Detritivory and the stoichiometry of nutrient cycling by a dominant fish species in lakes of varying productivity

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1 OIKOS : /, 26 DOI: /j x Detritivory nd the stoichiometry of nutrient cycling by dominnt fish species in lkes of vrying productivity Kren A. Higgins, Michel J. Vnni nd Mri J. González Higgins, K. A., Vnni, M. J. nd González, M. J. 26. Detritivory nd the stoichiometry of nutrient cycling by dominnt fish species in lkes of vrying productivity. / Oikos : /. Little is known bout the stoichiometry of nutrient cycling by detritivores. Therefore, we explored stoichiometric reltionships in n omnivorous/detritivorous fish (gizzrd shd, Dorosom cepedinum) in three lkes tht differed in productivity. Gizzrd shd cn feed on plnkton nd sediment detritus, but in ll three lkes dult gizzrd shd derived /98% of crbon (C) nd phosphorus (P), nd /9% of nitrogen (N) from sediment detritus, nd the reminder from zooplnkton. Gizzrd shd selectively consumed detritus with higher C, N nd P concentrtions thn mbient lke sediments. Selective detritivory (i.e. the nutrient content of consumed detritus divided by the nutrient content of mbient detritus) ws most pronounced in the lke with the lowest detritl nutrient concentrtions. N nd P cycling rtes per fish were lso consistently higher in this lke, in greement with the prediction of stoichiometry theory tht excretion rtes should increse with food nutrient content. Among-lke differences in nutrient cycling rtes were unrelted to inter-lke vrition in fish body nutrient contents, which ws miniml. The N:P rtio excreted ws ner Redfield (/14:1) in ll three lkes. Stoichiometric nlyses showed tht the C:N nd C:P rtios of sediment detritus were much higher (/2.8/) thn rtios of gizzrd shd bodies, reveling substntil N nd P imblnces between consumers nd their food source. Gizzrd shd llevite N imblnce by selectively feeding on high N detritus (low C:N, high N:P), nd pprently llevite P imblnce by excreting nutrients t higher N:P thn tht of their food or their bodies. Thus, this detritivore pprently regultes nutrient cquisition nd lloction vi both pre-bsorption processes (selective feeding) nd post-bsorptive processes (differentil N nd P excretion). K. A. Higgins, M. J. Vnni nd M. J. González, Dept of Zoology, Mimi Univ., Oxford, OH 46 USA (vnnimj@muohio.edu). Present ddress for KAH: North Crolin Dept of Environment nd Nturl Resources, 22 Division of Wter Qulity, 1617 Mil Service Center, Rleigh, NC USA. Ecologicl stoichiometry hs emerged s frmework for understnding nutrient limittion of consumers nd consumer-medited nutrient cycling (Sterner nd Elser 22, Frost et l. 2, Hessen nd Elser 2, Moe et l. 2). Stoichiometry theory predicts tht nutrient cycling by consumer depends on the imblnce between the nutrient content of the consumer nd its food. All else being equl, consumer will relese more nutrients if its food nutrient content is high thn if its food nutrient content is low. Similrly, given equivlent food, consumer with high body nutrient content should relese less of tht nutrient thn consumer with low body nutrients. Nutrient rtios should lso behve ccording to stoichiometric principles, i.e. consumer with low body nitrogen:phosphorus (N:P) rtio should excrete nutrients t higher N:P rtio Accepted 9 Februry 26 Copyright # OIKOS 26 ISSN OIKOS : (26) Online Erly (OE): 1-OE

2 thn consumer with high body N:P, if the two consumers et the sme food (Elser nd Urbe 1999, Sterner nd Elser 22). Most studies ddressing the stoichiometry of consumer /resource interctions focus on herbivore /plnt interctions (Sterner nd Elser 22, Moe et l. 2). In contrst, few studies hve exmined stoichiometric reltionships between detritivores nd detritus (Cross et l. 23, Moe et l. 2, Frost et l. 2). Detritus is often poor qulity in terms of nutrient:crbon rtios; thus, detritivores my be prticulrly nutrient-limited becuse of reltively strong stoichiometric imblnce (Moe et l. 2). This potentil imblnce lso hs implictions for nutrient cycling, becuse the rtes nd rtios by which detritivores relese nutrients should depend on this imblnce (Vnni 1996, Vnni et l. 22). Consumers hve severl potentil strtegies for deling with stoichiometric imblnces (Anderson et l. 2, Frost et l. 2). For exmple, consumers my selectively feed on high nutrient resources. Even detritivores feeding on pprently morphous detritus cn exhibit selectivity for high nutrient detritus (Bowen 1983). Consumers cn lso llevite stoichiometric imblnces vi post-ingestion processes, e.g. by selectively ssimilting, or llocting to growth, nutrients in short supply (Anderson et l. 2, Frost et l. 2). Yet, little is known bout how consumers, especilly detritivores, compenste for stoichiometric imblnces nd how these imblnces medite nutrient cycling. In freshwter ecosystems, nimls cn ply importnt but vrible roles in nutrient cycling (Vnni 22). The role of fish in nutrient cycling seems prticulrly vrible mong ecosystems (Vnni 22, Mehner et l. 2, Srnelle nd Knpp 2). In lkes, benthic-feeding detritivorous fish re often importnt in nutrient cycling (Brbrnd et l. 199, Schus et l. 1997, Zimmer et l. 26, Vnni et l. in press), nd some evidence suggests tht these detritivores re more consistently importnt thn plnktivorous fish in nutrient cycling (Srnelle nd Knpp 2). Yet, little