Biotic and abiotic controls on the ecosystem significance

15 Pages·2010·0.44 MB·English

FreshwaterBiology(2010)55,2047–2061 doi:10.1111/j.1365-2427.2010.02461.x
Biotic and abiotic controls on the ecosystem significance
of consumer excretion in two contrasting tropical streams
JONATHAN P. BENSTEAD*, WYATT F. CROSS†, JAMES G. MARCH‡, WILLIAM H.
MCCDOWELL§, ALONSO RAMI´REZ– AND ALAN P. COVICH†
*DepartmentofBiological Sciences,Universityof Alabama,Tuscaloosa, AL,U.S.A.
†Odum SchoolofEcology, UniversityofGeorgia, Athens, Georgia, GA,U.S.A.
‡Biology Department, Washington and JeffersonCollege,Washington, PA,U.S.A.
§Department ofNaturalResources and theEnvironment, UniversityofNew Hampshire, Durham,NH, U.S.A.
–Institutefor Tropical Ecosystem Studies,UniversityofPuerto Rico,SanJuan,PR, Puerto Rico
SUMMARY
1. Excretion of nitrogen (N) and phosphorus (P) is a direct and potentially important role
for aquatic consumers in nutrient cycling that has recently garnered increased attention.
The ecosystem-level significance of excreted nutrients depends on a suite of abiotic and
biotic factors, however, and few studies have coupled measurements of excretion with
consideration of its likely importance for whole-system nutrient fluxes.
2. We measured rates and ratios of N and P excretion by shrimps (Xiphocaris elongata and
Atya spp.) in two tropical streams that differed strongly in shrimp biomass because a
waterfall excluded predatory fish from one site. We also made measurements of shrimp
and basal resource carbon (C), N and P content and estimated shrimp densities and
ecosystem-level N and P excretion and uptake. Finally, we used a 3-year record of
discharge and NH -N concentration in the high-biomass stream to estimate temporal
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variation in the distance required for excretion to turn over the ambient NH -N pool.
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3.PercentC,N,andPbodycontentofXiphocariswassignificantlyhigherthanthatofAtya.
Only per cent P body content showed significant negative relationships with body mass.
C:NofAtyaincreasedsignificantlywithbodymassandwashigherthanthatofXiphocaris.
N : P of Xiphocaris was significantly higher than that of Atya.
4. Excretion rates ranged from 0.16–3.80 lmol NH -N shrimp)1 h)1, 0.23–5.76 lmol total
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dissolved nitrogen (TDN) shrimp)1 h)1 and 0.002–0.186 lmol total dissolved phosphorus
(TDP) shrimp)1 h)1. Body size was generally a strong predictor of excretion rates in
both taxa, differing between Xiphocaris and Atya for TDP but not NH -N and TDN.
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Excretion rates showed statistically significant but weak relationships with body content
stoichiometry.
5.Largebetween-streamdifferencesinshrimpbiomassdrovedifferencesintotalexcretion
by the two shrimp communities (22.3 versus 0.20 lmol NH -N m)2 h)1, 37.5 versus
4
0.26 lmol TDN m)2 h)1 and 1.1 versus 0.015 lmol TDP m)2 h)1), equivalent to 21% and
0.5% of NH -N uptake and 5% and <0.1% of P uptake measured in the high- and low-
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biomass stream, respectively. Distances required for excretion to turn over the ambient
NH -N pool varied more than a hundredfold over the 3-year record in the high-shrimp
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stream, driven by variability in discharge and NH -N concentration.
4
Correspondence:JonathanP.Benstead,DepartmentofBiologicalSciences,UniversityofAlabama,Tuscaloosa,AL35487,U.S.A.
E-mail:[email protected]
Presentaddress:WyattF.Cross,DepartmentofEcology,MontanaStateUniversity,Bozeman,MT59717,U.S.A.
(cid:2)2010BlackwellPublishingLtd 2047
2048 J. P. Benstead et al.
6. Our results underscore the importance of both biotic and abiotic factors in controlling
consumer excretion and its significance for nutrient cycling in aquatic ecosystems.
Differences in community-level excretion rates were related to spatial patterns in shrimp
biomass dictated by geomorphology and the presence of predators. Abiotic factors also
hadimportanteffectsthroughtemporalpatternsindischargeandnutrientconcentrations.
Future excretion studies that focus on nutrient cycling should consider both biotic and
abiotic factors in assessing the significance of consumer excretion in aquatic ecosystems.
Keywords:consumer-driven nutrient recycling, ecological stoichiometry, ElYunque,Luquillo
Experimental Forest, Puerto Rico
at the level of the individual consumer constrain
Introduction
rates and ratios of excretion, the abiotic environment
Animals have direct effects on nutrient cycling in ultimately sets the template for assessing the relative
aquatic ecosystems through their excretion of waste significance of recycled nutrients. Both the volume
products (Kitchell et al., 1979; Vanni, 2002). Inputs of and turnover rate of water (relative to consumer
biologically important elements (i.e. nitrogen [N] and biomass) are important, as are ambient nutrient
phosphorus [P]) from excretion complement and concentrations (McIntyre et al., 2008). Finally, the
interact with the indirect effects on nutrient cycling identity of the limiting nutrient may control the
mediated by consumers through their consumption potential significance of consumer excretion for eco-
and removal of biomass (Knoll et al., 2009). Fluxes of system processes (Vanni et al., 2002). Biotic and
N and P through consumer biomass have long been abiotic factors thus interact to control the potential
ofinteresttoaquaticecologists,fromtheperspectives role of consumer excretion as a significant flux in
of both physiology and nutrient cycling (e.g. Rigler, aquatic nutrient cycles (Hall et al., 2007; McIntyre
1961; Pomeroy, Matthews & Min, 1963). Interest in et al., 2008).
