further, labileorganic matter would be depleted and respiration ratewould drop to zero within 80 h of when surfacewater downwells into hyporheic sediments (assumingrespiration rate vs. water residence time is linear andoxygen is not limiting) and 175 m downstream alongsubsurface flowpaths (assuming mean a subsurface
flow rate of 2.2 m h"'; Valett el al, 1990). Incorporatingeffects of oxygen consumption (assuming an initialoxygen concentration of 8 mg O2 I"'), aerobic respira-tion should be oxygen limited within 9 h and only20 m downstream along a subsurface flowpath.
Similar relationships between origins of streamwater and metabolism have been observed elsewhere.Bott, Kaplan & Kuserk (1984), working in a piedmontstream in Permsylvania, demonstrated that surfacewater supported a greater benthic respiration rate thangroundwater, presumably due to differences in DOMavailability. Leff & Meyer (1991) reported biologicalavailability of DOM in stream water of the OgeecheeRiver in Georgia declined downstream along the rivercontinuum. In Sycamore Creek, in situ respirationconforms to the expectation derived from the laborat-ory experiments reported here. Hyporheic respirationrate declined more than 50% as water flowed throughh5^orheic sediments from downwelling to upwellingzones Oones et al., 1995a).
Sources of organic matter and nutrient limitation
Previous studies have reported an increase of microbialactivity with amendments of leaf (Cummins et al,1972; Lock & Hynes, 1976; Kaplan & Bott, 1983; Dahm,1984; McDowell, 1985; Findlay, Smith & Meyer, 1986)and algal leachates (Kuserk, Kaplan & Bott, 1984; Bott& Kaplan, 1985; Miller, 1987); however, the influenceof organic matter from different leaves and algalspecies is variable. For example, Findlay et al. (1986)reported that micro-organisms mineralize alligator-weed detritus 2.5 times faster than detritus from oakleaves. Previous exposure of bacteria to organic matteralso affects decomposition (Kaplan & Bott, 1985;McArthur, Marzolf & Urban, 1985; McArthur & Mar-zolf, 1986). Although organisms can degrade organicmatter foreign to them through enzymatic induction,growth is elevated on native substrates for whichmicrobes are enzymatically prepared (Kaplan & Bott,1985; Leff, Burch & McArthur, 1991). Elevated respira-tion in response to amendments of algal leachate isconsistent with the hypothesis that hyporheic micro-organisms in Sycamore Creek have previously beenexposed to algae-derived organic matter.
Nutrient content of organic matter also affectsdecomposition (Bengtsson, 1982). For carbon-rich sub-strates such as cellulose, mineralization is typicallynitrogen limited (Benner et al, 1988). Organic matter
in the hyporheic zone of Sycamore Creek is, however,rich in nitrogen with an atomic ratio of carbon tonitrogen of 7.3-9.3 (Grimm, 1992), a ratio generallythought to indicate carbon limitation (Triska ctal,1975). In addition, nitrification is prevalent in thehyporheic zone of Sycamore Creek (Holmes et al,1994; Jones, Fisher & Grimm, 1995b), presumablysupported by mineralization of excess organic nitrogenduring decomposition and indicating that nitrogen isnot limiting to respiration. Another nutrient poten-tially limiting decomposition is phosphorus. Whilephosphorus was not specifically tested in this studyit was probably not limiting to decomposition.Hyporheic water in Sycamore Creek is enriched insoluble reactive phosphorus relative to surface water(Jones et al, 1995a) presumably due to decomposition.
Hedin (1990) suggested that in woodland streams,where particulate organic matter (POM) storage is highand predominantly allochthonous in origin, ecosystemrespiration is largely associated with sediment POM.He further contended that where algae and macro-phytes dominate organic matter inputs in aquaticecosystems, respiration is probably more closelyrelated to autochthonous production than POM stor-age. This study supports Hedin's contention.Hyporheic respiration in Sycamore Creek appearedlimited by availability of labile organic carbon. Waterfrom the surface flow is probably enriched in labileorganic matter derived from algae and stimulatesrespiration at points where surface water downwellsinto hyporheic sediments. The physical structure ofhyporheic sediments further affects metabolism bydetermining the area available for microbial coloniza-tion, and influences interstitial flow rate and flux ofmetabolic substrates.
