Anthropogenic alterations of lotic food web structure: evidence fromthe use of nitrogen isotopes

Caroline Anderson and Gilbert Cabana

C. Anderson (caroline.anderson@uqtr.ca) and G. Cabana, Dept de Chimie�Biologie, Univ. du Quebec a Trois-Rivieres, 3351 Boul. Des Forges,CP 500, Trois-Rivieres, QC, G9A 5H7, Canada.

Understanding the processes that regulate food chain length in nature is a classic theme in ecology. Two factorsexpected to explain variation in food chain length are resource availability (productivity) and environmental stress. Weexamined the impact of anthropogenic activities, both a source of stress and productivity, on lotic food webs using twosimple food web descriptors based on stable nitrogen isotopes (d15N). We used 1) trophic position of small fish and 2)slopes of d15N-size class relationships in the invertebrate community as variables related to food chain length. Trophicpositions and d15N-size slopes changed significantly across the 23 study sites selected to vary in productivity and impactfrom industrial activities (trophic position�0.4 to 1.9; slopes��1 to �2.8). Fish trophic position was not affectedby productivity (chlorophyll a) or environmental stress (number of factories on the watershed) and was not modulatedby the proportion of predatory invertebrates in the food web leading to fish. This lack of relationship suggests thatvariation in trophic position is likely influenced by fish feeding behaviour and is therefore not a good integrator ofchanges in food chain length induced by anthropogenic activities. d15N-size slopes significantly increased withproductivity and decreased with stress, suggesting that trophic organization by size within invertebrate communities isaffected by these factors. These slopes also tended to be greater when the proportion of predators in the communityincreased in larger size classes. These results suggest that when productivity is high and stress is low, proportionsof higher d15N-value predators in lotic food webs tend to increase, contributing to the lengthening of food chains.They also suggest that d15N-size relationships of invertebrate communities may be used as indicators of food webstructure alteration by human activities.

In past decades, numerous researchers have sought toidentify the factors regulating food chain length in naturalsystems. Two of the most widely discussed factors areresource availability (productivity) and environmentalstress. Early theoretical models predicted longer food chains(more trophic levels) in more productive systems (Fretwell1977, Oksanen et al. 1981), because higher productivity atthe base of the food web can support larger populations ofconsumers (primary, secondary, etc.). On the other hand,the environmental stress hypothesis states that food chainlength should decline with increased stress, because ofreduced energy flow to predators (e.g. loss of prey speciesat lower trophic levels) and greater sensitivity of predatorsto stress (Odum 1985, Menge and Sutherland 1987,Jenkins et al. 1992). These studies have often focussed onthe addition or removal of top predators, but systemproductivity and environmental stress may also influencefood chain length through the addition or removal ofintermediate trophic levels (Wootton and Power 1993,Sherwood et al. 2002, Thompson and Townsend 2005).This mechanism is what Post and Takimoto (2007) termed‘insertion mechanism’. They proposed that the addition orremoval of species in the lower echelons of the food web

(intermediate predators) is an important factor accountingfor variability in food chain length.

Human activities have the potential to influence foodchain length in aquatic ecosystems through removal oraddition of intermediate trophic levels because they affectresource availability (release of large amounts of nutrients)and increase environmental stress (e.g. inputs of contami-nants, controlled flooding regimes). Cultural eutrophicationof aquatic systems could increase food chain length byinducing greater primary productivity, which would subse-quently support larger populations of aquatic consumers.This hypothesis is supported by Townsend et al. (1998) andThompson and Townsend (2005) who found a significantpositive correlation between food chain length, measured astotal number of links, and algal primary productivity instreams. These increases in the number of links were largelygenerated by the introduction of predatory invertebrates inthe food webs (intermediate-level consumers). Conversely,contaminants released by industrial activities in lakesand rivers (heavy metals, PCBs, etc.) could reduce foodchain length by increasing environmental stress. Severalstudies have found simplified food webs and fewer trophiclevels in acidified and industrially-contaminated systems

Oikos 118: 1929�1939, 2009

doi: 10.1111/j.1600-0706.2009.17368.x,

# 2009 The Authors. Journal compilation # 2009 Oikos

Subject Editor: Jonathan Shurin. Accepted 29 June 2009

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(Ford 1989, Havens 1991, Locke 1996, Sherwood et al.2002). Sherwood et al. (2002) found such simplification tobe induced mostly by the loss of intermediate predators(predatory invertebrates) leading to fish.

Previous studies that have examined the effect ofproductivity or stress on food chain length have either beenlimited to simple food web descriptions using discretetrophic levels, which underestimated omnivory (Oksanenet al. 1981, Persson et al. 1992), or have necessitated inten-sive sampling and identifying efforts in order to properlyevaluate food web structure (e.g. connectance and/or gutcontent analyses; Briand and Cohen 1987, Spencer andWarren 1996, Townsend et al. 1998, Thompson andTownsend 2005). Stable nitrogen isotopes can be usedas a tool to effectively evaluate food web structure becausethey are a bulk integrator of long-term diet and takeinto account complex interactions such as omnivory(Cabana and Rasmussen 1994, Vander Zanden et al.1997, Post 2002).