consumer excretion has recently increased, however, Given the potential interactions between these
spurred by renewed emphases on ecological stoichi- biotic and abiotic factors, populations of shrimps in
ometry and body size (Sterner & Elser, 2002; Wood- tropical streams represent useful model systems in
ward et al., 2005; Hall et al., 2007) and the role of whichtoexaminetherelativeimportanceofconsumer
excretion in mediating trophic cascades (e.g. Findlay excretion for ecosystem-level nutrient cycling.
et al., 2005). Despite this ongoing interest, the general Shrimps are relatively common components of trop-
significance of consumer excretion for whole-system ical stream communities, often occurring at high
nutrient cycling in aquatic ecosystems is still unclear densities and biomass (Covich, 1988b). Their spatial
(Vanni, 2002; Cross et al., 2005). distribution is often patchy at the catchment scale,
The relative magnitude of consumer excretion and because of interactions between geomorphology and
its potential significance to ecosystem-level nutrient the relative abundance of their predators. For exam-
cycling depend on a number of biotic and abiotic ple,inPuertoRico,densitiesofshrimpsarehighestin
factors. Characteristics of the consumer community thosereachesabovewaterfallsthatcannotbeaccessed
are clearly important. Both biomass of consumers by their predators (mostly fish species; Pringle et al.,
andthesizestructureoftheirpopulationscontrolthe 1999; Covich et al., 2009). In addition to spatial
rate of total nutrient excretion, with small consumers variability in shrimp density, the streams inhabited
having higher mass-specific rates of excretion than by these consumer taxa are relatively dynamic sys-
larger individuals (Hall, Tank & Dybdahl, 2003; Hall tems, in which the abiotic conditions that affect the
et al., 2007). Elemental demand (driven by body potential significance of consumer excretion (i.e.
stoichiometry and constrained by phylogeny) com- discharge and ambient nutrient availability) are
bines with diet nutrient content to control the extremely variable temporally. In sum, the spatial
nutrient ratios of excretion (Vanni et al., 2002; Torres and temporal variability typical of shrimps and their
& Vanni, 2007). Although stoichiometric interactions stream habitat results in the potential for great
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N and P excretion by stream consumers 2049
variation in the significance of shrimp excretion for Table1 Long-termmeandischargeandnutrientchemistry
nutrient cycling in these systems. data(±1SE)forthePrietaandBisleystreams,LuquilloExperi-
mentalForest,PuertoRico(January2000–October2003)
In this study, we measured resource and body
stoichiometry (%C, %N and %P) and excretion rates Variable Prieta Bisley
of N and P in two cosmopolitan genera of shrimps Discharge(Ls)1) 26 24
(Atya and Xiphocaris) collected from two tropical NH4-N(lMM) 0.5±0.03 0.3±0.04
Puerto Rican streams that differed greatly in shrimp NO3-N(lMM) 4.4±0.19 7.9±0.31
biomass because of geomorphic exclusion of preda- TDN(lMM) 9.6±0.50 12.6±0.29
tors.Toassessthesignificanceofshrimpexcretionfor SRP(lMM) 0.3±0.02 0.65±0.02
whole-reach nutrient dynamics, we combined excre- TDN,totaldissolvednitrogen;SRP,solublereactivephosphorus.
tion data with estimates of densities for these fresh-
watershrimpgenera(Crosset al.,2008)andcompared (R. Graham) Nichols. (sierra palm). Litter fall is
rates of potential N and P supply by shrimp to the continuous throughout the year, with maxima and
magnitude of ecosystem demand. Finally, we esti- minimaoccurringbetweenApril–JuneandDecember–
mateddistancesrequiredforshrimpexcretiontoturn March, respectively (Zou et al., 1995). Stream temper-
over the ambient NH -N pool over a 3-year period. atureissimilarinbothstreamsandrangesfrom18to
4
We discuss our results with respect to the likely 26 (cid:3)C (mean: 22 (cid:3)C; A. Ram´ırez, unpubl. data). Dis-
significance of consumer excretion for fluxes and charge responds rapidly to local storm events, is
cycling of nitrogen and phosphorus in these tropical highlyvariableandshowsnomajorseasonalpattern.
