Leaf quality influences invertebrate colonizationand drift in a temperate rainforest stream

Liliana García, John S. Richardson, and Isabel Pardo

Abstract: Changes in riparian forest composition and diversity, such as plantations of exotic species, may alter resourcequality, detritivore assemblages, and litter breakdown rates in streams. We hypothesized that different litter resources may in-fluence colonization and drift of invertebrates inhabiting small, temperate rainforest streams in southwestern British Colum-bia, Canada. Leaves of different quality and origin were incubated in stream-side channels to test this hypothesis. Thesequence of leaf decomposition rates was as follows: alder > alder + cedar > cedar ≥ eucalyptus. Cedar litter decayed fasterwhen mixed with alder than when alone. Invertebrates colonizing leaf bags were predominantly collector–gatherers andshredders, particularly on alder leaves. Drift density varied over the incubation period and seemed to be controlled by leafquality, since there were more individuals drifting from channels with alder leaves than from channels with cedar or euca-lyptus. However, we observed different species-specific invertebrate responses controlled by leaf traits, particularly by nu-merically dominant chironomid species. Indeed, invertebrate drift from channels incubated with alder bags was mostly dueto pupation and emergence of orthoclad midges, whereas this was not observed in the other channels. This differential re-sponse in colonization and drift has the potential to modify the transfer rates of organic matter to higher trophic levels andthus ecosystem functioning.

Résumé : Des changements dans la composition et la diversité des forêts riveraines, comme la plantation d’espèces exoti-ques, peuvent modifier la qualité des ressources, les assemblages de détritivores et le taux de décomposition de la litièredans les cours d’eau. Nous avons postulé que différentes ressources de litière pourraient influencer la colonisation et la dé-rive d’invertébrés habitant de petits cours d’eau de forêts humides tempérées dans le sud-ouest de la Colombie-Britannique(Canada). Des feuilles de qualités et d’origines différentes ont été incubées dans des chenaux au fil de l’eau afin de vérifiercette hypothèse. La séquence des taux de décomposition des feuilles, en ordre décroissant, était la suivante : aulne > aulne +thuya > thuya ≥ eucalyptus. La litière de thuya se décomposait plus rapidement quand elle était mélangée avec de la litièred’aulne que par elle-même. Les invertébrés qui colonisaient les sacs de feuilles étaient principalement des collecteurs–cueilleurs et des déchiqueteurs, en particulier sur les feuilles d’aulne. La densité des invertébrés dans le matériel en dérivevariait selon la période d’incubation et semblait être contrôlée par la qualité des feuilles puisqu’il y avait plus d’individusdérivant de chenaux contenant des feuilles d’aulnes que de chenaux contenant des feuilles de thuya ou d’eucalyptus. Nousavons toutefois observé différentes réponses pour des espèces d’invertébrés données selon les caractères des feuilles, en par-ticulier chez les espèces de chironomidés, les invertébrés les plus nombreux. En effet, la dérive de chenaux où étaient incu-bés des sacs de feuilles d’aulne était principalement due à la pupaison et à l’émergence d’orthocladinés, un phénomène nonobservé dans les autres chenaux. Ces différentes réponses sur le plan de la colonisation et de la dérive pourraient modifierles taux de transfert de matière organique vers des niveaux trophiques plus élevés et ainsi la dynamique des écosystèmes.

[Traduit par la Rédaction]

IntroductionFactors controlling the productivity and biodiversity of

ecosystems are an important focus in ecology, and heterotro-phic headwater streams dependent on particulate detritus areexcellent systems for examining these processes because ofstrong terrestrial–aquatic linkages (Hynes 1975; Cummins et

al. 1989; Wallace et al. 1999). Changes in riparian forestcomposition and diversity have the potential to strongly alterdecomposer assemblages (Bärlocher and Graça 2002), litterbreakdown rates (Swan and Palmer 2004; Lecerf et al.2005), resource quality for consumers in streams (Graça etal. 2002; Kominoski et al. 2011), and stream productivity(Swan and Palmer 2006). Hence, the quality and quantity ofresources available in ecosystems are key factors that deter-mine the spatial and temporal distribution of organisms andrates of consumer-mediated ecosystem processes.Increasing domination of ecosystems by humans is pro-

moting changes in riparian-zone vegetation composition. Asa result, there has been extensive research on the consequen-ces of biodiversity losses on stream ecosystem structure andfunctioning (Loreau et al. 2002; Gessner et al. 2004; Giller etal. 2004). In particular, Eucalyptus plantations are a commonanthropogenic disturbance affecting riparian forest composi-tion in many parts of the world (Graça et al. 2002). Usuallystudies investigating the consequences of these changes are

Received 22 December 2011. Accepted 18 July 2012. Publishedat www.nrcresearchpress.com/cjfas on 27 September 2012.J2011-0527

L. García and I. Pardo. University of Vigo, Department ofEcology and Animal Biology, 30310 As Lagoas-Marcosende,Vigo, Spain.J.S. Richardson. The University of British Columbia,Department of Forest Sciences, 3041 – 2424 Main Mall,Vancouver, BC V6T 1Z4, Canada.

Corresponding author: Liliana García(e-mail: lilizar@uvigo.es).