is known bout the stoichiometry of nutrient cquisition, incorportion, nd relese by these importnt consumers (Schindler nd Eby 1997, Hood et l. 2, Moe et l. 2). In this study, we investigted the stoichiometry of nutrient cycling by dominnt omnivorous/detritivorous fish species, the gizzrd shd (Dorosom cepedinum). Gizzrd shd re widespred throughout the midwestern nd southern US, nd often dominte fish biomss in reservoirs (Vnni et l. 2, in press) nd wrm-wter nturl lkes (Bchmnn et l. 1996). Severl studies show tht gizzrd shd cn be importnt in nutrient cycling nd/or food web regultion (reviewed by Vnni et l. 2). Gizzrd shd re omnivores, displying both ontogenetic shifts in diet s well s omnivory within individuls. Lrve re obligte zooplnktivores, but post-lrvl individuls (i.e. those /2 or 3 months old) consume detritus (sediments) nd zooplnkton (nd occsionlly phytoplnkton). Understnding the extent to which gizzrd shd consume zooplnkton versus sediments is importnt, becuse detritivorous shd trnslocte nutrients from sediments to the wter column, thereby providing new nutrients for phytoplnkton (sensu Dugdle nd Goering 1967, Crco et l. 1992). In contrst, plnktivorous shd recycle nutrients lredy in the wter column (Vnni 22). In ddition, the stoichiometric reltionships between gizzrd shd nd their food resources re likely to differ depending on whether shd re zooplnktivorous or detritivorous. Our objective in this study ws to quntify the stoichiometric reltionships between gizzrd shd, their food resources, nd their excret. Towrds tht end, we quntified gizzrd shd diet composition, the nutrient (N nd P) contents nd rtios of gizzrd shd bodies nd their food resources, nd the rtes nd rtios t which gizzrd shd excrete nutrients. We then evluted the extent to which excretion rtes nd rtios cn be explined by stoichiometric constrints. We evluted these stoichiometric reltionships in three lkes tht differ in productivity, so tht we cn ssess the generlity of our findings. Severl spects of gizzrd shd biology nd their food resources my vry with productivity, such s gizzrd shd bundnce nd diets (Vnni nd Hedworth 24, Vnni et l. 2) nd the nutrient content of sediment detritus (Nürnberg 1988). The three study lkes spn regionl lke productivity grdient, nd re representtive of low, moderte nd high productivity lkes (Vnni et l. 2). Thus, generlities discovered here re likely to pply to the productivity grdient in this geogrphic region. In complementry study, we used the nutrient cycling results we report here, nd other informtion, to ssess the extent to which nutrient cycling by gizzrd shd sustins whole-lke primry productivity in these nd four other lkes (Vnni et l. in press). Methods Study sites This study ws conducted in three reservoirs in Ohio, USA (Tble 1). Burr Ok is mesotrophic nd resides in mostly forested wtershed, Plesnt Hill is eutrophic nd hs wtershed with nerly equl proportions of forest nd griculture, nd Acton Lke is hypereutrophic nd locted in n griculturl wtershed (Knoll et l. 23). These lkes spn representtive productivity grdient for lkes in this region (Knoll et l. 23, Vnni et l. 2). They lso exhibit grdient with respect to zooplnkton ssemblges. Burr Ok hs the highest cldocern biomss nd the lowest rotifer biomss, while 2-OE OIKOS : (26)

3 Tble 1. Chrcteristics of the three study lkes. Totl phosphorus, chlorophyll nd primry production dt re epilimnetic vlues t the deepest re ner the dm, from My through September 1998/2, nd re tken from Knoll et l. (23). Acton hs the lowest cldocern biomss nd the highest rotifer biomss; Plesnt Hill is intermedite (Bunnell et l. 23). The study lkes re typicl of most midwestern reservoirs in tht they re comprtively wrm nd shllow with reltively lrge wtersheds reltive to lke surfce re (Knoll et l. 23). Gizzrd shd diet nlyses Burr Ok Plesnt Hill Acton Surfce re (h) Men depth (m) Totl phosphorus (mg Pl 1 ) Chlorophyll (mg l 1 ) Phytoplnkton primry production (mg Cm 2 d 1 ) To quntify diets, 1 dult gizzrd shd were collected from ech lke vi electrofishing on three dtes June, July, nd October 2), for totl of 9 fish (148/ 27 mm totl length; medin/189). Fish were immeditely plced on dry ice. In the lbortory, we dissected the fish, removed the contents of the foregut, nd split the contents into two smples. One ws nlyzed microscopiclly to quntify zooplnkton in diets (recognizble phytoplnkton were rrely observed in guts nd were not quntified), nd the other ws used for nutrient nlyses. To clculte the number of zooplnkton in guts, two subsmples were tken from the smple set side for microscopic nlysis (ech subsmple/% of totl smple) nd exmined under microscope. All tx were counted, nd cldocerns nd non-nuplir copepods were lso mesured. Biomss of individuls ws obtined using published weights for prticulr rotifer species, nd from length /mss regressions for cldocerns nd copepods (Sigler 22). Then the entire smple used to quntify zooplnkton, including processed subsmples, ws filtered onto Gelmn AE 47-mm glss fiber filter, dried nd weighed to obtin totl dry mss. The hlf set side for nutrient nlyses ws used to quntify prticulte phosphorus (P), crbon (C), nd nitrogen (N). Subsmples were plced in drying oven t 68C for 24 h nd then weighed to obtin dry mss. The P content ws then determined by shing in muffle furnce, followed by HC1 digestion nd subsequent nlysis