streams, as well as in aquatic ecosystems in general. Streamcommunities of ElYunquecontain upto 10
species of shrimps, including four species of Atyidae
(Atya lanipes Holthuis, Atya innocuous [Herbst], Atya
Methods scabra[Leach],andMicratyapoeyi[Gue´rin-Me´neville]),
one species of Xiphocarididae (Xiphocaris elongata
Study sites
[Gue´rin-Me´neville])andfivespeciesofPalaemonidae
Fieldwork for this study was conducted in single (Macrobrachium carcinus [L.], Macrobrachium faustinum
reachesoftwosecond-orderrainforeststreams,Queb- [De Saussure], Macrobrachium crenulatum Holthuis,
rada Prieta and Quebrada Bisley-3 (hereafter, Prieta Macrobrachium acanthurus [Wiegmann], and Macrob-
and Bisley, respectively), which drain the Luquillo rachium heterochirus [Wiegmann]). The shrimp assem-
Long-TermEcologicalResearch(LTER)sitewithinthe blage in the Prieta is dominated by X. elongata and
Luquillo Experimental Forest (LEF) in northeastern A. lanipes (>90% of individuals), with lower numbers
Puerto Rico (also known as the El Yunque National of A. innocuous, A. scabra, Micratya poeyi, and Macrob-
Forest and formerly the Caribbean National Forest). rachiumspp.TheBisleycontainsprimarilyX. elongata,
The LEF is characterised as tropical-wet forest and M. carcinus and M. faustinum (Covich & McDowell,
receives an average of 3.5 m of precipitation per year 1996). The two streams also differ with respect to
at the altitudes at which these streams are located densitiesofbothshrimpsandfishes.Ourstudyreach
(Heartsill-Scalley et al., 2007). Long-term averages on the Prieta is just upstream of a >10-m waterfall
indicate that May through December is typically that excludes all fishes except the algivorous goby
wetter than the rest of the year, but this seasonal Sicydiumplumieri(Bloch).Theabsenceofthepredatory
patternishighlyvariable.Thetwostreamreachesare mountain mullet (Agonostomus monticola [Bancroft])
similar in size (mean width 2–3 m) and mean dis- and American eel (Anguilla rostrata [Lesueur]) results
chargeandnutrientchemistry(Table 1).Bothstreams inrelativelyhighdensitiesofshrimpsinthisreach(up
drainsmall,steepcatchmentsandarecharacterisedby to 25 individuals m)2; Covich, 1988a; Covich et al.,
seriesofpoolsinterspersedwithboulder-linedriffles. 2009). Our study reach on the Bisley has no waterfall
Largebouldersandcobbledominatethesubstrata;fine downstream, supports populations of Agonostomus
sedimentsandsiltarepresentindepositionalareasof and Anguilla, and consequently has densities of
pools and between large boulders. The streams are shrimpsthataretwoordersof magnitudelower than
heavily shaded by riparian forest dominated by those in the Prieta (c. 0.1 individuals m)2, mostly
DacryodesexcelsaVahl.(tabonuco)andPrestoeamontana X. elongata;Townsendet al.,2002;Covichet al.,2009).
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2050 J. P. Benstead et al.
Shrimp excretion and body content measurements Basal resource stoichiometry
Shrimp excretion rates were measured during two We collected samples of dominant basal resources
periods in each stream: 23–26 March and 24 Novem- from each stream for C, N and P analysis during
ber–20 December 2004. Shrimps were captured using March and November–December 2004. Microbially
dip and seine nets. To aid capture, we sometimes conditioned,mixed-speciesleaflitterwascollectedby
usedshort(<1 s)pulsesfromabackpackelectrofisher hand along each stream reach. Suspended fine par-
to dislodge shrimps into the current where they ticulateorganicmatterwascollectedbyfilteringc. 4 L
could be more easily seined. Shrimps were never of stream water through 0.7-lm glass-fibre filters
incapacitated during capture using this method. (n = 5).Periphytonwascollectedbybrushingcobbles
Shrimps were held for <15 min before excretion (n = 5) and filtering slurries onto glass-fibre filters.
incubations began. Incubations were carried out by BasalresourcesampleswereanalysedforC,NandP
introducing single shrimps into 100 mL of filtered content using the same methods as earlier.
(glass-fibre, 0.7-lm pore size) stream water held in
polyethylene bags (22 · 12 cm) suspended in the
Estimating shrimp biomass and whole-reach excretion
stream. Timed incubations lasted c. 60 min (range
49–100 min). At the start and conclusion of the Toestimateabundanceandbiomassofshrimpsinthe
incubation, two 20-mL water samples were collected Prieta,weusedpass-depletionsamplingontwodates
and filtered (0.7-lm pore size). The water samples (20 February and 1 August 2005). On each date, six
and shrimp from each incubation were then placed sub-reaches (three pools and three riffles) were sam-
on ice and frozen within 6 h. pledbasedonfeasibilityofdepletion,whichrequired
Watersampleswereanalysedfor ammonium,total thattheupstreamanddownstreamendsbeeffectively
dissolved nitrogen (TDN), and total dissolved phos- blocked with seine nets (4-mm mesh). After blocking
phorus (TDP). Ammonium was measured using the bothendsofasub-reach,athirdseinenetwasdragged
phenol-hypochlorite colorimetric method (Solorzano, in a downstream direction by two people so that
1969) automated with a SmartChem robotic analyzer shrimps were captured in the downstream net. The
(Westco Scientific Instruments, Inc., Brookfield, CT, downstream net was briefly removed, captured
U.S.A.). TDN was measured using a Shimadzu TOC shrimp were placed in a bucket with stream water,
5000 carbon analyzer (Shimadzu Corp., Columbia, andthenetwasreplaced.Thisprocesswasrepeated3–
MD, U.S.A.) connected to an Antek 720C chemilu- 5 times in each sub-reach, and captured shrimp from
minescent nitrogen detector (Antek Instruments, each run were temporarily held in separate buckets.