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Can. J. Fish. Aquat. Sci. 69: 1663–1673 (2012) doi:10.1139/F2012-090 Published by NRC Research Press

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made in places already altered or manipulated, so it is poten-tially confounded by effects caused by previous adaptation.Coastal, temperate rainforest streams have no prior exposureto Eucalyptus plantations. However, studies in the Pacificcoastal ecoregion (Richardson 1991) and in the west coast ofEurope (García and Pardo 2012) have found similar congene-ric species among the dominant invertebrate species inhabit-ing leaves, suggesting the potential for direct comparisonsusing exotic leaf species. Therefore, we assume that we areable to test quality effects without any previous adaptationby consumers.The seasonal input of terrestrial litter supply to small, for-

ested streams results in leaf accumulations made up of a mix-ture of leaves. The quantity and timing of resource inputsinfluence food web dynamics and stream productivity (Ri-chardson 1991; Wallace et al. 1999; Richardson et al. 2010).These mixtures of leaves can present a suite of both positive(i.e., nutrients) and negative (i.e., secondary compounds) fac-tors that drive consumer feeding preferences and performan-ces (Swan and Palmer 2006). Although leaf quality effectshave often been studied for a single leaf species, recent stud-ies have demonstrated that mixtures of leaves have the poten-tial to strongly affect decomposition dynamics andinvertebrate composition inhabiting resources patches (Komi-noski and Pringle 2009; Sanpera-Calbet et al. 2009). Conse-quently, the understanding of effects of mixtures of resourcespecies have become a key set of questions in communityecology, with further implications for nutrient cycling andecosystem productivity (Guenet et al. 2010).At the community level, many environmental factors and

ecological interactions influence the assemblage of co-occurring species (Power et al. 1988; Allan 1995; Polis et al.1997). Consumers move actively among leaf packs by driftand other movements, and they can subsequently colonizeother leaf packs depending on local physical and biologicalconditions (Minshall and Petersen 1985; Rowe and Richard-son 2001; Downes et al. 2011). Experimental manipulationsof litter quantity in stream channels have demonstrated thatconsumers can track litter resource patches, resulting in ag-gregation of individuals and acceleration of leaf decomposi-tion (Richardson 1991; Rowe and Richardson 2001; Tiegs etal. 2008). In addition, recent studies have suggested that lifehistory traits, competition, and resource availability, individu-ally or in combination, can drive invertebrate responses to se-lect food resources (Silver et al. 2004; LeRoy and Marks2006). By understanding those factors that control commun-ity structure and its coupling to resource dynamics, we candetermine limits on ecosystem productivity and biotic diver-sity (e.g., Dyer and Letourneau 2003).In the present study, we assume that leaf litter quality, in

combination with quantity, is a limiting factor for invertebratepopulations. Our main objective was to assess invertebrate re-sponses to different leaf litter inputs in experimental channelsand evaluate how the interaction between biotic and abioticforces influences detritivore colonization and drift. We ma-nipulated terrestrial litter quality in replicated stream-sidechannels using two native species (red alder (Alnus rubra),western red cedar (Thuja plicata)) and one exotic (Eucalyptusglobulus) as single species leaf bags and one mixture of thetwo native species to assess our objectives. Since many stud-ies have tested the influence of leaf litter quality and diver-

sity on leaf decomposition rates, and invertebrates (mostlyshredders) prefer high-quality food items, we expect that in-vertebrate dynamics will be also influenced by leaf litterquality, and thus emigration from the channels with high-quality leaves will be lower than from the others.

Materials and methods

Site descriptionThis study was carried out in the Mayfly Creek experi-

mental channels in The University of British Columbia’sMalcolm Knapp Research Forest (MKRF), near MapleRidge, British Columbia, Canada (49°16′N, 122°34′W). Theclimate is wet-temperate with mild summers, wet, cool win-ters, and annual precipitation around 2200 mm, mostly asrain (Kiffney et al. 2004). Mayfly Creek flows through asteep and narrow valley in a mostly coniferous forest, withdeciduous trees along the riparian area. The watershed lies inthe Coastal Western Hemlock forest, and the conifers Tsugaheterophylla (western hemlock), Thuja plicata (western redcedar), and Pseudotsuga menziesii (Douglas-fir) are the dom-inant forest species. The major riparian tree species were Al-nus rubra (red alder) and Acer circinatum (vine maple),together with the shrub Rubus spectabilis (salmonberry),based on litterfall estimates (Richardson 1992). Mayfly Creekis a second-order stream with a bankfull width of ≈3 m, aslope of 0.08, and at an altitude of 315 m. Mean daily watertemperature in the channels during the study period was12 °C. The stream is generally shaded by riparian vegetationso that stream temperatures vary at most 3 °C daily (Richard-son 1992). Physico-chemical characteristics and hydromor-phological variables are similar to other streams in theMKRF (e.g., Kiffney et al. 2003).

Experimental channelsWe built experimental channels in the lower reach of exist-

ing channels, which mimicked forest headwater streams inthe coastal range of the Pacific coastal rainforest in BritishColumbia, Canada (for further details, see Richardson 1991).A total of 16 experimental channels (each 1.5 m × 0.15 m,with area of 0.225 m2 and slope of 3%; Fig. 1) were usedfor this experiment. Channels were sealed with several layersof plastic sheets to remain watertight, and the top was cov-ered with plastic net to avoid litter inputs from the surround-ing forest. The substrate was 3–4 cm diameter rounded gravelplaced to a depth of 10 cm in each channel with intersticesmostly filled with sand (<5 mm diameter). The arrangementof experimental channels allowed for invertebrate access andleaf colonization. Discharge estimates ranged from 0.17 to0.42 L·s–1 through each channel (three replicates per channeltaken one per collection date), but there were no significantdifferences among channels (one-way analysis of variance(ANOVA), p > 0.05). Water temperature (mean 12 °C, range9.8 to 14.1 °C) was continuously recorded with data-loggers.Experimental streams were flushed using a portable pump toreduce the residual coarse detritus and to allow the coloniza-tion in channels 2 weeks prior to the beginning of the experi-ment.