Desert streams may represent one extreme of acontinuum of ecosystem dependence on autochthon-ous and allochthonous inputs of detritus to supportrespiration. Respiration in desert streams is clearlylinked to algal production of organic matter andprovides valuable insight for ecosystems in whichmetabolism is supported by a mix of detrital sources.Moreover, factors controlling respiration affect a rangeof hyporheic zone and surface-stream ecosystem pro-cesses. Nitrification in the hyporheic zone of SycamoreCreek is coupled to organic matter mineralization(Jones et al, 1995b). Thus, factors governing respirationalso affect ammonium supply to nitrifying bacteria.Microbial metabolism of DOM captures energy that is
98 J.B. Jones
used by higher trophic levels (Barlocher & Murdoch,1989); hyporheic meiofaunal and macroinvertebratesecondary production may thus depend on microbialdecomposition and assimilation of organic matter.
Acknowledgments
Special thanks to M. Mallett for help in the laboratoryand field and to S.G. Fisher and N.B. Grimm forcomments on the project and manuscript. Thanks toDrs C. Dahm, J. Elser, W. Minckley, C. Townsend andan anonymous referee for constructive comments onthe manuscript. In addition I thank Mr John Whitneyfor access to Sycamore Greek through Dos S Ranch.This research was supported by National ScienceFoundation's Ecosystem Studies Program (grants DEB-9224059 to J.BJ. and S.G. Fisher, and BSR-8818612,DEB-9108362, and DEB-9306909 to S.G. Fisher andN.B. Grimm).
References
Barlocher F. & Murdoch J.H. (1989) Hyporheic biofiims -a potential food source for interstitial animals.
Hydrobiologia, 184, 61-67.Bengtsson G. (1982) Patterns of amino add utilization by
aquatic hyphomycetes. Oecologia, 55, 355-363.Benner R., Lay J., K'ness E. & Hodson R.E. (1988) Carbon
conversion efficiency for bacterial growth onlignocellulose: implications for detritus-based foodwebs. Limnology and Oceanography, 33, 1514-1526.
Bott T.L. & Kaplan L.A. (1985) Bacterial biomass,metabolic state, and activity in stream sediments:relation to environmental variables and mulfiple assaycomparisons. Applied and Environmental Microbiology,50, 508-522.
Bott T.L., Kaplan L.A. & Kuserk FT (1984) Benthicbacterial biomass supported by streamwater dissolvedorganic matter. Microbiai Ecology, 10, 335-344.
Grimm N.B. (1987) Nitrogen dynamics during successionin a desert steam. Ecology, 68, 1157-1170.
Grimm N.B. (1992) Biogeochemistry of nitrogen inSonoran Desert streams. Journal of the Arizona-NevadaAcademy of Science, 26, 139-155.
Grimm N.B. & Fisher S.G. (1984) Exchange betweeninterstifial and surface water: implications for streammetabolism and nutrient cycling. Hydrobiologia, 111,219-228.
Grimm N.B. & Fisher S.G. (1986) Nitrogen limitation ina Sonoran Desert stream. Journal of the North AmericanBenthological Society, 5, 2-15.
Hargrave B.T. (1972) Aerobic decomposition of sedimentand detritus as a function of particle surface areaand organic content. Limnology and Oceanography, 17,583-596.
Holmes R.M., Fisher S G. & Grimm N.B. (1994) Parafluvialnitrogen dynamics in a desert stream ecosystem. Journalof the North American Benthological Society, 13, 468-478.
Hynes H.B.N. & Kaushik N.K. (1969) The relationshipbetween dissolved nutrient salts and proteinproduction in submerged autumnal leaves.Verhandlungen der Intemationalen Vereinigung fiirTheoretische Und Angewandte Limnologie, 17, 95-103.
Jones J.B., Jr., Fisher S.G. & Grimm N.B. (1995a) Verricalhydrologie exchange and ecosystem metabolism in aSonoran Desert stream. Ecology, 76, 942-952.