of liberted soluble rective P (Stinton et l. 1977). C nd N contents were determined using Perkin Elmer Series 24 elementl nlyzer. Fish presumbly do not ssimilte inorgnic C (i.e. C ssocited with crbontes), but the sediments of these lkes contin OIKOS : (26) considerble mounts of crbontes. Therefore, we obtined the orgnic crbon content of food in the gut s the difference between totl C nd inorgnic C. To obtin inorgnic C, subsmples were plced in muffle furnce t 8C for 4 h to burn off orgnic mtter, then nlyzed for C. Totl C ws obtined by nlyzing nonshed subsmples. These methods provide mesure of totl nutrient mss in guts (i.e. detritl nd zooplnkton nutrients). To estimte the mounts of nutrients tht gizzrd shd obtined from detritus, we subtrcted nutrients in zooplnkton from the totl nutrient mss in gut smples. To estimte nutrients in zooplnkton, we multiplied zooplnkton biomss times the C, N nd P concentrtion (nutrient mss dry mss 1 ) for ech zooplnkton group nd then summed these products. Nutrient concentrtions of zooplnkton were ssumed to be.4 (C),.1 (N) nd.1 (P), except for Dphni, which ws ssumed to hve P concentrtion of.1 (Andersen nd Hessen 1991). To determine potentil detritl food qulity vilble to shd, three sediment cores were collected t shllow res in the upstrem portion of ech lke (i.e. gizzrd shd hbitt) in mid summer, lte summer, nd erly fll in 2 nd 21 (totl N/18 for ech lke). The top two cm of sediment (the lyer most likely consumed by gizzrd shd) ws scrped off nd ground to fine powder. Subsmples were processed for nutrients in exctly the sme mnner s gut nutrient smples. Sediment nutrient concentrtions did not vry over time within lke (ANOVA, P/., log-trnsformed dt), so we pooled ll smples from ll dtes nd exmined differences in nutrient concentrtions nd rtios mong the three lkes using ANOVA nd Tukey-Krmer HSD tests on log-trnsformed dt. We lso evluted gizzrd shd feeding selectivity within ech of the generl food ctegories (i.e. detritus nd zooplnkton). To evlute detritivorous feeding selectivity, we clculted selectivity index for ech element (C, N nd P), defined s the concentrtion of tht element in gut detritus (totl nutrients in foregut minus nutrients derived from zooplnkton) divided by nutrient concentrtion of the sediment (Mris 198). Rtios tht were t lest two stndrd errors greter thn 1. were tken s evidence of selective feeding. Differences in selectivity indices mong elements nd lkes were tested by performing two-wy ANOVA (/.) on log-trnsformed dt. To quntify zooplnktivorous feeding selectivity, Chesson s (1983) coefficient of selectivity ws clculted for ech zooplnkton group (rotifers, copepods, nuplii, nd cldocerns) s /(r i /p i )/ (r i /p i ), where r i is the proportion of totl zooplnkton individuls in gizzrd shd guts comprised of group i. p i is the proportion of totl zooplnkton individuls comprised of group i in zooplnkton smples tken with plnkton net (63 mm mesh) t upstrem sites where shd were collected. Chesson s coefficient vries 3-OE

4 from /1, nd vlue /1/number of prey items (in this cse,.2) indictes selective feeding on tht group. Excretion experiments We mesured the rtes t which gizzrd shd excreted N (s mmonium) nd P (s soluble rective phosphorus) in the three study lkes in July 1999 (temperture /248C), June 2 (/248C), July 21 (/288C), nd October 21 ( /18C), using methods similr to those of Schus et l. (1997). Our gol ws to mesure rtes on /3 fish of vrying size per lke per experiment, but this ws not lwys possible given the vilbility of fish on ny given dte. We included fish of ge /3 yers, lthough we did not include ny lrve. Gizzrd shd were collected by electrofishing t the upstrem end of ech reservoir during middy, i.e. fter shd hd been feeding for severl hours (Pierce et l. 1981). Individul fish were plced for /3 min in coolers with 4 l of lke wter prefiltered (.3 mm glssfiber filter) to remove lge nd bcteri tht could tke up relesed nutrients. Smples for finl nutrient concentrtions were collected nd immeditely filtered (Gelmn AE filters). Excretion rtes were obtined s the difference between initil nd finl N nd P concentrtions (Schus et l. 1997). Comprisons of excretion rtes using this method nd bioenergetics/mss blnce models show tht the two pproches yield similr rtes (Vnni 1996, Schus et l. 1997, Schindler nd Eby 1997, Vnni et l. 22, Vnni nd Hedworth 24, Hood et l. 2). Becuse excretion rtes (per fish) usully vry llometriclly with body mss (e.g. Schus et l. 1997, Gido 22), we exmined differences mong lkes in excretion rtes using ANCOVA with log excretion rte (N or P excreted per individul) s the dependent vrible nd log wet body mss s covrite. We first conducted two-wy ANCOVA contining dte nd lke s min effects, s well s lke/dte nd lke/log body mss interction terms. We found significnt lke/dte interction, so we then conducted seprte ANCOVAs on ech dte. For ll of these ANCOVAs, we initilly included lke/log body mss interction term. However, if this interction term ws not significnt (P/.), we deleted it nd re-rn ANCOVAs. We conducted the sme nlyses on the N:P rtio t which nutrients were excreted, except tht rtios were not logtrnsformed prior to nlyses. Specific differences mong lkes in excretion rtes nd rtios were compred using orthogonl contrsts. Gizzrd shd body nutrients We quntified nutrient contents of gizzrd shd bodies in