Leaf bags and drift netsA litter-bag approach was used to determine decomposi-

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tion rates and invertebrate dynamics. Leaf bags were con-structed using plastic net with 10 mm mesh as a frame (tocreate a volume for the leaves) surrounded with 1 mm meshsize with 10 holes of 1.5 cm (Fig. 1b) to allow access for thelargest invertebrates inhabiting the channels to the leaveswhile retaining small leaves such as cedar. Three differentleaf types (alder (Alnus rubra), cedar (Thuja plicata) and eu-calyptus (Eucalyptus globulus)), plus a mixture of alder–cedar were randomly assigned to channels under base-flowconditions in the experimental channels from 25 June to 18September 2007. Each leaf bag had 4 g total litter in all treat-ments, with the mixed-species treatment in equal proportionby mass (2 g of each leaf type). Leaves were selected accord-ing to different aspects; red alder and cedar (native species)were selected because of its dominance in the area, and theexotic eucalyptus tree was chosen because it is a completelyexotic species in this area, despite its high use in plantationforestry in several parts of the world, and thus consumerscannot have had any previous evolutionary experience withit. The three leaf types differ in structure and chemical com-position (Canhoto and Graça 1995, 1999; Richardson et al.2004). The collection of leaves occurred after abscission andwere captured on plastic nets below trees in the MKRF, pre-vious to the experiment, or from northwest Spain (in the caseof eucalyptus leaves), and transported to the laboratory, air-dried, and weighed into batches of 4.00 ± 0.01 g. Afterweighing, each batch was remoistened to render leaves plia-ble, and the leaves were placed in mesh bags and stored for24 h at room temperature.The experimental setup resulted in a complete block de-

sign in which each channel was an independent replicate,with only one leaf type per channel (see Fig. 1). A total of192 leaf bags were constructed for the experiment (i.e., in-cluding 16 control bags). Initially, 96 leaf bags (4 leaf types ×4 replicate channels × 6 dates) and control bags were ex-posed in channels. Control bags were used to correct for hu-midity and handling. The remaining 80 leaf bags (4 leaftypes × 4 replicate channels × 5 dates) were added as extrabags to avoid the complete elimination of food by replace-ment, only to provide food resources, and were not includedas part of the decomposition experiment. Collections of leafbags from the channels were at 0, 7, 14, 28, 42, and

56 days. One leaf bag was randomly removed from eachchannel on each sampling date and immediately sealed andlabelled in plastic ziplock bags. Then, samples were kept onice for transport prior to further processing in the laboratory.Drift rates were measured with one drift net (100 µm

mesh) per channel installed on the channel outflow pipe (theentire flow could be filtered; see Fig. 1c). One drift net perchannel was placed for the 24 h period immediately prior tocollection of leaf bags to avoid confounding effects due tothe collection and replacement of bags. Later, drift nets werecollected at each collection time, and invertebrates were pre-served in 70% ethanol until their analysis in the laboratory.Drift density was estimated as number of invertebrates drift-ing per 100 m3 of stream water (Hauer and Lamberti 1996).

Laboratory procedureOnce in the laboratory, leaves were carefully removed from

bags and individually rinsed with water onto a 100 µm meshsieve to remove the adhering detritus and to separate inverte-brates from leaves. Invertebrates (removed by hand sorting)were sorted in a white enamel pan containing water and pre-served in 70% ethanol. Leaf litter was oven-dried at 55 °C(until constant mass) and weighed to the nearest 0.01 g.These procedures were completed within 24 h after each col-lection time. Subsamples (10% of each sample) were ashed at550 °C for 1 h to estimate ash-free dry mass (AFDM). Afterweighing, leaves were stored for further stoichiometric analy-sis at the University of Vigo (Vigo, Spain).Invertebrates were identified to the lowest practical taxo-

nomic level under a stereomicroscope (Nikon SMZ645 at5×) and a microscope (Olympus U-TV1X at 40×), counted,and assigned to functional feeding groups (Merritt et al.2008).

Stoichiometric analysis of leaf litterDried leaf samples were ground and homogenized using a

ball mill (Retsch MM 200). For C and N analysis, sampleswere weighed in tin capsules to the nearest 1 µg (Mettler Tol-edo AB104 balance, Switzerland) and analyzed with a CarloErba EA 1108 CHN analyser (Fisons Instruments, Milan,Italy). For P analysis, samples were weighed, acid-washed,

Fig. 1. Experimental channels constructed near Mayfly Creek to carry out the experiment. Panels show pictures of different parts of channelsfrom the top to the bottom of the channels: (a) mixing box that allows the complete mixing of the water, (b) leaf bag constructed usingdifferent mesh sizes (10 mm mesh to create a fixed structure and 1 mm mesh as a cover) and with five holes of 1.5 cm to allow the coloni-zation of larger macroinvertebrates, and (c) lower part of channels with one outflow pipe per channel, which allows the attachment of driftnets when necessary.

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and pre-ashed in ceramic crucibles and ashed at 550 °C.Then, leaves were acid-digested (69% HNO3) in a LT100microdigestor at 140 °C until evaporation (Thermostat DRLange) and removed with 2% HNO3 for subsequent determi-nation by atomic absorption (ICP-OES Optima 4300 DV,USA). All data were presented as either %C, %N, and %P ofdry mass or as molar ratios.