Two simple food web descriptors based on nitrogenisotopes could be useful in assessing the effects of anthro-pogenic activities on food chain length. Fish trophicposition measured using d15N could be used as anintegrator of changes in the trophic structure and in thelength of the food chain leading to these consumers(Cabana and Rasmussen 1994, Vander Zanden et al.1999, Post et al. 2000). For example, Cabana andRasmussen (1994) and Vander Zanden et al. (1999) usednitrogen isotopes to examine variability in lake trout trophicposition. They found that trophic position was greatlymodulated by the presence of intermediate trophic-levelconsumers (predatory invertebrates (mysids) and foragefish). They also found that the addition of such inter-mediate trophic levels to the food web resulted in thelengthening of the path of energy (longer food chains) andin increased biomagnification of contaminants in lake trout.These results suggest that trophic position measured withd15N can be used to examine the effects of the insertionmechanism discussed by Post and Takimoto (2007).

Variation in d15N with size in the invertebrate commu-nity may also help assess the effects of anthropogenicactivities on food chain length through the insertionmechanism. Relationships between d15N and body sizehave been found to be sensitive to the presence of predatoryorganisms or parasites (organisms with higher d15N values)in the food web. Positive d15N-size slopes have been foundin aquatic food webs where predation or proportions ofpredators increased with body size (Fry and Quinones1994, France et al. 1998, Jennings et al. 2002). Conversely,negative relationships have been documented in commu-nities dominated by small predators or parasites (high d15Nbut smaller size than their prey; Leaper and Huxham 2002)or by large primary consumers with low d15N values(Maxwell and Jennings 2006). Anthropogenic activitiesthat influence the presence of high d15N-value invertebratesat different size classes should therefore affect d15N-sizeslopes of the invertebrate community. For instance, severallarge common predatory invertebrates are known to bepollutant-sensitive (Hilsenhoff 1988, Resh et al. 1996).These large predators are more exposed to bioaccumulationof toxins via biomagnification than other large non-predatory organisms (Vander Zanden and Rasmussen

1996, Stewart et al. 2004, Croteau et al. 2005). This couldlead to a preferential loss of large predatory invertebrates instressed systems, a loss that would result in shorter foodchains and weaker d15N-size slopes.

In the present study, we examine whether smallinvertebrate-feeding fish trophic position measured withd15N and d15N-size relationships of the invertebratecommunity can be used as indicators of the alteration offood chain length by anthropogenic activities. We firstexamine the effects of chlorophyll a (productivity) andnumber of factories with pollutant-releasing potential onthe watershed (environmental stress) on these food websattributes. Our aim is also to evaluate whether the insertionmechanism accounts for a large part of the variability inboth isotopic descriptors. We therefore look at the effect of1) increases in percent predatory invertebrates in the wholecommunity and 2) increases in percent predatory inverte-brates with size class (predatory invertebrate-size slopes) ontrophic position and d15N-size relationships. We hypothe-size that the trophic position of invertebrate-feeding fishshould reflect changes in the composition of the inverte-brate community trophically linked to them. Highertrophic position should be associated with greater propor-tions of predatory invertebrates (either in the wholecommunity or in larger size classes (steeper predatoryinvertebrate-size slopes)). It should also increase withproductivity, and decrease with increasing numbers offactories on the watershed. Likewise, d15N-size slopes ofinvertebrate communities should be steeper in moreproductive systems because of increasing proportions ofpredatory invertebrates with size (e.g. large predatoryinvertebrates feeding on smaller-sized predators, etc.).Conversely, slopes should be lower in systems impactedby industrial pollutants, where pollutant-sensitive predatorsare scarce.

Methods

Site selection

Our goal was to select sites showing variable levels of systemproductivity and potential stress associated with industrialactivities. We used chlorophyll a concentrations in riverwater (active chlorophyll a in the water column) as aproductivity index and number of factories with pollutant-releasing potential on the watershed as an environmentalstress index. Chlorophyll a is an indicator of algal biomassand reflects the primary productivity of a system. Positivecorrelations between water column chlorophyll a andnutrient concentrations have been documented in largerivers (Basu and Pick 1996, Heiskary and Markus 2001,Smith 2003). Industrial activities on the watershed can be asource of contaminants to rivers and lakes and, conse-quently, a greater number of factories may be associatedwith greater concentrations of contaminants. We usednumber of factories instead of contaminant concentrationsin river water because these concentrations were notavailable for all our sites.

To justify the use of number of factories on thewatershed as an indicator of contaminant concentrations,we examined in a different data set the relationship between

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the concentration of industrial contaminants in river waterand number of factories on the watershed using datapublished in previous reports of the Ministry of Environ-ment of Quebec (Berryman 1996, Berryman and Nadeau1998, 1999, Berryman et al. 2002). Types of factoriesincluded wood and pulp industry, chemical industry,primary metal industry, textiles, food industry, and oilrefineries (activities having a potential to pollute aquaticsystems due to the quality and quantity of their dischargesfollowing Dartois and Daboval 2003). Briefly, we per-formed a principal components analysis on the waterchemistry data shown in these reports and obtained a firstaxis (PC1; accounting for 33% of the variability of the dataset composed of 13 types of contaminants) characterized bysix industrial pollutants: aluminium, chromium, copper,magnesium, nickel and lead, which scored at least 0.45 onPC1 (loadings considered at least fair; Tabachnick andFidell 2001). We then plotted the factor scores of PC1against the total number of factories on the watershedshown in these reports. The relationship between thenumber of factories (log-transformed) and PC1 was mod-est, but significant (n�19, r2�0.31, p�0.013; higherconcentrations found in more industrial watersheds),supporting our decision to use the total number of fac-tories on the watershed as an indicator of industrialcontamination.