Jones JB. Jr., Fisher S.G. & Grimm N.G. (1995b)Nitrification in the byporheic zone in a Sonoran Desertstream ecosystem. Journal of the North AmericanBenthological Society, 14, 249-258.
Jones J.B., Jr., Fisher S.G. & Grimm N.B. (in press)Biogeochemistry of dissolved organic carbon inSycamore Creek, Arizona. Hydrobiologia.
Jones S.E. & Lock M.A. (1989) Hydrolytic extracellularenzyme activity in heterotrophic biofilms from twocontrasting streams. Freshwater Biology, 22, 289-296.
Kaplan L.A. & Bott TL. (1983) Microbial heterotrophicutilization of dissolved organic matter in a piedmontstream. Freshwater Biology, 13, 363-377.
Kaplan L.A. & Bott T.L. (1985) Acclimation of stream-bed heterotrophic microflora; metabolic responses to
King D,K. & Cummins K.W. (1989) Estimates of detritaland epilithon community metabolism from particle-sized riffle sediments of a woodland stream. Journal ofFreshwater Ecology, 5, 231-245.
Kuserk FT, Kaplan L.A. & Bott T.L. (1984) In situ measureof dissolved organic carbon flux in a rural stream.Canadian Journal of Fisheries and Aquatic Sciences, 41 ,
use of dissolved organic carbon from Carolina Bays.American Midland Naturalist, 126, 308-316.
Leff L.G. & Meyer J.L. (1991) Biological availability ofdissolved organic carbon along the Ogeechee River.Limnology and Oceanography, 36, 315-323.
Lock M.A. & Hynes H.B.N. (1976) The fate of 'dissolved'organic carbon derived from autumn-shed mapleleaves (Acer saccharum) in a temperate hard-waterstream. Limnology and Oceanography, 21, 436-443.
McArthur J.V. & Marzolf G.R. (1986) InteracHons of thebacterial assemblages of a Prairie stream with dissolvedorganic carbon from riparian vegetation. Hydrobiologia,134, 193-199.
McArthur J.V., Marzolf G.R. & Urban J.E. (1985) Responseof bacteria isolated from a pristine Prairie stream toconcentration and source of soluble organic carbon.Applied and Environmental Microbiology, 49, 238-241.
McDowell W.H. (1985) Kinetics and mechanisms ofdissolved organic carbon retention in a headwaterstream. Biogeochemistry, 1, 329-352.
Factors controlling hyporheic respiration 99
Meyer J.L., Edwards R.T & Risley R. (1987) Bacterialgrowth on dissolved organic carbon from a blackwaterriver. Microhial Ecology, 13, 13-29.
Miller J.C. (1987) Evidence for the use of non-detritaldissolved organic matter by microheterotrophs on plantdetritus in a woodland stream. Freshwater Biology, 18,
Peters GT., Webster J.R. & Benfield E.F. (1987) Microbialactivity associated with seston in headwater streams:effects of nitrogen, phosphorus and temperature.Freshwater Biology, 18, 405-413.
Tank J.L., Webster J.R. & Benfield E.F. (1993) Microbialrespiration on decaying leaves and sticks in a southernAppalachian stream. Journal of the North AmericanBenthological Society, 12, 394-^05.
Triska F.J., Sedell J.R. & Buckley B. (1975) The processingof conifer and hardwood leaves in two coniferousforest streams: U. biochemical and nutrient changes.Verhandlungen der Internationalen Vereinigung furTheoretische und Angewandte Limnologie, 19, 1628-1639.
Valett H.M., Fisher S.G. & Stanley H.H. (1990) Physicaland chemical characteristics of the hyporheic zone ofa Sonoran Desert stream. Journal of the North AmericanBenthological Society, 9, 201-215.
Ward G.M., Ward A.K., Dahm CN. & Aumen N.G.(1990)Origin and formation of organic and inorganic particlesin aquatic systems. The Biology of Particles in AquaticSystems (ed. R. S. Wotton), pp. 27-56. CRC Press, BocaRaton, Florida, USA.
Wilkinson L. (1990) SYSTAT: the System for Statistics.SYSTAT, Inc., Evanston, Illinois, USA.