Data analyses

Leaf processing and nutrient contentRemaining leaf dry mass was calculated as the ratio be-

tween final and initial dry mass (after correcting for humidityand handling) and expressed as a percentage. Leaf decompo-sition rates were calculated as the rate coefficient (k) by re-gressing the natural logarithm of remaining leaf AFDM (%)against time in the channels (days). Analysis of covariance(ANCOVA) with time as a covariate (but not includingtime 0) was used to test for differences in breakdown ratesamong four leaf types (alder, cedar, mixed, and eucalyptus),and subsequent pairwise comparisons were performed withTukey’s test. Expected mass remaining for mixed-speciesbags was calculated as the average of individual species littermass remaining from single-species leaf bags and checked fordifferences between single and mixed treatments with one-way ANCOVAs.Leaves belonging to the mixed treatment were treated inde-

pendently (i.e., five treatments) to evaluate nutrient contents.We used analysis of variance (ANOVA) followed by Tukey’stests to examine differences of chemical properties amongleaf treatments at the beginning (t0) and the end (t56) of theexperiment. We tested for normality using the Shapiro–Wilktest, and square-root transformation was used to meet the as-sumption of homogeneity of variances. Linear regressionswere used to determine if there was a relationship betweendecomposition rates and leaf nutrient contents or invertebratedensities (i.e., colonizing and drifting from leaves).

Invertebrate colonization and driftDensities of invertebrates colonizing the leaf bags and

numbers drifting from the channels were analyzed using anal-ysis of variance (ANOVA, SPSS ver. 16.0, SPSS Inc., Chi-cago, Illinois, USA). The ANOVA model included twofactors: leaf type (four levels, fixed factor) and time (five lev-els, not including time 0, random factor). When significantdifferences among the main factors or their interactions werefound, Tukey’s tests were used for post hoc comparisons.Data were log(x + 1)-transformed when necessary to removeheteroscedasticity (Underwood 1997). Later, invertebrate data(colonization and drift) were analyzed with multivariate anal-ysis using the PRIMER software package (Clarke and Gorley2006) to understand how the assemblage differed amongtreatments. A SIMPER analysis (similarity percentage) wascarried out with all taxa collected in samples to estimate thedegree of similarity among leaf types and to estimate the in-dividual contribution and the importance of each taxon to theglobal similarity. This analysis was based on the Bray–Curtissimilarity index, which combines information on the speciesconcentration and faithfulness of the occurrence of speciesabundances in particular groups. Finally, simple linear regres-sions were used to determine if there was a relationship be-

tween colonization and drift densities. To better understandthese relationships, total densities were also partitioned intotwo components, such as mature specimens (i.e., pupae andadults) and larvae.

Results

Leaf processing and nutrient dynamicsDecomposition rates were calculated as the slope of the

negative exponential model (Table 1). Decomposition ratewas significantly affected by the leaf type and time interac-tion (F[3,72] = 122.9, p < 0.001), indicating that alder leavesdecomposed more rapidly than the other three leaf types (Ta-ble 1; Fig. 2a). Significant differences were found among allleaf treatments, except between cedar and eucalyptus leaves(p > 0.05). Alder and mixed leaves were classified as fast de-composing (k > 0.01; Petersen and Cummins 1974) and lost50% of their initial leaf mass in less than 20 days (Fig. 2a).However, cedar leaves were classified as medium and euca-lyptus as slow (Table 1), though they were not significantlydifferent. At the end of the 56-day incubation period, theamount of mass loss differed significantly among leaf spe-cies. Alder leaves lost 89.4% and mixed leaves lost 67.7% ofthe initial leaf litter, while cedar lost 33.6% and eucalyptusonly 18.1%. When we compared litter AFDM remainingfrom single versus mixed bags, we did not observe signifi-cant differences between alder or cedar treatments (one-wayANCOVAs, both with p > 0.05). However, deviations ofleaf mass remaining in the mixed bags compared with thatpredicted from the single-species bags indicates a trend tofaster decomposition, at least for cedar, when in mixed bags(Fig. 2b).Initially, alder leaves had a higher nutrient content than ce-

dar and eucalyptus leaves, and N and P concentration variedstrongly over the incubation time (Table 2; Fig. 3). Despiteinitial similarities between alder treatments, those alder leavesincluded in the mixed treatment showed faster losses thansingle leaves (Fig. 3). In cedar and eucalyptus leaves,changes in P content through time were slight, but in alderleaves P decreased in a continuous way. Interestingly, P of al-der leaves and cedar leaves decreased faster when included inthe mixed than in the single treatment (Fig. 3).Leaf decomposition rates were positively related to the

number of invertebrates colonizing leaf bags (adjusted R2 =0.35, F[1,98] = 54.5, p < 0.001), N content of leaves was pos-itively related to the invertebrate density (adjusted R2 = 0.11,F[1,98] = 13.1, p < 0.001), and P content of leaves was alsopositively related to the invertebrate density (adjusted R2 =0.18, F[1,98] = 22.6, p < 0.001). There were no significant re-

Table 1. Mean values of the decomposition coefficient (k, day–1)derived from an exponential decay model using days per unit time.