In order to select sampling sites, we compiled existingdata on chlorophyll a concentrations and number offactories on the watershed for 76 river sites, from whichwe subsequently selected a fewer number of sites showingcontrasting chlorophyll a concentrations and numbers offactories. Overall, 23 sites were selected.

Land use and water quality data

Delineation of the 23 selected watersheds and land usecharacterization were performed as shown in Andersonand Cabana (2005, 2006). Sites were located within11 subwatersheds of the St. Lawrence River watershed(Quebec, Canada; Fig. 1), and catchments ranged from 175to 42 820 km2. Number of factories (types cited above) onwatersheds upstream of each potential study site wasestimated using databases from the Centre de RechercheIndustrielle du Quebec (2003) for spring 2003, and rangedfrom 0 to 432 (mean�84, SD�120). Total number offactories was also divided by water discharge to yield anindustrial gradient corrected by river discharge. Estimatedwater discharge ranged from 4.5 to 641 m3 s�1 (mean�88.4, SD�158.7). Chlorophyll a concentrations (watercolumn; mg m�3) were averaged by study sites using datafrom august 1998 to august 2003 (average of the five yearspreceding the sampling month) provided by the Ministry ofEnvironment of Quebec (Ministere de l’Environnement duQuebec 2004). Measurements were taken, on average, onceor twice per month for each study site during the summerperiod (May to October). The total number of chlorophylla measurements by site ranged from 15 to 38. Chlorophyll aconcentrations ranged from 0.66 to 16.92 mg m�3

(mean�4.96, SD�4.00).

Sampling and identification

Invertebrates and fish were collected in August 2003.Invertebrates were collected with a Surber net (0.1 m2;0.6 mm mesh size; four to seven replicates taken at eachsite) and a D-frame aquatic net (1 mm mesh size). Fish werecaptured by electro fishing. Invertebrates caught withSurber nets were used to derive d15N-size slopes of thecommunities examined, whereas invertebrates collectedusing the D-frame nets (primary consumers) and fishwere used to estimate fish trophic position (invertebrateshere were used to derive the baseline d15N values; Andersonand Cabana (2007)). Samples were kept in coolers andfrozen within eight hours and then thawed for sorting andidentification. Invertebrates caught with the D-frame netwere sorted and identified to family or genus. Invertebratescaught with the Surber net were sorted by size class bywashing organisms through a series of 10 brass-framelaboratory sieves (mesh sizes: 0.5, 0.71, 0.85, 1, 1.41, 2,2.83, 3.36, 4 and 8 mm), and identified to family.Invertebrates that fell through the 0.71 mm mesh size sievebut which were retained by the 0.5 mm mesh size sieve werekept in all analyses, despite the fact that the Surber net had amesh size of 0.6 mm. This could have induced certainvariability in the 0.5 mm size class results.

Invertebrates collected with the surber net were classifiedinto six groups according to Merritt and Cummins’ (1996)and Thorp and Covich’s (1991) classifications (primaryconsumer (except chironomids, nematods and zooplankton,which were not separated in predatory and non-predatorygroups), predator (including potential parasites such asleeches and water mites), omnivore, chironomid (identifiedto the family), nematoda (identified to the family), andzooplankton). Predators, which made up 2.4% of allorganisms captured, were principally composed of Plecop-tera (32%; almost exclusively Perlidae) and Diptera (27%;mostly Empididae and Athericidae). Fish were identified tospecies (Scott and Crossman 1974). Captured fish were

Figure 1. Study sites sampled in summer 2003.

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small specimens of four non-piscivorous species (longnosedace Rhinichthys cataractae; blacknose dace Rhinichthysatratulus; Johnny darter Etheostoma nigrum; logperchPercina caprodes) and juvenile smallmouth bass Micropterusdolomieui (5103 mm). These species were selected becausethey were well distributed throughout study sites. A total of121 individual fish were captured and used for isotopicanalyses (2�11 individuals per site; 1�4 species per site).Their overall size (total length; measured after freezing andthawing) ranged from 37 to 117 mm (mean�68 mm,SD�19 mm).

Once identified, all samples were dried at 608C for atleast 48 h and ground into a homogenous powder. Inverte-brates collected with the Surber net were pooled by size classfor isotopic analyses. Two to five samples randomly drawnfrom the Surber samples collected on the field were analysedfor each study site. Surber replicates showing too smallamounts of material for isotopic analyses were pooled forsome sites (replicates of the 0.5, 0.71 and 0.85 mm classeswere combined for 15, 12 and 8 sites, respectively). Otherinvertebrates (D-frame net), which were used to derive thebaseline d15N values used in the fish trophic positionestimates, were pooled and analysed by genus or family.Invertebrates were used whole, except molluscs which wereremoved from their shells. Non-animal materials wereremoved from the samples prior to the analyses. In thecase of fish, small sections of muscle tissue were taken fromindividual fish. Isotopic analyses were performed on allsamples as shown in Anderson and Cabana (2005). A totalof 610 samples were analysed and used in the present study.54 samples were analysed in duplicate and showed a meanstandard deviation of 0.21�.