the three study lkes. Shd were collected during lte summer 1999 nd 2, de-gutted, dried, nd ground to fine powder with Retsch Model ZM tissue grinder. Smples of dried, ground fish were weighed nd nlyzed for C nd N (duplicte smples on ech fish) nd P (triplicte smples on ech fish) using the sme methods s used for sediments nd guts. We ssyed body nutrients on totl of 61 fish (16 from Burr Ok, 26 from Plesnt Hill nd 19 from Acton) rnging in size from 163 / 264 mm. Becuse nutrient contents of fish sometimes vry with body size (Dvis nd Boyd 1978), we used ANCOVA with log wet mss s covrite, to ssess differences mong lkes in body nutrient contents nd rtios. Initilly, ANCOVAs included lke/mss interction term, but this term ws not significnt in ny of the ANCOVAs. Therefore we deleted the interction terms nd re-rn nlyses. We lso compred coefficients of vrition (CV//SD/men) mong tissue smples within fish, nd mong fish, to ssess sources of vribility in body nutrient contents. Results Gizzrd shd diets Diet composition Gizzrd shd diets in ll three lkes were comprised lrgely of sediment detritus. In ll three lkes, shd derived /99% of their orgnic C, /98% of their P, nd /9% of their N from sediments. Differences mong lkes in these percentges were slight nd not significnt (P/. for ll 3 elements). Zooplnktivorous feeding selectivity The few zooplnkton tht occurred in the guts were mostly rotifers, followed by nuplii, copepods, nd cldocerns in order of descending frequency (Sigler 22). Zooplnktivorous feeding selectivity vried considerbly mong lkes nd dtes, but there ws no generl trend towrds selectivity of lrge tx (Fig. 1). Burr Ok gizzrd shd strongly selected rotifers on ll three dtes, s did those in Plesnt Hill in October 21 (Fig. 1). Nuplii were strongly preferred in Plesnt Hill in June 2 nd were lso selected (long with cldocerns) in Plesnt Hill in July 21. In Acton, cldocerns were selected in June 2, copepods were selected in July 21, nd no txon ws preferred in October 21 (Fig. 1). Nutrient contents of sediment detritus Acton sediments tended to hve the highest nutrient concentrtions, lthough differences in N concentrtion were not significnt (Fig. 2). Burr Ok sediments hd the lowest C concentrtion, while Plesnt Hill sediments hd the lowest P concentrtion. Nutrient rtios of sediments differed little mong lkes. Neither the C:N 4-OE OIKOS : (26)

5 Rotifers Nuplii Copepods Cldocerns Burr Ok Plesnt Hill Orgnic crbon (mg C/g dry mss) Nitrogen (mg N/g dry mss) Sediment detritus,b b (.7) Ingested detritus 12.9 (1.6) 3. (.3) b 7. (.9) b 3.7 (.7),b 8.7 (2.6),b Chesson's index Acton Phosphorus (mg P/g dry mss) C:N (molr) ,b b (.8) 4.3 (.6) b b 3.7 (.),b,b.2. June 2 July 21 October 21 Fig. 1. Chesson s index of feeding selectivity for zooplnktivorous feeding by gizzrd shd. Vlues bove dshed lines indicte selective feeding on tht group. nor the N:P rtio differed significntly mong lkes, while the C:P rtio ws higher in Plesnt Hill thn the other two lkes (Fig. 2). Nutrient contents of ingested detritus C, N nd P concentrtions in ingested sediment detritus were significntly higher in Burr Ok thn in Plesnt Hill, with Acton intermedite (Fig. 2). In ll three lkes, nutrient concentrtions of ingested detritus were higher thn those of mbient lke sediments, indicting selective feeding on reltively high qulity detritus (see lso next section). The C:N rtio of ingested detritus ws higher in Plesnt Hill thn in Burr Ok, but other differences in nutrient rtios were not significnt (Fig. 2). OIKOS : (26) C:P (molr) N:P (molr) 1 1 b BO PH AC 1 1 BO PH AC Fig. 2. C, N nd P contents nd rtios (men9/se) in mbient lke sediment detritus (left-hnd column) nd in detritus ingested by gizzrd shd (right-hnd column). Error brs represent vrition mong fish in prticulr lke. All rtios re molr. Within pnel, mens tht re not significntly different from ech other hve common letters t the bse of brs. Numbers bove brs in the pnels depicting C, N nd P concentrtions represent detritivorous feeding selectivity indices (SE in prentheses). Index vlues significntly /1 indicte selective feeding on detritus tht is enriched with tht element, compred to lke sediments. -OE

6 Detritivorous feeding selectivity For ll elements, detritivorous feeding selectivity indices were significntly /1., indicting selective feeding on nutrient-rich detritus (Fig. 2). Two-wy ANOVA reveled significnt min effects of lke nd element (PB/.1) nd no lke/ element interction. Thus, we deleted the interction term, re-rn the ANOVA nd explored differences in min effects by exmining pired contrsts. This reveled tht feeding selectivity ws higher in Burr Ok thn in Plesnt Hill or Acton (which did not differ significntly from ech other) nd tht feeding selectivity ws higher for N thn for C or P (which did not differ significntly from ech other). Nutrient rtios provide dditionl evidence of higher feeding selectivity for N thn for C or P. In ll three lkes, the C:N rtio of ingested detritus ws lower thn tht of lke sediments, while the N:P rtio of ingested detritus ws higher thn tht of lke sediments. In contrst, C:P rtios were similr in ingested sediments nd lke sediments (Fig. 2). Acton Plesnt Hill Nutrient excretion For ll ANCOVAs on excretion rtes, the lke/body mss interction ws not significnt, so we deleted the interction term nd re-rn ANCOVAs. The ANCOVA models