Houston, TX, U.S.A.; Merriam, McDowell & Currie, Allshrimpswereidentified,counted,measured(orbi-
1996). TDP was measured using the molybdate blue- talcarapacelength)withcallipers,andreturnedtothe
ascorbic acid reaction after digestion by acid-persul- stream. Total abundance was estimated using maxi-
phate oxidation (APHA, 1998). Shrimps were mum-likelihood methods (Removal Sampling 1.2,
thawed, measured (ocular carapace length, mm), PiscesConservationLtd.,U.K.),andsize-classpropor-
dried at 60 (cid:3)C for 3 days, weighed (±0.1 mg) and tions of captured shrimps were applied to boot-
ground by hand using a pestle and mortar. Ground strapped total abundance estimates. Biomass of
subsamples were subsequently analysed for per cent individuals was calculated using orbital carapace
CandNcontentonaPerkinElmerModel2400Series length-drymassregressions.Depletionsamplingwas
II CHN analyzer (Perkin Elmer, Waltham, MA, attemptedintheBisley,butshrimpabundancewastoo
U.S.A.). Per cent P content of ground subsamples lowforthismethodtobeeffective.Consequently,we
(c. 0.5 mg) was measured in 10 mL of deionized used abundance data generated from minnow-trap
water using the same methods as TDP mentioned samplingin2005(Crosset al.,2008).
earlier. Ground bovine liver (NIST 1577a; 1.11% P) Thesurfaceareaofeachsub-reachwasmeasuredto
was used as an organic P standard in all digestions. estimate shrimp abundance and biomass per square
Excretion rates of ammonium, TDN and TDP were metre. We used a bootstrap-resampling technique to
expressed as lmol shrimp)1 h)1 and plotted against approximate the true distribution and variability of
body size (dry mass, g). shrimp population abundance and biomass (Efron &
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N and P excretion by stream consumers 2051
Tibshirani, 1993). For each genus on each sampling the flashy hydrology of our study sites, we also
date, abundance data from the six sub-reaches were estimated temporal variability in NH -N turnover
4
resampled with replacement to generate 1000 esti- distance in the Prieta using our estimates of shrimp
matesofmeanabundance.Thisprocesswasrepeated densityandNH -Nexcretionrates,a3-yearrecordof
4
for each date, and the values for multiple dates were weekly discharge and ambient NH -N concentration
4
averaged to get 1000 estimates of mean annual data,andrelationshipsamongdischarge,reachdepth
abundance. From these data, we calculated a grand and width. Area was kept constant in the numerator
mean with bootstrapped 95% confidence intervals. of the equation in these long-term calculations (i.e.
We combined shrimp density data with field shrimp densities declined in proportion to increasing
measurements of excretion to calculate whole-reach discharge and reach area, but were otherwise not
estimates of nutrient excretion by the shrimp com- affected by changes in discharge). NH -N chemistry
4
munity in each stream. Whole-reach rates were and discharge data were collected from the Prieta
calculated using the allometric excretion equations weekly between February 2000 and October 2003 as
obtained in this study and by summing the propor- part of the Luquillo LTER sampling program using
tionalcontributionsof1-mm(orbitalcarapacelength) analytical techniques described earlier for NH -N.
4
size-classes for each genus. If allometric relationships
did not differ significantly between the two genera,
Nutrient-uptakeratesandlong-termnutrientchemistry
we used the same equation for both. The same
excretion equations were used in both the Prieta and Ammonium and phosphorus uptake rates were mea-
Bisley streams. Atya were present at such low densi- suredsimultaneouslyusingasingle short-termnutri-
ties in the Bisley that we included only Xiphocaris in ent release in each stream during February 2006
the whole-stream excretion calculations for that (Webster & Valett, 2006). Ammonium-N was added
stream. The Atya equation for TDP excretion rate as NH4Cl (target concentration 2.1 lMM). Phosphorus
was used in the Prieta calculation even though the was added as KH2PO4 (target concentration 1.6 lMM).
slope of the relationship was not significantly differ- Chloride was used as a conservative tracer for
ent from zero (see Results). calculation of discharge and dilution along each
To shed light on temporal variability in the contri- reach. Water samples were analysed as described
bution of shrimp excretion to ambient nutrient pools, earlier.Threecaveatsmustbeconsideredwithregard
we adopted the approach of McIntyre et al. (2008) by to the results of our nutrient releases. First, a single
calculating volumetric nutrient excretion and turn- release in each stream precludes any estimate of
overdistances.Volumetricexcretion(E ,molnutrient temporal variability in uptake kinetics. Second, the
V
per unit volume) was calculated as E = (E · enrichmentmethodweusedmayhaveoverestimated
V A
A · T)⁄V,whereE isarealexcretionrate(mol nutri- uptake lengths because of saturation of uptake
A
entm)2 h)1),Aisreacharea(length · width,m2),Tis (Mulholland et al., 2002). Third, simultaneous addi-
traveltimethrougheachreach(length⁄watervelocity, tion of nitrogen and phosphorus may have relaxed
h)andVisvolume(length · cross-sectionalarea,m3) limitation of a primarily limiting nutrient, potentially
at a given discharge. E is a useful metric because it altering demand for the other nutrient. While these
V
describestheaverageadditionofexcretednutrientsto caveats limit strong inference from our results, we
water as it flows along a given reach, assuming no chosetomakethiscomparisonofarealexcretionrates
uptake and perfect mixing (McIntyre et al., 2008). with areal uptake rates because it is the most mean-
Excretion turnover distance (m) is the distance ingfulmeasureofecosystem-levelsignificanceofcon-
required for excretion to turn over the ambient sumerexcretion.