Trophic position estimates

Using baseline organisms belonging to various functionalfeeding and taxonomic groups can lead to biases in trophicposition estimates (Anderson and Cabana 2007). In thepresent study, we used the procedure detailed in Andersonand Cabana (2007) to estimate fish trophic position.Briefly, ubiquitous primary consumers (three scraperfamilies) with low d15N values were used as baselineindicators. We also included d15N values of hydropsychids(Trichoptera: Hydropsychidae) in the baseline d15N esti-mates because they were dominant in numerous sites andtheir exclusion would have lead to fewer sites for whichtrophic position could have been estimated. Before comput-ing baseline d15N, we corrected Hydropsychidae d15Nvalues toward Psephenidae (Coleoptera) d15N as was donein Anderson and Cabana (2007) for two scraper families.This correction was necessary in order to reduce potentialbiases related to the use of different invertebrate groups withvariable d15N values. In Anderson and Cabana (2007),psephenids were identified as baseline indicators towardwhich d15N values of other organisms should be corrected,because they showed the lowest d15N values compared toother scrapers (suggesting little or no omnivory). The meandifference between hydropsychids and psephenids calcu-lated using the dataset of Anderson and Cabana (2007), wasof 1.42� (paired t-test, Bonferroni corrected; pB0.0001).We used this value to correct Hydropsychidae d15N

downwards toward Psephenidae d15N. Last, d15N valuesof Ephemerellidae (Drunella), Heptageniidae (Heptageniaand Stenonema), and Hydropsychidae were all correctedtowards Psephenidae d15N, as shown in Anderson andCabana (2007), and d15N values of these four families wereaveraged by site to yield baseline d15N. Using this baselined15N value, we estimated trophic position following theequation:

trophic positionconsumer

�((d15Nconsumer�d15Nbaseline)=3:4)�2 (1)

where d15Nconsumer is the d15N value of the consumer forwhich the trophic position is estimated, d15Nbaseline is thed15N value of the baseline organism, and 2 is the expectedtrophic position of the organism used to estimate baselined15N (e.g. an herbivore). Trophic position was onlyestimated for fish and not for invertebrate size classes, sincecorrecting for baseline d15N was not necessary to examined15N-size slopes of the invertebrate community.

Statistical analyses

Analysis of covariance (ANCOVA) was used to examine theeffects of fish species and fish size on trophic position. TheANCOVA model included fish size (covariate), species(categorical variable), and an interaction term (species�size). Spatial variation in trophic position was examinedwith a one-way Anova using site as a factor. These analyseswere performed using data on individual fish as replicateswithin sites. Percent predatory invertebrates (% individuals)was calculated on the total number of organisms collectedfor each size class, as well as for the entire invertebratecommunity (all size classes combined). Slopes of therelationship between d15N and size (log-transformed), andslopes of change in percent predatory invertebrates with sizewere computed using linear regressions. d15N values andpercent predatory invertebrates were averaged by size classfor each site (two to five replicates averaged) prior tostatistical analyses. Changes in d15N and percent predatorswith size among sites were examined using covarianceanalyses with log size and study sites as factors.

Relationships between trophic position and d15N-sizeslopes, and relationships between these two dependentvariables and the independent variables (chlorophyll a,number of factories, percentage of predators, and predatoryinvertebrate-size slopes) were examined using simple linearregressions. A multiple linear regression was used toevaluate the combined effect of chlorophyll a and numberof factories on trophic position and d15N-size slopes,respectively. We further examined the relative contributionof chlorophyll a and number of factories to the multipleregression with d15N-size slopes using a partial r2 analysis.We also performed a linear regression between the residualsof the chlorophyll a/d15N-size slopes relationship and thenumber of factories to assess the relative effect of the twoindependent variables on d15N-size slopes. Lastly, we usedan Akaike information criterion (AIC) model selection testto determine which model (linear regression or multipleregression) best explained the variability in d15N-size slopes(Tabachnick and Fidell 2001).

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Statistical analyses were performed using SYSTAT (ver.8.0, SPSS Inc. 1998) and SAS (ver. 8.0, SAS Inst. Inc.1999). In order to meet regression analysis assumptions(Zar 1999, Tabachnick and Fidell 2001), fish body size,invertebrate size class and number of factories (and numberof factories/discharge) were log-transformed. Chlorophyll aconcentrations were square-root transformed and percen-tages (predators) were arcsin transformed.