Leaf type k R2 pAlder 0.044a 0.93 <0.001Mixed 0.020b 0.88 <0.001Cedar 0.007c 0.86 <0.001Eucalyptus 0.003c 0.77 <0.001

Note: Coefficient of determination (R2) and significance for model fitare also shown (n = 20). Letters denote significant differences among de-composition rates.

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lationships between decomposition rates or nutrient contentswith invertebrate drift density (p > 0.05).

Colonization of invertebratesLeaf bags were colonized by 63 taxa, although only nine

taxa contributed more than 0.1% each to the total abundance(Table 3). SIMPER analysis indicated that the invertebrate as-semblage colonizing leaf bags showed approximately 70%average similarity between leaf types and slightly higher sim-ilarity within leaf types (Table 4), and these results weremostly determined by the abundance of the numerically dom-inant taxa. However, the assemblage of invertebrates inhabit-ing alder bags (both single and mixed) showed significantdifferences from that inhabiting cedar or eucalyptus leaves(one-way ANOSIM, p < 0.01; Table 4).

Fig. 2. Decomposition of different leaf types in experimental chan-nels over 56 days. (a) Percentage of the leaf litter ash-free dry mass(AFDM) remaining is shown for four treatments (mean ± standarderror (SE), n = 4). Symbols represent different leaf types: alder (so-lid circles), a 50:50 mixture of alder and cedar (open circles), cedar(solid triangles), and eucalyptus (solid squares), and lines are regres-sion lines based on the negative exponential model. (b) Observedlitter AFDM remaining (%) in single vs. mixed leaf bags, with thedashed line representing the 1:1 relation. Alder leaves are repre-sented by circles and cedar leaves by triangles.

Fig. 3. Nutrient dynamics of carbon (C), nitrogen (N), and phos-phorus (P) of each leaf type along the incubation period (mean ± SE,n = 4). Nutrient concentration is expressed as milligrams of C, N,and P per gram of litter ash-free dry mass (AFDM). Symbols repre-sent different leaf types: alder (solid circles), alder mixed (open cir-cles), cedar (solid triangles), cedar mixed (open triangles), andeucalyptus (solid squares).

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Although the invertebrate composition showed strong sim-ilarity, the total density of individuals that had colonized leafbags varied significantly because of leaf type (F[3,60] = 54.95,p < 0.01) and incubation time (F[4,60] = 14.95, p < 0.01), butthere was no interaction between main factors (F[12,60] =1.71, p > 0.05). There were more individuals colonizing sin-gle alder leaves than other leaf types (Table 3; Fig. 4). Themixed treatment was also colonized by many invertebrates,and it differed significantly from those observed in cedar oreucalyptus leaves. Maximum densities were observed atday 28 in those channels supplied with alder leaves (singleand mixed). Maximum densities per unit AFDM on alderleaf bags were reached on day 28, after which densities werereduced to 36% of maximum by day 56 (Fig. 4). Neverthe-less, eucalyptus and cedar were less colonized than otherleaves, and maximum density values were found at the endof the incubation period. In general, mixed leaf bags werecolonized by half the number of invertebrates that colonizedalder leaves over the incubation period (52.5% on mixedleaves vs. 100% on alder leaves), while cedar and eucalyptusleaf bags were colonized by approximately a quarter of theinvertebrates that colonized alder leaves (25.2% and 20.0%,respectively). Alder leaves seemed to be the preferred foodresource.Invertebrate assemblages colonizing leaf bags were repre-

sented by different functional feeding groups (Table 3).Collector–gatherers and shredders were the most dominantgroups in all leaf types, although collector–filterers and pred-ators were also present. When each leaf type was observedindependently, at time of maximum colonization, a more pre-

cise pattern could be discerned (Fig. 5). Indeed, alder andmixed bags were colonized mostly by shredders andcollector–gatherers (Table 3). However, leaf bags constructedwith cedar and eucalyptus leaves had a high abundance ofcollector–gatherers (and also more predators and collector–filterers), but fewer shredders than alder leaf bags. Brillia re-tifinis and Corynoneura spp. (both Orthocladiinae chirono-mids, but from different functional feeding groups) colonizedall leaf bags at higher densities than other species. Za-pada spp. (Plecoptera) and Lepidostoma spp. (Trichoptera)were the most abundant shredders, aside from B. retifinis,colonizing leaf bags during the incubation period, mostly inalder leaves (Table 3). Although these shredders appeared inlower abundance than other species, they may represent aproportionally higher biomass.

Table 2. Nutrient content of leaves (mean ± 1 SE, n = 4), expressed as percentages (carbon (C), nitrogen (N), and phosphorus (P)), at thestart (t0) and end (t56) of the incubation period.

%C %N %P

Leaf type Treatment t0 t56 t0 t56 t0 t56Alder Single 48.3±0.3a 48.0±0.2a 2.1±0.1a 1.8±0.1d 0.09±0.01a 0.04±0.0c

Mixed 48.3±0.3a 48.5±0.1a 2.1±0.1a 1.8±0.1d 0.09±0.01a 0.01±0.0bCedar Single 49.8±0.1a 51.5±0.1b 1.0±0.1b 1.1±0.1b 0.05±0.02ab 0.07±0.0ab

Mixed 49.8±0.1a 50.9±0.2b 1.0±0.1b 1.1±0.1b 0.05±0.02ab 0.07±0.01abEucalyptus Single 52.3±0.8b 54.1±0.2c 0.6±0.0c 0.8±0.1e 0.02±0.0b 0.02±0.0b

Note: Leaf types: alder, mixed alder, cedar, mixed cedar, and eucalyptus. Different letters represent significant mean differences among leaf treatments(p < 0.05).