explined /4% of the vrince in excretion rtes in ll cses except July 21 (R 2 /.49 for P nd.23 for N). N nd P excretion rtes of individul gizzrd shd were significntly (P/.1 in ll cses) nd positively (Fig. 3) correlted with fish wet mss. N nd P excretion rtes differed significntly mong lkes during ll experiments (PB/.31 in ll cses). N excretion rtes in Burr Ok were higher thn those in Plesnt Hill on ll dtes, nd higher thn those in Acton on ll dtes except one (Fig. 3). N excretion rtes differed between Acton nd Plesnt Hill on two dtes, but the rnking of these two lkes ws not consistent mong experiments. Burr Ok P excretion rtes were higher thn t lest one other lke on ll dtes, while Acton nd Plesnt Hill differed on only one dte (Fig. 3). Among-lke Burr Ok July 1999 July 1999 N excretion rte (µg N fish -1 h -1 ) AC PH BO 1 June 2 PH AC BO 1 July 21 PH AC BO 1 October 21 AC PH BO 1 1 Wet mss (g) P excretion rte (µg P fish -1 h -1 ) 1 June 2 1 July 21 1 October 21 AC PH BO PH AC BO PH AC BO AC PH BO 1 1 Wet mss (g) Fig. 3. N nd P excretion rtes of gizzrd shd in four experiments in the three lkes. Ech point represents n individul fish. Letters connected by line indicte sttisticlly indistinguishble excretion rtes between lkes, bsed on ANCOVA (AC/Acton; BO/Burr Ok; PH/Plesnt Hill). 6-OE OIKOS : (26)

7 differences in excretion rtes corresponded to monglke differences in nutrient contents of detritus ingested by gizzrd shd. Tht is, fish in Burr Ok hd the highest excretion rtes s well s the highest gut nutrient contents, while Plesnt Hill fish tended to hve the lowest excretion rtes nd the lowest gut nutrient contents (Fig. 2, 3). Overll, excretion rtes were lowest in the October experiment, corresponding to the lower temperture during this time. However, N excretion rtes of lrger fish were lso reltively low in July 21, when tempertures were highest (Fig. 3). Differences in N:P excretion rtios mong lkes were not nerly s consistent s those for excretion rtes, nd vrince explined ws much less for rtios (R 2 lwys B/.36; Sigler 22) thn for excretion rtes. N:P excretion rtio differed mong lkes in two experiments (June 2 nd October 21) nd vried significntly with body mss in only one experiment (October 21). In the October experiment, the N:P excretion rtio ws significntly higher in Plesnt Hill thn in the other two lkes. However, in the June 2 experiment, significnt lke/body mss interction precluded specific comprisons mong lkes. Averged over ll experiments, men N:P excretion rtios were very similr mong lkes (14., 14. nd 13.6 (molr) for Acton, Plesnt Hill, nd Burr Ok, respectively). Gizzrd shd body nutrients We found severl differences mong lkes in gizzrd shd body nutrient contents nd rtios, s well s significnt effects of fish body mss in most cses. However, differences mong lkes were generlly smll (Fig. 4), s ws the mount of vrince explined by these reltionships (R 2 B/.17 in ll cses). Body C nd P, s well s body C:N nd C:P rtios, vried significntly with fish mss. The reltionship between mss nd body P ws positive, while mss ws negtively correlted with body C, C:N nd C:P (Fig. 4); however, slopes were reltively shllow. Body C, s well s C:N nd C:P rtios, were significntly higher in Plesnt Hill thn in the other lkes, while fish in Burr Ok hd the highest N content. Body P content ws not significntly different mong lkes. We observed reltively little vrition mong tissue smples (i.e. within fish) in C nd N contents nd the C:N rtio (Tble 2). Pooling ll lkes, the men coefficient of vrition (CV) mong replicte tissue smples (i.e., within-fish vrition) ws only 2.9% for C nd 4.4% for N, wheres the men CV mong fish ws 12.7% for C nd 7.1 for N (Tble 2). For the C:N rtio, the CV mong fish ws lso much higher thn tht within fish (17.3 vs 2.8%, Tble 2). Thus, for C, N nd C:N, vrition mong fish ws much greter thn Fig. 4. Gizzrd shd body C, N nd P contents nd rtios in the three study lkes. Ech point represents n individul fish. Percentges re expressed per unit dry mss, nd rtios re molr. %C %N %P Wet mss (g) Wet mss (g) Burr Ok C:N C:P N:P Plesnt Hill Acton OIKOS : (26) 7-OE

8 Tble 2. Vrition within fish (i.e. mong replicte tissue smples) nd mong fish for body C, N, P nd C:N. CV is the coefficient of vrition (SD/men), nd the rtio refers to tht obtined by dividing mong- by within-. Men within- ws obtined by clculting CV (vrition mong tissue smples) for ech individul fish, then tking the men of these vlues. See text for detils. Lke Crbon Nitrogen Phosphorus C:N Among () Men within (b) Rtio (/b) Among () Men within (b) Rtio (/b) Among () Men within (b) Rtio (/b) Among () Men within (b) Rtio (/b) Burr Ok Plesnt Hill Acton All lkes pooled tht within fish (i.e., mong replicte tissue smples) (Tble 2). In contrst, within-fish vrition in P ws nerly s gret s mong-fish vrition in P (Tble 2), even though we nlyzed more tissue smples per fish for P (3 smples) thn for C nd N (2 smples). Note tht we cnnot quntify within-s for N:P or C:P rtios, becuse within fish we ssyed P on different tissue smples from those used to ssy C nd N. Discussion Detritivory versus zooplnktivory Gizzrd shd obtined nerly ll ingested C, N nd P from sediment detritus in ll three lkes. This contrsts with the prediction of Vnni nd Hedworth (24) tht these fish would consume reltively more detritus nd less zooplnkton t high productivity. The