Results

Trophic position and d15N-size relationships

Fish trophic position varied greatly across sampling sites,ranging from 2.39 to 3.89 trophic levels (Table 1). Nosignificant effects of fish species (ANCOVA, p�0.644)and size (p�0.744) were found on trophic position, andthere were no significant differences between the slopes ofchange in trophic position with size among fish species(interaction between size and species, p�0.629), enablingus to use fish trophic position without correcting for sizeor species effect. An analysis of variance showed that71% (F�10.847, DF�22,99, pB0.0001) of the varia-tion observed in fish trophic position was attributable tosite effects, suggesting heterogeneity in food web struc-ture among our study sites.

d15N values of invertebrates increased significantly withsize in 14 of the 23 study sites (pB0.05, Table 1, Fig. 2).Slopes of these 14 relationships spanned from 0.54 to 6.78.Of the remaining nine sites (slopes from �0.99 to 1.1; Fig.2), one site showed a trend towards a decrease in d15N withsize (r2�0.35, p�0.072; site C8 in Table 1), whereasrelationships for the 8 other sites were non significant atp�0.10. A covariance analysis using log size and study sites

as factors confirmed that change in d15N with size wassignificantly different among the 23 study sites (interactionof site and log size on d15N: F�3.57, DF�22,198,pB0.0001). The highest slope (6.78) measured in one sitewas clearly an outlier. This high slope was potentiallycaused by the presence of small zooplankton (personalobservation) with low d15N values in the food web likelyoriginating from a reservoir (dam) located upstream of thesampling site (�500 m). This site was removed fromsubsequent analyses involving d15N-size slopes.

Fish trophic position and slopes of d15N-size relation-ships of the invertebrate community were not significantlycorrelated (p�0.742).

Table 1. Statistics for fish trophic position and d15N-size relationships of the invertebrate community for the 23 study sites. First letter of thestudy site corresponds to the main watershed in which the site belongs (A�Sainte-Anne, As�L’Assomption, B�Batiscan, Bc�Becancour,C�Chaudiere, E�Etchemin, F�Saint-Francois, L�du Loup, M�Saint-Maurice, N�Nicolet, Y�Yamaska).

Study site River Fish trophic position d15N-size slope r2 (d15N-size slope)

A3 Sainte-Anne 3.79 �0.37 0.05As1 L’Assomption 3.64 0.89 0.56**As2 L’Assomption 3.51 0.09 0.00As5 L’Assomption 2.90 �0.99 0.18As7 De L’Achigan 3.52 2.23 0.57**B2 Des Envies 3.41 1.53 0.68***Bc1 Becancour 3.13 1.77 0.65**C5 Chaudiere 3.18 0.96 0.51*C6 Beaurivage 2.39 0.54 0.52*C8 Chaudiere 3.87 �0.97 0.35E1 Etchemin 2.83 0.88 0.17F10 Saint-Francois 3.11 6.78 0.89***F14 Saint-Francois 3.09 1.44 0.65**F4 Magog 3.89 1.09 0.29L1 Du Loup 3.44 1.04 0.47*M1 Shawinigan 3.09 �0.16 0.02M3 Saint-Maurice 3.63 1.02 0.80**M5 Saint-Maurice 3.17 �0.33 0.02N2 Nicolet 3.71 0.89 0.70**N5 Nicolet Sud-Ouest 3.17 2.76 0.82***Y4 Noire 3.55 0.20 0.03Y5 Yamaska 3.19 1.29 0.89***Y8 Yamaska 3.23 1.67 0.62**

*�pB0.05; **�pB0.01, ***�pB0.001.

Figure 2. Relationships between d15N and size class of theinvertebrate community for the 23 study sites. Note that one siteconsidered as an outlier was removed from the figure (slope�6.78). Relationships were scaled to a common intercept bysubtracting the d15N value of the smallest size class from alld15N values (difference in d15N) for each study site. Regres-sion lines of significant relationships (pB0.05) are represented bysolid lines. Non significant ones (p�0.05) are represented bybroken lines.

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Productivity and environmental stress

Fish trophic position was not significantly correlated withchlorophyll a concentrations measured in water (p�0.633,Fig. 3a). However, d15N-size slopes were modestly, butsignificantly correlated with chlorophyll a concentrations(r2�0.22, p�0.029), d15N values showing greater in-creases with size in more productive systems (Fig. 3b).Industrial activities did not significantly affect trophicposition or d15N-size relationships (log factories or logfactories/watershed area: p�0.05).

Combining total number of factories on the watershedwith chlorophyll a concentrations (multiple regression)helped explain a larger proportion of the variation ind15N-size slopes, but not in trophic position (p�0.876).Slopes of d15N-size increased with productivity anddecreased as number of factories increased. The multipleregression obtained (r2�0.43; p�0.005) is:

slope d15N-size

��0:08�0:86 (chlorophyll a0:5)

�0:67 (log10 number of factories) (2)

We further examined the relative contribution of eachvariable to this multiple regression (partial r2) and foundthat, when number of factories was held constant, chlor-ophyll a explained 42% of the variation in d15N-size slopes(p�0.002), whereas when chlorophyll a was held constant,factories explained 27% of this variation (p�0.016). Thesum of chlorophyll a and number of factories partial r2

exceeded the multiple r2, suggesting a correlation betweenboth variables, which also have an opposite effect (e.g. one

variable is hindering the contribution of the other). APearson correlation showed that chlorophyll a and factorieswere significantly correlated (r�0.52, p�0.011), support-ing this interpretation. In addition, the relationship betweenresiduals of chlorophyll a/d15N-size slopes and number offactories showed a weak, but significant effect of industrialactivities on residuals, where negative residuals wereassociated with greater numbers of factories (r2�0.19,p�0.046; Fig. 4). The weak relationship however suggeststhat there are other factors accounting for variability inchlorophyll a/d15N-size slopes residuals. The use of an AICmodel selection test showed that the multiple regressionmodel was the best one to use (DAIC�4.91 comparedto the second best model (simple linear regression ofchlorophyll a vs d15N-size slopes)).