nutrient pool completely and was calculated by
dividing ambient nutrient concentration (MM) by EV Statistical analysis
(MM)andmultiplyingbythereachlength(m)forwhich
E was calculated (100 m). We calculated volumetric Our initial approach to analysing excretion and body
V
excretion and turnover distance of NH -N, TDN and content data was to use multiple analysis of covari-
4
TDPinbothstreamsatlong-termmeandischargeand ance (MMAANNCCOOVVAA), with genus and stream as factors
ambient nutrient concentrations (see Table 1). Given and body mass as the covariate. We combined data
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2052 J. P. Benstead et al.
from the two sampling periods to simplify statistical higher than those of Atya (P < 0.0001 for all three
analyses because we were less interested in potential relationships;seeFig. 1a–c).BodycontentC:NofAtya
temporaldifferencesinallometricexcretionandbody was significantly higher than that of Xiphocaris
content relationships. Dependent variables in the (P < 0.001; Fig. 1d). Body content N:P of Xiphocaris
excretion MMAANNCCOOVVAA were excretion rates of ammo- was significantly higher than that of Atya (P < 0.016).
nium, TDN and TDP (lmol shrimp)1 h)1) and The two genera did not differ significantly with
TDN:TDP (hereafter N:P) excretion ratio. Dependent respect to body content C:P (Fig. 1f).
variables in the body content MMAANNCCOOVVAA were %C, Relationships of elemental content with body mass
%N, %P, C:N, N:P, and C:P. Preliminary analyses weresignificantonlyfor%P(Xiphocaris:P = 0.03;Atya:
showed that the genus · stream interaction term was P = 0.0006); slopes of this relationship did not differ
not significant in either the excretion or body content between the two genera (P = 0.65 for the interaction
MMAANNCCOOVVAA, so we repeated both MMAANNCCOOVVAAs without term;seeFig. 1c).RelationshipsofC:Nwithbodymass
the stream factor. MMAANNCCOOVVAA significance indicated were significant only for Atya (P = 0.01; Fig. 1d).
that one or more of the dependent variables differed Relationships of N:P with body mass were weakly
between genera (Wilks’s k, P < 0.05) and was fol- significant for Atya (P = 0.07; Fig. 1e). The overall
lowed by individual one-way analysis of covariance relationship of C:P with body mass was significant
(AANNCCOOVVAA)foreachdependentvariable,withgenusas andpositiveforbothtaxa(P < 0.0001;Fig. 1f).
the factor and body mass as the covariate. Significant
differences between slopes or intercepts were fol-
Basal resource stoichiometry
lowed by individual regressions for each genus. Per
cent data were arcsine square-root transformed and MMAANNOOVVAA results indicated thatthere were significant
all other data were log transformed to meet assump- differences in nutrient content (%C, N and P) and
tions of normality and equal variance. ratios (C:N, N:P and C:P) between resource types
Per cent C, N and P (dry mass) and nutrient ratios (epilithon and seston) and streams (Wilks’s k,
of epilithon and seston were initially analysed using P < 0.0001). Patterns between %C and %N of epili-
multiple analysis of variance (MMAANNOOVVAA) with thonandsestoninthetwostreamsweresimilar,with
resource type and stream as factors. MMAANNOOVVAA signif- significantly higher content of both elements in
icance indicated that one or more of the dependent epilithon from the Prieta (Fig. 2a,b). Per cent P of
variablesdifferedbetweenfactors(Wilks’sk,P < 0.05) epilithon was significantly higher in the Prieta, while
and was followed by individual one-way analysis of seston did not differ between the two streams
variance (AANNOOVVAA) for each dependent variable, with (Fig. 2c). No differences in C:N were found between
resource type and stream as the factors. Significant resources or streams (Fig. 2d). The two streams did
differences among factors were followed by Tukey not differ in epilithon N:P, but seston N:P was
Honestly Significant Difference (HSD) tests. Per cent significantly higher in the Prieta (Fig. 2e). Epilithon
data were arcsine square-root transformed and ratios C:P was significantly higher in the Prieta; seston N:P
were log transformed to meet assumptions of nor- did not differ between the streams (Fig. 2f).
mality and equal variance. Data for leaf litter were Differences in elemental composition of leaf litter
excluded from statistical analyses because of the low between the two streams were not analysed statisti-
number of these composite samples. cally. Per cent C, C:N and C:P of leaf litter were
c. 4 times higher than those of epilithon and seston
(Fig. 2a,d,f).PercentN,%PandN:Pofleaflitterwere
Results intermediate relative to those of epilithon and seston
in either stream.