prediction is bsed on the ssumptions tht lrge-bodied (hence energeticlly preferred) zooplnkton re reltively more vilble t low productivity, nd tht gizzrd shd prefer zooplnkton over detritus, becuse the former re more nutritious. Cldocerns re in fct reltively more bundnt, nd rotifers less bundnt (in terms of both percent individuls nd biomss), in Acton thn in Burr Ok, with Plesnt Hill intermedite. This pttern holds on the dtes we smpled s well s in generl in these lkes (Bunnell et l. 23, Vnni et l. 2). However, we found no evidence tht dult gizzrd shd selectively preyed on lrge zooplnkton. However, lrge tx were exceedingly scrce in these lkes. For exmple, Dphni never comprised /1% of totl zooplnkton biomss, nd only comprised /% in 2 of 9 smples. The observtions tht zooplnkton comprised smll frction of shd diets, nd tht shd did not select lrgebodied zooplnkton, suggest tht these fish my more esily cpture smll-bodied zooplnkton s they feed on detritus. As lrve, gizzrd shd visully select individul zooplnkters. However, when they re few months old (/2/3 mm in length), gizzrd shd become pump filter feeders (Drenner et l. 1984), t which time they lso obtin the cpcity to consume nd digest detritus (Pierce et l. 1981, Heinrichs 1982). Smll zooplnkton tht re wek swimmers (i.e. nuplii nd mny rotifers) my be esier to cpture in this feeding mode (Drenner et l. 1984). Alterntively, zooplnkton species composition my be different ner the sediments (where shd feed) thn in integrted wter column smples (where zooplnkton smples were collected). We observed selective detritivory in ll three lkes. Tht is, shd consumed detritus tht ws reltively nutrient rich compred to lke sediments. Selectivity ws highest in Burr Ok, where sediment C nd nutrient concentrtions were lso lowest (Fig. 2), suggesting tht gizzrd shd exhibit higher selectivity when feeding on poorer qulity detritus. Such pttern ws lso observed by Mundhl nd Wissing (1988), who found tht gizzrd shd feeding on Acton Lke sediments hd selectivity index for N of 6.1, while gizzrd shd fed low-qulity lbortory diet hd selectivity index for N of 13.2, similr to the rnge we observed (Fig. 2). Other detritivorous fish lso hve the cpcity to selectively feed, prticulrly on detritus with high N concentrtions (Odum 197, Bowen 1983, Ahlgren 1996). The behviorl nd/or morphologicl mechnisms by which detritivorous fish ccomplish this re not well known (Bowen 1983). In Acton Lke, gizzrd shd feed selectively on sediment prticles of low density, which contin higher concentrtions of orgnic mtter, C nd N (Smoot 1999). Thus, reltively light, orgniclly enriched sediment prticles my be selectively filtered over hevier prticles such s inorgnic sediments, s hs lso been observed for mullet, detritivorous fish common in esturies (Odum 197). Little is known bout the stoichiometric reltionships between detritivores nd their food (Sterner nd Elser 22). However, it hs been suggested tht detritivorous fish re more likely to be nutrient-limited (s opposed to energylimited) thn other fish becuse of the lrge imblnce between the nutrient contents of detritus nd fish (Schindler nd Eby 1997, Sterner nd Elser 22). While 8-OE OIKOS : (26)

9 detritivorous fish my in fct be nutrient-limited, selective feeding on high qulity detritus cn t lest prtilly llevite nutrient limittion, nd must be considered in models of detritivore stoichiometry (Vnni 1996). We ssessed detritl resources using 2-cm deep sediment cores, but gizzrd shd my forge in thinner lyer of freshly deposited surficil sediments tht my be more enriched in crbon nd nutrients thn 2-cm core smple. It is therefore possible tht the selectivity we observed resulted from indequte smpling of food resources. However, we do not think this is the cse, bsed on the work of Mundhl nd Wissing (1988). They quntified C nd N feeding selectivity of detritivorous Acton Lke gizzrd shd using the sme methods we used, except tht they collected freshly deposited sediments using sediment trps tht were deployed in the lke for just 18/2 h. The C nd N contents of these freshly deposited sediments were similr to, or lower thn, those we observed. For exmple, Mundhl nd Wissing (1988) report rnge of.1 /.4% N (s dry mss) in their sediments, wheres we observed men of.18% N (rnge.13 /.23) in our Acton sediment smples. Mundhl nd Wissing (1988) report rnge of totl C (they did not quntify orgnic C) of 2.8 / 3.4%, wheres we observed somewht higher C concentrtions (men totl C/4.6% [rnge 4.3 / 4.9]; men orgnic C/2.1% [rnge 1.7 / 2.6]) in our sediment smples. In ddition, s mentioned bove, Mundhl nd Wissing (1988) observed C nd N selectivity indices similr to those we observed (they did not quntify P in sediments or shd guts). Thus, gizzrd shd pper ble to selectively consume high C nd N detritus, even compred to freshly deposited sediments. Nutrient excretion N nd P excretion rtes were lwys higher in Burr Ok thn in t lest one other lke, nd fish in Burr Ok lso consumed detritus with the highest nutrient concentrtion. This reltionship supports stoichiometry theory, which predicts tht excretion rtes will increse with food nutrient content, s long s other fctors (e.g. consumer body nutrient content, feeding rte, growth rte) remin constnt (Sterner nd Elser 22). We found no significnt mong-lke differences in fish body P contents, so the higher