Predatory invertebrates

Percent predatory invertebrates found in the invertebratecommunity varied from 0.1 to 14.7% across sites (all sizeclasses combined by site) and slopes of change in percent(arcsin transformed) predatory invertebrates with sizeranged from �14.1 to 46.0. These slopes varied signifi-cantly among sites (ANCOVA, interaction of site and logsize: F�4.95, DF�22,206, pB0.0001).

No significant relationship was found between fishtrophic position and percent predatory invertebrates acrosssites (total proportion of predatory invertebrates in thecommunity: p�0.965; slope of percent predatory inverte-brate-size: p�0.194). d15N-size slopes of the invertebratecommunity were not significantly correlated with the totalproportion of predatory invertebrates in the community(p�0.742), however, they became marginally steeper (r2�0.18, p�0.053) as the proportion of percent predatoryinvertebrates increased with size (e.g. steeper predatoryinvertebrate-size slopes; Fig. 5).

Discussion

Trophic position and d15N-size relationships

Trophic position estimates of small fish were highly andsignificantly variable among sites and ranged from 2.39(mostly feeding on primary producers) to 3.89 trophic

Figure 3. Relationship between (A) trophic position and (B)slopes of d15N-size slopes and chlorophyll a concentrations. Thelinear regression equation between d15N-size and chlorophyll aconcentrations is: slope d15N-size��0.28�0.52 chlorophylla0.5. Regression lines are represented by solid lines.

Figure 4. Relationship between the residuals of the chlorophyll a/d15N-size slope relationship and number of factories on thewatershed. Regression line is represented by a solid line.

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levels (mostly feeding on secondary consumers). Compar-ably large variability in trophic position estimates of foragefish has been reported in previous studies (Vander Zandenand Rasmussen 1996, Fry et al. 1999, Vander Zanden et al.2000, Anderson and Cabana 2007). Such variability in fishtrophic position can be attributed to three mechanismsdescribed by Post and Takimoto (2007): 1) addition orremoval of intermediate predators, 2) changes in the degreeof trophic omnivory by the top predator (or, in our case, byinvertebrate-feeding fish), and 3) changes in the trophicposition of intermediate predators. In the present study, weexamined the insertion mechanism by comparing changesin trophic position with changes in percent predatoryinvertebrates (e.g. addition of intermediate predators). Weexpected fish trophic position measured with d15N tointegrate the trophic structure of the invertebrate commu-nity (Cabana and Rasmussen 1994). We did not observeany significant relationship between fish trophic positionand percentage of intermediate predators. This lack ofrelationship suggests that the insertion mechanism (increas-ing presence of intermediate predators) is not the dominantmechanism leading to spatial changes in invertebrate-feeding fish trophic position. This is further supported bythe lack of relationship between trophic position and d15N-size slopes of the invertebrate community. We initiallypredicted that steeper d15N-size slopes would be associatedwith higher trophic position. Indeed, if invertebrates tendto show greater trophic position (d15N) with size, fish,which feed on these invertebrates, should also exhibit agreater trophic position. The absence of such a correlationmay be explained by one or both of the two remainingmechanisms identified by Post and Takimoto (2007): fishand intermediate-consumer feeding behaviour.

Several studies have examined fish feeding preferences,with a particular interest in the size of preferred prey.Although some studies found that invertebrate-feeding fishpreferentially ate large prey (Brooks 1968, Werner and Hall1974), others observed humped size preference or prefer-ence for smaller prey (Hansen and Wahl 1981, Teska andBehmer 1981, Bence and Murdoch 1986). These latterstudies examined relationships between prey and predatorsrelatively close in size, which are comparable to theorganisms examined in the present study. Perhaps therelatively small size of fish used in our study (mean size of

68 mm) compared to large invertebrates (up to 8 mm sievesize: equivalent to �21.5 mm mean body length) couldexplain the lack of relationship between fish trophicposition and 1) percent predatory invertebrates (wholecommunity and predatory invertebrate-size slopes) and 2)d15N-size slopes. Unger and Lewis (1983) examined therelationship between length and gape size of a small (16�84 mm body length) planktivorous fish and found a gapesize of �4 mm for fish of �68 mm. We also found(Anderson and Cabana unpubl.) that the average size ofinvertebrates found in the guts of the five fish species used(n�99 fish collected in 6 of the present study’s sites) wasonly of 0.62 mm (sieve size equivalent). Moreover, thelargest invertebrate size class found in the fish stomachs was3.36 mm (sieve size equivalent; in 3 out of 99 fish). Thesefindings suggest that gape size of the invertebrate-feedingfish selected might preclude them from eating largeinvertebrates (]4 mm sieve size) with potentially highertrophic position. They also propose that fish used in thecurrent study seldom feed on very large invertebrates andtherefore do not constitute good integrators of the isotopicsignals present in the size range of invertebrates examined.