Table 3. Density of invertebrates colonizing leaf bags (mean number of animals per gram of leaf ash-free dry mass ± 1 SE) over the in-cubation period within each leaf type (n = 20, resulting from 4 replicates × 5 collection times).

Taxon name Functional groupFrequency(%) Alder Mixed Cedar Eucalyptus

Chironomidae Corynoneura spp. Collector 36.06 215.55±15.52a 121.30±14.29b 91.32±13.23b 70.09±5.78bChironomidae Brillia retifinis Shredder 27.43 359.38±77.92a 170.70±29.85b 64.23±15.15c 39.34±6.71cChironomidae Orthocladiinae* Collector 4.22 34.28±7.68a 19.62±6.76a 15.94±4.64a 10.32±2.11aChironomidae Tanypodinae Predator 2.67 31.52±10.66a 9.64±2.45b 8.52±2.98b 6.46±1.93bNaididae Naididae Collector 1.90 14.17±5.76a 7.56±3.12a 9.31±6.00a 7.50±3.60aChironomidae Tanytarsini Collector–filterer 1.56 14.07±4.81a 7.42±2.65ab 4.98±1.50ab 3.58±0.96bChironomidae Chironomini Collector 1.12 11.21±3.85a 5.21±1.94a 3.38±1.14a 2.87±0.90aNemouridae Zapada spp. Shredder 0.60 7.19±2.01a 2.10±0.70b 1.53±0.49b 0.99±0.30bLepidostomatidae Lepidostoma spp. Shredder 0.23 5.30±2.81a 0.35±0.24b 0.48±0.22b 0.35±0.21b

Note: The taxa order is based on frequency and expressed as a percentage of the total abundance. Functional feeding groups are also included. Note thatthe table shows only those taxa that contributed more than 0.1% to the total abundance. Letters represent significant mean differences among leaf treatments(p < 0.05).*Not including larvae of Brillia or Corynoneura species.

Table 4. Comparison of the invertebrate assemblage between leaftypes.

Alder Mixed Cedar EucalyptusAlder 78.85% 0.065 0.633* 0.650*Mixed 74.40% 72.75% 0.335* 0.294*Cedar 69.28% 71.36% 77.59% 0.150Eucalyptus 67.41% 70.06% 77.47% 74.70%

Note: SIMPER results are shown in the table as percentages of averagesimilarity (%) along and below the diagonal. The R values resulting fromthe ANOSIM analysis are shown above the diagonal in bold letters, andsignificant differences between leaves (p < 0.01) are indicated with anasterisk (*).

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Drift densityInvertebrates collected in drift nets were also diverse,

although only 10 taxa showed abundances higher than 1% ofthe total numbers. The assemblage of invertebrates driftingfrom channels showed no significant differences betweenleaf types (one-way analysis of similarity (ANOSIM), p >0.05). In general, the chironomid subfamily Orthocladiinaewas the most abundant taxa group drifting from the channels,mostly B. retifinis (average contribution 24.7%) and Coryno-neura spp. (average contribution 21.5%). Moreover, there wasa strong contribution (31.5%) of orthoclad midges drifting asmature individuals (i.e., pupae and adults). Other taxa suchas Baetis spp. also contributed to the average similarityamong leaf types (average contribution 8.5%). In general, to-tal density of individuals drifting from the channels variedsignificantly by leaf type (F[3,60] = 3.22, p < 0.05) and incu-bation time (F[4,60] = 2.64, p < 0.05), without a significantinteraction effect (F[12,60] = 0.59, p = 0.84). There was ahigher number of individuals drifting from channels with al-der leaves (≈30% in single and mixed bags) than from chan-nels with cedar (22.3%) or eucalyptus leaves (19.5%).However, when we eliminated from the analysis the matureindividuals, we did not observe differences for leaf type(F[3,60] = 0.46, p = 0.75), incubation time (F[4,60] = 2.15,p = 0.09), or interaction (F[12,60] = 1.08, p = 0.39).

Invertebrate dynamics and dominant speciesThe total number of individuals colonizing the leaf bags

per channel was related to the total number of individualsdrifting from them (adjusted R2 = 0.09, F[1,98] = 9.1, p <0.05). However, when drift density was fractioned into twocomponents (mature and larvae), the invertebrate colonizationwas not related to larvae drift (adjusted R2 = 0.01, F[1,98] =1.4, p > 0.05), which may indicate that individuals driftfrom channels mostly as mature individuals (i.e., pupae oremerging adults).

Initially, Corynoneura spp. colonized all leaf types athigher proportions than B. retifinis. After the first week, den-sity of B. retifinis increased at a higher rate than other spe-cies, and thus, the invertebrate dynamics observed in thisstudy seemed to be mainly determined by the dynamics ofthe numerically dominant species B. retifinis (Fig. 6). A fur-ther graphical exploration of colonization vs. drift dynamics,coupled with the combined representation of dominant taxacomponents of colonization (B. retifinis) and drift numbers(total, mature, B. retifinis), revealed differences in coloniza-tion and drift rates depending upon the leaf type (Fig. 6).The colonization dynamics of B. retifinis showed sigmoidpatterns for all leaf types, except for cedar leaves where thecolonization was slow and it showed a negative asymptoticpattern (Fig. 6). Maximum rates of colonization were ob-served in alder treatments (i.e., single and mixed) at day 28.We observed differences in both drift densities and compo-

sition depending upon the leaf types and mixtures. Drift waslow at day 7, independent of leaf type, and later increased(Fig. 6). The high percentage of total drift observed for alderleaves at day 14 was mainly due to the drift of Coryno-neura spp. individuals. By day 14, 40% of individuals drift-ing from alder leaves (i.e., single and mixed treatment) weremature, whereas this component of drift from cedar and eu-calyptus leaves was only 20%. Interestingly, there was a highdrift density of B. retifinis larvae from cedar and eucalyptusleaves over the study period (Fig. 6).