P excretion rtes of Burr Ok fish cnnot be explined by differences in body P. Burr Ok gizzrd shd ctully hd higher body N contents thn fish in the other lkes, yet still hd higher N excretion rtes. While this reltionship ppers to contrdict stoichiometry theory, differences mong lkes in fish body N were reltively smll, especilly in reltion to vrition within lke (Fig. 4). In ddition, we observed considerble vrition mong fish in body nutrient contents, nd for P, considerble vrition OIKOS : (26) mong replicte tissue smples within fish (Tble 2). This vrition mong nd within fish my hve mde it more difficult to detect differences mong lkes in body nutrients. Vrition mong fish in C content my be due to vrible lipid storge; we noticed considerble vrition in oil content mong fish s they were ground for nutrient nlyses. Higher within-fish vrition for P (compred to tht for C or N) my result from vrition in the contribution of smll bone or scle frgments (which re P-rich) to smples. The positive ssocition between the nutrient contents of ingested detritus nd nutrient excretion rtes re consistent with the predictions tht nutrient relese rtes increse with food nutrient content. However, lterntive explntions re possible. For exmple, feeding rtes nd/or ssimiltion efficiencies (for N nd/or P) of Burr Ok gizzrd shd my hve been higher thn in the other lkes. If either feeding rtes or ssimiltion efficiencies were higher in Burr Ok, the totl mount of nutrients ssimilted per fish would be higher, which could potentilly led to higher nutrient excretion rtes. We hve no informtion on how feeding rte or ssimiltion efficiency vries mong lkes, so we cnnot explicitly evlute these lterntive mechnisms. Recent models suggest tht post-ssimiltion mechnisms (i.e. djustment of excretion rtes) my be more effective thn differentil ssimiltion for generlist consumers (Anderson et l. 2), but much more work is needed to test this hypothesis (Frost et l. 2). Assuming tht the observed mong-lke differences in excretion rtes re due to stoichiometric constrints, our results suggest tht vrition in food nutrient content is more importnt thn vrition in consumer body nutrient content in determining excretion rtes. Few studies hve explicitly quntified how nutrient excretion vries with these two fctors. Elser nd Urbe (1999) nlyzed dt from severl zooplnkton studies nd concluded tht vrition in food (phytoplnkton) nutrient content ws more importnt thn vrition in zooplnkton body nutrients in determining N:P excreted by zooplnkton, in greement with our results. In contrst, Vnni et l. (22) found tht interspecific vrition in body P ccounted for lrge frction of interspecific vrition in P excretion rtes nd N:P excreted of fish nd tdpoles in tropicl strem. These pprently contrdictory findings probbly relte to the reltive vrition in food nutrient content versus consumer nutrient content. Phytoplnkton exhibit tremendous vrition in nutrient content compred to zooplnkton, so vrition in phytoplnkton my be reltively importnt in determining vrition in zooplnkton nutrient excretion. Regrding nutrient cycling by fish, body nutrient content my hve hd stronger effect on excretion in the Vnni et l. (22) study thn in our study becuse interspecific vrition in body P ws much greter thn the mong-lke vrition we 9-OE

10 observed in gizzrd shd body nutrients. More studies under nturl conditions nd with controlled, relistic diets re needed to help elucidte how diet nd consumer nutrient contents modulte excretion rtes nd rtios (Frost et l. 2). Although per cpit N nd P excretion rtes were highest in the lke of lowest productivity (Burr Ok), t the ecosystem scle nutrient flux through gizzrd shd increses with lke productivity (Vnni et l. in press). This is becuse gizzrd shd biomss increses gretly with productivity in these ecosystems (Vnni et l. 2, in press), nd this increse in biomss outweighs the opposing trend we found here of decresing per cpit rtes with incresing productivity. Thus, in terms of regulting ecosystem-scle nutrient cycling, gizzrd shd my hve stronger impcts in high-productivity lkes, lthough this will depend on how the mgnitude of other nutrient supplies vries long the productivity grdient. Selective detritivory, stoichiometry, nd nutrient excretion by gizzrd shd We observed substntil imblnces between mbient sediments nd shd bodies for both N nd P, reltive to C. Thus, the C:N nd C:P of mbient sediments were both /2.8/ tht of shd bodies (Fig. ). Gizzrd shd pprently hve different strtegies for deling with N versus P imblnces, yet strtegies pper to be the sme in ll three lkes. Selective feeding on high N detritus reduces the imblnce for N by roughly hlf, but selective feeding does not substntilly reduce the imblnce for P, reltive to C (Fig. ). As consequence, the N:P of consumed sediment is /1./ higher thn the N:P of mbient sediment or shd bodies. Thus, once sediments re consumed, shd pprently must selectively incorporte P, reltive to N, to mintin their body N:P. This is lso pprent from N:P excretion rtios, which re /2.1 higher thn shd bodies nd somewht higher ( /1.2/) thn consumed detritus (Fig. ). N:P rtios lso support stoichiometry theory, which predicts tht if food N:P is higher thn body N:P, the consumer will excrete t n N:P tht is even higher thn ingested food (Sterner nd Elser 22). Note tht the N:P reltionships we