Omnivory in consumers leading to fish is a thirdmechanism that could explain the observed variation infish trophic position. In their food web study, VanderZanden et al. (1999) found that omnivory by intermediatetrophic levels explained part of the variability observed inlake trout trophic position in Canadian lakes. We similarlyobserved great spatial variability in invertebrate trophicposition in lotic systems (Anderson and Cabana 2007). Inthe present study, we did not measure trophic position ofindividual invertebrates, but have captured changes inoverall trophic position of the invertebrate communitythrough d15N-size slopes. For instance, steeper slopessuggest that a larger proportion of available prey havehigher d15N values (higher trophic position), which shouldlead to higher fish trophic position. Our findings were notconsistent with this hypothesis, probably because of thereasons mentioned above. They point at fish feedingbehaviour as the main mechanism influencing fish trophicposition.

d15N-size slopes were highly variable across sites,suggesting spatial heterogeneity in food web structure. Wehypothesized that d15N-size slopes would be correlated withpercent predatory invertebrates in the community (wholecommunity and predatory invertebrate-size slopes) andyield information on the lengthening of food chainsthrough the addition of successively larger predators(potentially feeding on smaller ones). We found thatvariability in slopes was weakly but significantly influencedby percent predatory invertebrates in the food web. Perhapsthis weak relationship was caused by the exclusion ofpotentially carnivorous genera or species of invertebrategroups which were only identified to family (e.g. chirono-mids). Omnivory in several groups classified as being nonpredatory (Anderson and Cabana 2007) might also haveinfluenced d15N values and accounted for variability ind15N of size classes. Nonetheless, our results suggest thatvariation in trophic position (d15N) with size in loticcommunities is modulated, in part, by the presence of largepredatory invertebrates, which may themselves be influ-enced by anthropogenic activities.

Figure 5. Relationship between slope of d15N-size and slope ofarcsin transformed percent predatory invertebrates with size.Regression line is represented by a dashed line (marginal relation-ship).

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Size has been suggested as a key factor in the organiza-tion of predator�prey relationships and food web structure(Wilson 1975, Cohen et al. 1993) and one would thereforeexpect to see positive d15N-size relationships in aquaticcommunities. Such relationships have been observed inbenthic (France et al. 1998, Jennings et al. 2002) andzooplanktonic communities (Fry and Quinones 1994,Montoya et al. 2002). However, lack of relationship ordecreases in d15N values with size have also been reported(Leaper and Huxham 2002, Maxwell and Jennings 2006).For example, Maxwell and Jennings (2006) found decreasesin d15N with size for benthic fauna collected in the NorthSea (all fauna combined). The presence of small polychaeteswith high d15N values and large bivalves with low d15Nvalues explained these negative slopes. These studies showthat trophic position does not necessarily increase with size,depending on the structure of the food web (e.g. presence ofsmall predators or parasites versus large predators), aconclusion consistent with our results.

Overall, fish trophic position and d15N-size slopesof lotic invertebrate communities seem to represent twodifferent measurements of food web structure. d15N-sizerelationships reflect changes in the trophic structure of theentire invertebrate community, whereas fish trophic posi-tion does not necessarily integrate such changes. Hence,d15N-size relationships are potentially better tools tomeasure the effect of various environmental factors onfood chain length through the addition or removal ofintermediate trophic levels than fish trophic position, whichseems too influenced by fish feeding preferences to be a soleindicator of impacts of external stressors on the food web.

Determinants of isotopic food web attributes

Although sites examined in the present study ranged fromoligotrophic to eutrophic and showed a wide range in totalnumber of factories on the watershed, fish trophic positionwas not significantly altered by productivity or stress relatedto industrial contaminants. This could be partly explainedby the lack of relationship between fish trophic position andpercent predatory invertebrates which is expected to beinfluenced by anthropogenic activities. However, our resultsare not consistent with previous studies that have observedfeeding behaviour impairment of fish in contaminatedsystems (Atchison et al. 1987, Brown et al. 1987, Weis et al.2000). Fish in such systems fed lower in the food web thanin reference sites. We did not find any evidence for shortertrophic position in industrial sites and our results suggestthat variation in fish trophic position related to feedingpreferences is influenced by others factors than productivityand stress induced by industrial contamination.

We found that d15N-size slopes were significantly steeperin productive sites (higher chlorophyll a concentrations),but weaker in stressed systems (greater number of factorieswith pollutant-releasing potential on the watershed). Stee-per d15N-size slopes in more productive systems support thehypothesis that richer systems favour the presence ofsuccessively larger predators, and consequently, longerfood chains. The fact that d15N-size slopes tended to besteeper when the proportion of predators increased in largersize classes supports this interpretation. In such cases, there

is an increased possibility for larger predators to feed onsmaller ones, thus lengthening the food chain. Townsendet al. (1998) and Thompson and Townsend (2005)documented significant increases in mean chain length,measured as total number of links, with greater algalproduction in streams. They found these increases to belargely associated with the introduction of predatoryinvertebrates in the food web (addition of intermediatetrophic links). Similarly, Wootton and Power (1993) foundthat greater primary productivity increased lotic primarypredators biomass (predatory invertebrates and smallinvertebrate-feeding fish) when larger predatory fish wereabsent. These results support our conclusions that produc-tivity can increase the proportions of intermediate trophiclevels (e.g. predatory invertebrates) in aquatic food webs,contributing to the lengthening of food chains.