Discussion

We compared leaf decomposition rates, nutrient dynamicsin leaves, and invertebrate responses as colonization and driftby manipulating native and non-native litter quality instream-side channels on a small, temperate rainforest stream.

Fig. 4. Colonization patterns of invertebrates on each leaf type, ex-pressed as number of individuals per gram of leaf ash-free dry mass(mean ± SE, n = 4). Symbols represent different leaf types: alder(solid circles), mixed (open circles), cedar (solid triangles), and eu-calyptus (solid squares).

Fig. 5. Invertebrate abundances of different functional feedinggroups colonizing leaf bags at the time (days) at which the maxi-mum colonization was achieved (i.e., days are shown in parentheseswithin each leaf type). Only those taxa with relative abundances>0.1% are represented. Functional feeding groups are shown by ca-pital letters: collector–gatherers (CG), predators (P), collector–filterers (CF), and shredders (SH). Treatment groups are as follows:A, alder; AC, alder–cedar; C, cedar; E, eucalyptus.

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The results were complex and showed interactions betweenspecies and ecosystem processes that may influence struc-tural components and functioning in these streams.

Decomposition and nutrient dynamicsThe sequence of decomposition rates of leaf species ob-

served in this study was as follows: A. rubra (single) > A. ru-bra and T. plicata (mixed) > T. plicata (single) ≥ E. globulus(single). Leaf decomposition rates of alder leaves (i.e., high-quality) tended to be faster than that for cedar and eucalyp-tus, which is consistent with previous studies (Webster andBenfield 1986; Canhoto and Graça 1999; Lecerf et al. 2007).Changes in the chemical composition and organic matter par-ticle size reflect inherent changes in leaf quality and wereproposed as useful predictors of decomposition (see Mooreet al. 2004). Accordingly, alder leaves had initially higher nu-trient content than the other leaves, which influenced higherdecay rates and higher quality resources for stream inverte-brates. The initial increase in N content in alder and mixedleaf bags can be explained as a result of N immobilizationby microbial and fungal activity (Webster and Benfield1986; Gessner 1991). In contrast, nutrient contents (i.e., Nand P) in cedar and eucalyptus leaves remained more or lessconstant during the incubation period. This result seems to be

related to specific leaf traits more than by leaf origin or iden-tity per se (Hladyz et al. 2009).In the present study, cedar leaves decomposed faster in the

mixed treatment than in the single one, suggesting that rap-idly decaying litter stimulates decay in adjacent, more recalci-trant litters (Gartner and Cardón 2004). Notwithstanding, Nimmobilization on single alder leaves was higher than thatobserved on mixed leaves. We suggest that there was a highdensity of shredders on alder leaves because of their high Ncontent and thus the potential for a priming effect (Guenet etal. 2010). In this case, the priming effect of the cedar may beto diminish biofilm development on alder, but more specificmicrobial experiments may need to be performed.

Invertebrate dynamicsRecent studies highlight the importance of species compo-

sition, dominance, and intra- and inter-specific relationshipsto achieve a more realistic view of what happens in nature(Woodward 2009). In the present study, we documented sim-ilarities in invertebrate community composition among thedifferent leaf types supplied (70% of average similarity),mostly due to the great abundance of dominant taxa. How-ever, invertebrate density and trophic structure (in terms offunctional feeding groups) differed among leaf types. This

Fig. 6. Cumulative plots of invertebrate densities (%) during the incubation time to compare the invertebrate dynamics in each leaf type:(a) alder, (b) mixed, (c) cedar, and (d) eucalyptus (mean ± SE, n = 4). Each figure represents colonization densities (i.e., Brillia retifinis) anddrift densities of total individuals, mature individuals (i.e., pupae and adults), and larvae of B. retifinis.

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different pattern of invertebrate colonization influenced bythe quality of leaf resources has been shown previously (Haa-pala et al. 2001; Lecerf et al. 2005; Hladyz et al. 2009). Ourresults support the idea that decomposition rate is a good in-dicator of food quality, especially for shredders. Althoughone field experiment carried out in Spain has suggested nodifferences in total density of invertebrates in leaf packs indeciduous forested streams in comparison with eucalyptusones (Larrañaga et al. 2006), other studies demonstrated sim-ilar differences as in this study (Abelho and Graça 1996; Ló-pez et al. 2001; García and Pardo 2012).Invertebrates that colonized leaf bags containing a mixture

of labile and recalcitrant species responded with an inter-mediate pattern between both leaf types. Indeed, the numberof invertebrates colonizing mixed leaves (52.5%) was almostproportional to the amount of each litter type (i.e., 100% onalder leaves and 25.2% on cedar leaves). In addition, low in-vertebrate densities per gram of eucalyptus leaves (20%) weresimilar to those observed in single cedar leaves, probably as aconsequence of their poor nutrient quality and physical prop-erties. Despite using only one exotic species in the presentstudy, our results indicate that these consumers did not dis-criminate among exotic and native leaves. In regions whereplantations with Eucalyptus or some other non-native treesreplace native riparian vegetation, it can lead to a strong de-crease in food quality and diminish productivity of thosestreams. On the other hand, red alder has increased in its ex-tent in coastal forests of North America because of humandisturbances, especially forestry, and has probably increasedproductivity of streams over pre-industrial levels owing to in-creased amounts of high-quality leaf inputs (Wipfli and Mus-slewhite 2004; Wipfli et al. 2007).In the present study, drift density varied over the incuba-