observed conform to stoichiometry theory only when we consider the N:P of detritus ctully consumed by shd, nd not just mbient lke sediments. Ambient sediments nd shd bodies hve similr N:P. Thus if we hd considered mbient sediments s food, we would hve predicted excretion N:P nd body N:P to be similr (Sterner nd Elser 22). Once gin, this highlights the importnce of selective detritivory in mediting the stoichiometry of nutrient cycling by gizzrd shd, nd more generlly, the need to crefully consider nutrient contents nd rtios of mteril ctully ingested by consumers rther thn Fig.. Men nutrient rtios of mbient lke sediments, detritus ingested by gizzrd shd, gizzrd shd bodies, nd (for N:P) nutrients excreted by shd. Arrows represent flow of nutrients nd energy in the lkes. All rtios re molr. relying on the nutrient sttus of mbient food sources s mesure of dietry nutrient content. Consumers relese nutrients vi egestion (feces) s well s excretion. We did not mesure egestion rtes, but it is useful to estimte how egestion nd excretion rtes my compre nd how they relte to stoichiometry. To do so, we used mss/blnce pproch to estimte egestion rtes in Acton Lke, where we hve considerble dt on gizzrd shd growth rtes. First we estimted ingestion rtes of detritivorous gizzrd shd in midsummer using the model described in Vnni nd Hedworth (24); most prmeters of this model derive from Acton gizzrd shd. Ingestion of sediment detritus (g dry mss 1-OE OIKOS : (26)

11 consumed fish 1 d 1 ) of g (wet mss) fish in lte July 2 ws estimted using dylength nd temperture. We converted this rte to N nd P ingestion rtes (g N or P consumed fish 1 d 1 ) using dt on gut sediment N nd P during the summer experiments reported here. We then estimted N ssimiltion by multiplying N ingestion by.77, the N ssimiltion efficiency reported for detritivorous Acton Lke gizzrd shd (Mundhl nd Wissing 1988). This yielded N ingestion nd ssimiltion rtes of 67.6 nd 2. mg N fish 1 d 1, respectively. Egestion ws then clculted s ingestion minus ssimiltion (1.6 mg N fish 1 d 1 ). We then compred tht to excretion using the mss blnce pproch nd using dt from the experiments we report here. To use the mss blnce pproch, we first estimted the mount of N llocted to growth using estimted growth rte of gizzrd shd of this size in summer 2 (22.4 mg dry mss d 1 ) nd the men body N content observed for Acton shd (9% of dry mss). This yielded n estimte of N llocted to growth of 2. mg N fish 1 d 1 ), nd predicted excretion rte of. mg N fish 1 d 1 (excretion/ssimiltiongrowth, or 2. / 2.). Thus, ccording to the mss blnce pproch, shd excreted 3.2/ s much N s they egested. The N excretion rte predicted by the mss blnce pproch ws /19% lower (. vs 62.1) thn the rte predicted from the mss vs N excretion regression generted from our July 2 experiment (Fig. 3), but ws within the confidence intervl of the regression generted by the experiment. We did the sme clcultions for P; however, we hve scnt dt on P ssimiltion efficiency, so for this exercise we used the sme vlue (.77) s for N ssimiltion efficiency. P ingestion, ssimiltion nd egestion were estimted to be 11.1, 8. nd 2.6 mg P fish 1 d 1, respectively. Alloction of P to growth ws estimted to be.7 mg P fish 1 d 1 (using men body P of 3.% of dry mss), yielding predicted excretion rte of 7.9 mg P fish 1 d 1,or/3./ s much s P egestion. The P excretion rte predicted by the mss blnce pproch ws bout 3% lower thn the rte predicted from the mss vs P excretion regression generted from our July 2 experiment (Fig. 3), but ws within the confidence intervl of this regression. Thus it ppers tht excretion is quntittively more importnt thn egestion, in terms of nutrient flux through gizzrd shd. In ddition, excreted N nd P re dissolved nd hence more biovilble (to phytoplnkton) thn egested nutrients, nd should thus hve greter impct on primry producers. Both excretion nd egestion my be importnt in the post-ingestion regultion of consumer body nutrient composition nd nutrient cycling (Anderson et l. 2, Frost et l. 2). However, we cnnot dequtely evlute the stoichiometry of egestion becuse we do not hve sufficient dt on P ssimiltion efficiencies. Future studies need to OIKOS : (26) quntify both egestion nd excretion so tht these postingestive processes cn be explicitly compred. Conclusions Mny spects of gizzrd shd diets nd nutrient cycling prmeters were similr in three lkes tht differ considerbly in productivity. In ll three lkes, nerly ll nutrients ingested by shd nd thus excreted into the wter column, were derived from sediment detritus. We did observe mong-lke vrition in excretion rtes, which ppers to be medited by selective detritivory. However, the rtio t which gizzrd shd excreted nutrients ws reltively constnt mong lkes, nd ppers to be driven by stoichiometric constrints, in prticulr the reltive imblnces between nutrients ingested nd sequestered in fish bodies. Becuse detritivores re criticl in nutrient cycling in mny ecosystems, it is importnt tht we quntify stoichiometric constrints on these consumers, nd how these constrints medite the mny linkges between detritus-bsed nd primry producer-bsed food chins (Moore et l. 24). Acknowledgements / We re grteful to the following individuls who ssisted with field work nd/or lbortory nlyses: K. Arend, H. 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