Shrimp body content stoichiometry
MMAANNCCOOVVAA results indicated that there were signifi-
Shrimp excretion rates and ratios
cant differences in nutrient content (%C, N and P)
and ratios (C:N, N:P and C:P) with body size and Rates of NH -N and TDN excretion did not differ
4
between shrimp genera (Wilks’s k, P < 0.0001). Per between the two shrimp genera (Fig. 3a,b), although
cent C, N and P of Xiphocaris were all significantly the overall relationships with body mass were highly
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N and P excretion by stream consumers 2053
1.8 1
s) (a) (d)
s
a
m )M
% dry C:N (
y C ( 1.6 body 0.75
g bod Log
o
L
1.4 0.5
–2 –1.5 –1 –0.5 0 0.5 –2 –1.5 –1 –0.5 0 0.5
1.2 1.5
Fig.1 Relationshipsbetweenbodysize s) (b) (e)
agfRaArtnei.oacnd,mloaefi.nbrltaOiolwpedpoedoysfe,nssfecyrtlierdermescmiahalbemmweosnlsaos=ttnaie=nAldrs.sAnstiohot=nyirrncaitXohmhsciieppoopahumpssost.c,ceea(ottrsrrrnlqiiylsaeuPncieanutlgreoelendterwsgsto-=o= dy N (% dry mas 0.81 g body N:P ()M 111...234
o o
A.scabra).Onlysignificantgenus-specific g b L 1.1
regressions(P<0.05)areshown(dotted Lo
line=Xiphocaris,solidline=Atya);where 0.6 1
regressionsdidnotdiffersignificantly –2 –1.5 –1 –0.5 0 0.5 –2 –1.5 –1 –0.5 0 0.5
betweengenera,asingledashedlineis
shown:(a)%carbon;(b)%nitrogen;(c) 0.1 2.25
(c) (f)
%phosphorus[Atya,r2=0.16,log s)
body%P=)0.046(logdrymass))0.084; mas 0.05 )M
Xiphocaris,r2=0.05,logbody y 0 P (
rm%m2oaP=slas=0r).0)+c9a0,0r.0b.l7o3o5g5n](;:blo(noegid)trydmorCgyoe:lNmanrar=nassit0ti)ro.0o)2[gA80e(t.nl0yo:2agp1,]hd;or(syd-) body P (% dr ––00.0.15 Log body C: 2
phorusratio;(f)molarcarbon:phospho- g –0.15
o
rusratio[Taxacombined,r2=0.12,log L
bodyC:P=0.054(logdrymass))2.06]. –0.2 1.75
–2 –1.5 –1 –0.5 0 0.5 –2 –1.5 –1 –0.5 0 0.5
Datafromthetwostreamsdidnotdiffer
significantlyandwerecombined. Log dry mass (g)
significant(P < 0.0001forbothrelationships).Patterns When examined across both taxa, relationships
of TDP excretion between the two genera were more between excretion rates and body content stoichiom-
complex, with significant differences in both the etrywerestatisticallyhighlysignificant,buthadweak
intercept (P < 0.0001) and slope (P < 0.006) of the explanatorypower(NH -Nexcretionrateversus%N
4
relationshipwithbodymass(Fig. 3c).Relationshipsof body content, P = 0.0008, r2 = 0.07; TDN excretion
TDP excretion rate with body mass were only signif- rate versus %N body content, P = 0.0007, r2 = 0.07;
icantforXiphocaris(P < 0.0001).Xiphocarishadhigher TDPexcretionrateversus%Pbodycontent,P = 0.04,
TDP excretion rates than Atya at most body masses r2 = 0.03; data not shown). Slopes for nitrogen were
measured. Excretion N:P ratio differed significantly negative, while that for phosphorus was weakly
between the two genera (P < 0.0001) and showed positive. The relationship between excretion N:P and
contrasting patterns with body mass (Fig. 3d). Excre- body content N:P across both taxa was also weak
tion N:P increased significantly with body mass in (P = 0.06, r2 = 0.02; data not shown).
Atya (P = 0.02), while it declined in Xiphocaris
(P = 0.05). This difference in N:P excretion allometry
Whole-stream shrimp excretion estimates
was driven by relatively steeper increases in P
excretion with body mass in Xiphocaris, giving rise Mean density of Atya was 14.5 m)2 in the Prieta and
to a negative excretion N:P slope. was too low to quantify in the Bisley (see Table 2 for
(cid:2)2010BlackwellPublishingLtd,FreshwaterBiology,55,2047–2061
2054 J. P. Benstead et al.
50 60
(a) (d)
50
40
ss) 40
ma 30 )M
C (dry 20 a C:N ( 2300
% 10 b b b
10
0 0
4 80
(b) (e) a
a a,b
s) 3 60
s
ma )M b
N (dry 2 b b b N:P ( 40 b
% 1 20
Fig.2 Boxplotsoffoodresource(epili-
0 0 thon,sestonandleaflitter)stoichiometry
inthetwostudystreamsinnortheastern
0.2 1800 PuertoRico:(a)%carbon,(b)%nitrogen,
(c) (f)
a (c)%phosphorus,(d)molarcarbon:
1500 a nitrogenratio,(e)molarnitrogen:phos-
s) 0.15 phorusratio,(f)molarcarbon:phospho-
y mas 0.1 b b,c P ()M1290000 rthursoruagtiho.thTehmetiodpd,lebootfttohme,baonxdcolirnreespond
dr C: tothe75th,25th,and50thpercentile
P ( c 600 a a,b (median),respectively.Thewhiskers
% 0.05 extendfromthe10thpercentiletothe90th
percentile.Thesolidsquarerepresentsthe
300 b
arithmeticmean.Differentlettersabove
0 0 barsindicatesignificantdifferences
Prieta Bisley Prieta Bisley Prieta Bisley Prieta Bisley Prieta Bisley Prieta Bisley (P<0.05).Leaflitterwasexcludedfrom
Epilithon Seston Litter Epilithon Seston Litter statisticalanalyses.