tion period and seemed to be influenced by leaf quality. Ingeneral, there were more individuals drifting from channelswith alder leaf bags (∼30%) than from channels with cedaror eucalyptus (22.3% and 19.5%, respectively). However,when we excluded pupae and adults from the analyses (i.e.,mature specimens), we did not find statistical differencesamong leaf types, and thus it is possible that some drift re-sponses may be related to life-stage-specific processes(Shearer et al. 2003). Indeed, our results showed that thisfact is more related to the emergence and presence of matur-ing individuals than to the larval stage.Some studies have suggested that taxa exploiting patchily

distributed resources such as leaf packs are among the mostlikely to enter the drift (Townsend and Hildrew 1976;Mackay 1992), and Orthocladiinae species are one of themost abundant groups drifting during warmer months innorth-temperate streams (Coffman 1973). Our drift samplesincluded a variety of taxa, although dominant species driftingfrom the channels were Orthocladiinae that colonized leafbags (including pupae and adults). The main difference be-tween colonization and drift samples was the absence of Bae-tis spp. (scraper) and simuliids (collector–filterer) in leafbags. Meanwhile, Zapada spp. and Lepidostoma spp. (shred-ders) appeared only in leaf bags but not in the drift. Thesedifferences can be explained by food availability and habitatrequirements, but also by traits of individual species. Theseindividuals have long life cycles and they were not nearingmaturation as we observed for Orthocladiinae species.

Dominant speciesThe numerically dominant taxa inhabiting leaf bags were

larvae of the midges B. retifinis and Corynoneura spp., buttheir colonization patterns showed differences among leaf lit-ter treatments. Corynoneura spp. colonized leaf bags duringthe first days, and after that, B. retifinis increased. Therefore,Corynoneura spp. seems to be more of a fugitive (or pioneer)since it comes in quickly but also gets displaced quickly, andB. retifinis seems to track shifts in resource abundance byvirtue of its short generation time and colonize leaf bags byreplacement of Corynoneura spp. These results demonstrate avery striking pattern, previously observed in these two genera(Richardson 1991, 1992), which may respond to the succes-sional replacement of the dominant, closely related speciesthat use leaves as a common habitat (food and refuge; see Al-lan 1995).The structural traits of particular leaf species are important

to test in consumer–resource interactions and their effect onecosystem functioning (Kominoski et al. 2011). In thepresent study, different interspecific invertebrate responseswere observed among leaf types, mostly with dominant chi-ronomid species. In those channels incubated with alderleaves (single or mixed), there was (i) a high number of ma-ture specimens (i.e., pupae and adults) of B. retifinis driftingfrom the channels at days 28 and 48, indicative of the com-pletion of their life cycle, and (ii) a maximum larval driftingof B. retifinis at day 42, when only 20% of leaf mass re-mained in the alder bags, indicative of a potential food quan-tity limitation by following a previous study thatdemonstrated behavioral, numerical, and life history re-sponses to fluctuations in resource level (Rowe and Richard-son 2001). Meanwhile, the highest total drift from high-quality leaves was at day 14 because of the early drift of Cor-ynoneura spp., the other dominant species. Corynoneura spp.is a collector–gatherer that emigrates from the leaf bags asother colonizers establish on the leaves. Corynoneura spp.appears to be a pioneer species and may be influenced by aninterspecific interaction with B. retifinis. In accordance withSwan and Palmer (2006), our results indicated that identityof resource species may be more important for detritivoreperformance than species richness per se.Following from the above discussion, drift of shredders

(mostly B. retifinis) inhabiting channels with slow- andmedium-decomposing leaves would occur as they search forbetter quality food patches (i.e., a density-dependent mecha-nism) but not for food quantity limitation. However, differentpatterns were observed between cedar and the other leaftypes. Indeed, a high larval drift of B. retifinis was foundfrom cedar leaves during the first weeks of the incubation,whereas the colonization pattern of leaves was slow. We ex-plain these results as a consequence of leaf-specific physicalattributes of this conifer species, such as small size, waxycoating, and low nutrient contents.The study of numerically dominant, strongly interacting

species is important to understanding their role and influenceon ecosystem functioning. In particular, B. retifinis seems tobe adapted to alder leaves, while it does not show preferencefor either other native or non-native leaves (i.e., poorconsumer–food response). Although our results do not showdifferent colonization patterns between cedar and eucalyptus,they should not be interpreted to mean that the planting of

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eucalyptus is inconsequential to consumer populations (e.g.,reductions in productivity), and reforestation with exotic spe-cies should be carefully controlled.

AcknowledgementsWe sincerely thank Antoine Lecerf for his selfless assis-

tance in the experimental design and everything involved incompletion of this experiment. We also thank Xavier Pintofor his help in the construction of experimental channels andAmandine Chargois, Trent Hoover, and Takashi Sakamaki fortheir assistance with field and laboratory work, as well asmoral support. We appreciate the assistance of the staff atthe MKRF. This work was partially supported by the ForestSciences Program of British Columbia.

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