95%confidenceintervalsderivedfrombootstrapping Table 2). Low shrimp densities in the Bisley
of density data). Atya biomass in the Prieta was resulted in extremely low whole-stream excretion
5.2 g DM m)2. Abundance and biomass of Xiphocaris estimates, for both nitrogen (0.2 lmol m)2 h)1 NH -
4
in the Prieta was 13.2 m)2 and 2.6 g DM m)2, N and 0.26 lmol m)2 h)1 TDN) and phosphorus
respectively. Abundance and biomass of Xiphocaris (0.015 lmol m)2 h)1; Table 2).
in the Bisley were more than a hundredfold lower Whole-stream shrimp excretion rates were com-
than that measured in the Prieta (0.12 m)2 and pared with whole-stream nutrient uptake measured
0.09 g DM m)2; Table 2). Combining density data, on a single date (see Table 3). In the Prieta, excretion
size-class distributions, and allometric excretion rela- rate of NH -N was equivalent to 21% of NH -N
4 4
tionships yielded whole-stream (i.e. both genera) uptake measured during the single release (Table 4).
excretion estimates of 22.3 lmol m)2 h)1 and Excretion by shrimp could potentially meet 5% of P
37.5 lmol m)2 h)1 for NH -N and TDN, respectively, demandinthePrieta.EquivalentproportionsofNH -
4 4
in the Prieta (Table 2). Whole-stream TDP excretion N and P demand excreted by shrimp in the Bisley
in the Prieta was much lower (1.1 lmol m)2 h)1; were 0.5% and <0.1%, respectively (Table 4).
(cid:2)2010BlackwellPublishingLtd,FreshwaterBiology,55,2047–2061
N and P excretion by stream consumers 2055
0.6 0
(a) (c)
–1h) 0.4 –1) –0.5
Log excretion rate –1ol NH-N shrimp 4––000...4202 Log excretion rate –1mol TDP shrimp h –1––.521
m–0.6 –2.5
(
(
–0.8 –3
–2 –1.5 –1 –0.5 0 0.5 –2 –1.5 –1 –0.5 0 0.5
0.8 3
(b) (d)
–1) 0.6 2.5
Log excretion rate –1mol TDN shrimp h–––00000.....642024 Log excretion N:P 1.512
0.5
(–0.8
–1 0
–2 –1.5 –1 –0.5 0 0.5 –2 –1.5 –1 –0.5 0 0.5
Log dry mass (g)
Fig.3 RelationshipsbetweenbodysizeandindividualnutrientexcretionratesandN:Pratiointwogeneraoffreshwatershrimps
collectedfromtwostreamsinnortheasternPuertoRico.Opendiamonds=Xiphocariselongata,filledsymbols=Atyaspp.(squares=
A.lanipes,circles=A.innocous,triangles=A.scabra).Onlysignificantgenus-specificregressions(P<0.05)areshown(dottedline=
Xiphocaris,solidline=Atya);whereregressionsdidnotdiffersignificantlybetweengenera,asingledashedlineisshown:(a)NH-N
4
excretion[Taxacombined,r2=0.66,logNH-Nexcretionrate=0.62(logdrymass)+0.31];(b)totaldissolvednitrogenexcretion[Taxa
4
combined,r2=0.39,logTDNexcretionrate=0.36(logdrymass)+0.39];(c)totaldissolvedphosphorusexcretion[Xiphocaris,r2=0.20,
logTDPexcretionrate=0.62(logdrymass))0.82];(d)molartotaldissolvednitrogen:totaldissolvedphosphorusratio[Atya,
r2=0.08,logexcretionN:P=0.25(logdrymass)+1.82;Xiphocaris,r2=0.04,logexcretionN:P=)0.30(logdrymass))1.19].Data
fromthetwostreamsdidnotdiffersignificantlyandwerecombined.
Volumetric excretion of NH -N, TDN and TDP in
4 Discussion
the100-mreachofthePrietaamountedto63,106and
3 nMM, respectively (see Table 4 for 95% confidence The relative magnitude and ecosystem-level signifi-
intervalsderivedfrombootstrappingofdensitydata). canceofconsumerexcretiondependonacombination
Equivalent estimates for the low-shrimp Bisley were ofrelativelywell-understoodbioticandabioticfactors
1,1and0 nMM forNH4-N,TDNandTDP,respectively (Schauset al.,1997;Vanniet al.,2002;Hallet al.,2007;
(Table 4). Combined with ambient nutrient concen- McIntyre et al., 2008). These factors include those
trations,thesevolumetricexcretionestimatesresulted related to supply rate from consumers (i.e. biomass,
in excretion turnover distances in the Prieta of 786 m consumer elemental demandanddiet stoichiometry),
for NH -N and c. 9 km for TDN and TDP (Table 4). those related to total pools and turnover of elements
4
Excretionturnoverdistanceswere>20 kmforallthree (i.e. habitat volume, turnover rate and the ambient
nutrientsintheBisley.Long-termmodellingrevealed concentration of limiting nutrients) and those related
considerable variability in the distance required for tonutrientsinks(i.e.biomass,activityandstoichiom-
shrimp excretion to turn over the ambient NH -N etryofmicrobesandprimaryproducers).Therelative
4
pool in the Prieta (Fig. 4a; range 12–8740 m, mean contributions of different factors in controlling the
661 m).Thisvariabilitywasdrivenbylargerangesin potential significance of excretion have rarely been
both discharge and ambient NH -N concentration. studied, however (but see McIntyre et al., 2008). We
4
Mostcalculateddistancesfellbetween200and600 m used measurements of shrimp excretion rates, densi-
(Fig. 4b). ties, and long-term records of discharge and nutrient
(cid:2)2010BlackwellPublishingLtd,FreshwaterBiology,55,2047–2061
2056 J. P. Benstead et al.
Table2 DensitiesofAtyaandXiphocaris
Variable Prieta Bisley
shrimpsandwhole-streamnutrient
excretionestimatesforthePrietaand
Shrimpabundance
Bisleystreams,LuquilloExperimental
Atya
Abundance(m)2) 14.5(7.0–22.8) – Forest,PuertoRico.Abundanceswere
Biomass(gDMm)2) 5.2(2.5–8.3) – estimatedinFebruaryandAugust2005.
ExcretionwasmeasuredinMarchand
Xiphocaris
Abundance(m)2) 13.2(8.8–18.0) 0.12(0.02–0.23) November–December2004.Valuesare
Biomass(gDMm)2) 2.6(1.7–3.6) 0.09(0.01–0.17) meanswith95%confidenceintervals
basedonbootstrappingofabundance
Whole-streamshrimpexcretion
estimates
Atya
NH-Nexcretion(lmolm)2h)1) 12.8(6.2–20.2) –
4
TDNexcretion(lmolm)2h)1) 20.0(9.6–31.4) –
TDPexcretion(lmolm)2h)1) 0.40(0.20–0.64) –
Xiphocaris
NH-Nexcretion(lmolm)2h)1) 9.5(6.3–12.9) 0.20(0.03–0.38)
4
TDNexcretion(lmolm)2h)1) 17.5(11.7–23.9) 0.26(0.04–0.49)
TDPexcretion(lmolm)2h)1) 0.71(0.47–0.96) 0.015(0.002–0.028)
Totalexcretion
NH-Nexcretion(lmolm)2h)1) 22.3(12.5–33.1) 0.20(0.03–0.38)
4
TDNexcretion(lmolm)2h)1) 37.5(21.3–55.3) 0.26(0.04–0.49)
TDPexcretion(lmolm)2h)1) 1.1(0.7–1.6) 0.015(0.002–0.028)
TDN,totaldissolvednitrogen;TDP,totaldissolvedphosphorus.
Table3 Dischargevaluesanduptake
Variable Prieta Bisley
parametersforNH-NandPduringthe
4
Discharge(Ls)1) 26 25 short-termreleasesconductedduring
February2006inthePrietaandBisley
NH-N
4
streams,LuquilloExperimentalForest,
Ambientconcentration(lMM) 0.24 0.18
PuertoRico.Errorestimatesforuptake
Uptakelength(m) 79(63–104) 141(133–150)
Uptakerate(lmolm)2h)1) 105.3(80.0–132.0) 39.3(36.9–41.7) parameters(inparentheses)arederived
Uptakevelocity(·10)4ms)1) 1.24(0.94–1.56) 0.61(0.58–0.65) fromthestandarderrorfortheslopeof
dilution-correctednutrientconcentration
SRP
regressedagainstdistance
Ambientconcentration(lMM) 0.18 0.37
Uptakelength(m) 270(157–959) 417(286–767)
Uptakerate(lmolm)2h)1) 23.7(6.7–40.7) 27.9(15.2–40.7)
Uptakevelocity(·10)4ms)1) 0.36(0.10–0.63) 0.21(0.11–0.30)
concentration to estimate spatial and temporal vari- tions, which affected the magnitude of nutrients
ability in the relative magnitude of excretion by excreted by shrimps relative to the ambient pool.
tropical freshwater shrimps. Our results demonstrate
the combined effects of biotic and abiotic factors in
Stoichiometry of shrimp body content and excretion
controlling the significance of consumer excretion for
nutrient cycling in aquatic ecosystems. Body content Growth rate may drive some of the differences we
stoichiometry affected excretion rates and ratios of observed in body content stoichiometry (e.g. %P),
shrimpsonlyweakly.Differencesincommunity-level both between the two shrimp genera and with
excretionwererelatedtovariationinshrimpbiomass increasing body mass. Growth rate and P associated
between streams, dictated by stream geomorphology with RNA are expected to decline with increasing
and the resulting presence of predatory fishes. Tem- body mass (Elser et al., 2003). Moreover, Xiphocaris
poral variability in the contribution of shrimp excre- exhibits faster growth rates than Atya, at least at
tiontoambientnutrientpoolswasdrivenbytemporal smaller body sizes (Cross et al., 2008), which may
patterns in stream discharge and nutrient concentra- partly explain its higher per cent P body content.
(cid:2)2010BlackwellPublishingLtd,FreshwaterBiology,55,2047–2061