The shallower d15N-size slopes observed in industrialwatersheds suggest shorter food chains in stressed systems.In these sites, larger organisms do not show much highertrophic positions than smaller ones. Weaker slopes inpolluted sites could be due to two mechanisms: 1) loss oflarge predatory invertebrates through death or migrationand/or 2) changes in large predatory invertebrates feedingbehaviour (decreasing predation). First, several large pre-datory invertebrate species (e.g. Perlidae (Plecoptera),Corydalidae (Megaloptera)) found in our study sites tendto be more sensitive to pollutants than smaller, moretolerant species such as chironomids or oligochaetes(Hilsenhoff 1988, Resh et al. 1996, Voshell 2002), andcould disappear from polluted sites. This greater suscept-ibility to stress may be attributed to life history traits oflarge predatory invertebrates (longer life span, fewer rest-ing stages to survive unfavourable periods, (Odum 1985,Voshell 2002), and feeding behaviour exposing them toincreased bioaccumulation of contaminants (Stewart et al.2004, Croteau et al. 2005). Loss of diversity in the lowerechelons of the food web is a second factor that might resultin loss of large predatory invertebrates because of reducedenergy flow to the top levels (Odum 1985, Carlisle andClements 2003). A third factor related to the firstmechanism could be the removal of large predatoryinvertebrates through migration. Following Menge andSutherland (1987), large mobile organisms are more likelyto leave stressed systems than small sessile organisms. Sincepredators are typically larger than their prey (Wilson 1975,Cohen et al. 1993), this could result in loss of predatoryinvertebrates. A second mechanism that may lead to weakerd15N-size slopes in stressed systems is feeding behaviourimpairment of predatory invertebrates. Feeding impairmentcould result in organisms feeding lower in the food web(lower d15N values) or being eliminated from the system(death � see first mechanism). A wealth of studies haveobserved feeding impairment of aquatic invertebrates instressed (acidified or polluted) systems (Gerhardt 1992,Maltby et al. 2002, McWilliam and Baird 2002). Gorhamand Vodopich (1992) have examined changes in predationrates of damselfly nymphs (Odonata: Coenagrionidae) inacidified systems, an insect comparable to the large loticpredatory invertebrates examined in our study. They foundthat predation rates of damselflies decreased with increasing

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acidification. Moreover, they found that the feeding rate ofthe largest size class was the most affected by stress.

A few experimental studies have observed shorter andsimplified food chains in acidified (Havens 1991, Locke1996) and metal-polluted systems (Sherwood et al. 2002).In particular, Sherwood et al. (2002) found that food webleading to yellow perch in metal-polluted lakes wasextremely simplified compared with reference lakes. Thissimplification was caused by the disappearance of benthicinvertebrates, especially predatory ones, and lead to atrophic bottleneck (successively larger prey not available).Other studies have also found significant effects ofindustrial activities and contaminants on the loss of aquaticinvertebrate species (Garie and McIntosh 1986, Ford1989), and support our hypothesis of reduction in foodchain length through loss of intermediate trophic levels withincreasing environmental stress induced by industrialpollution.

Conclusion

d15N-size slopes of the invertebrate community weresignificantly altered by human activities. In particular,d15N increased faster with size in productive systems anddecreased in stressed systems. d15N-size slopes also tendedto be steeper when the proportion of predators increased inlarger size classes. These results suggest that when produc-tivity is high and stress associated with industrial contam-ination is low, proportions of higher d15N-valueinvertebrates (e.g. intermediate trophic levels such aspredatory invertebrates) found in lotic food webs tend toincrease, thus contributing to the lengthening of foodchains. They also suggest that d15N-size relationships ofinvertebrate communities may be used as simple food websdescriptors, as well as indicators of food web structurealteration by human activities. The lengthening of foodchains through insertion of higher d15N-value invertebratesin the food webs was not reflected in fish trophic position,suggesting that this descriptor is likely influenced by fishfeeding behaviour and does not provide a good indicator ofthe trophic structure of the food web leading to fish.

Acknowledgements � We thank Melanie Lavoie, Benjamin Jacob,Rosalie Lefebvre, Maryse Longchamps, Mariannick Mercure,Sebastien Bouliane, Mylene Vallee, Marcel Chartrand and YvesParadis for their assistance on field trips and for the identificationof invertebrates and fish. This study was supported by a researchgrant from the Natural Sciences and Engineering ResearchCouncil of Canada to Gilbert Cabana and graduate fellowshipsfrom the Fonds Quebecois de la Recherche sur la Nature et lesTechnologies, the Fondation Desjardins and the Fondation duCentre des Etudes Universitaires de l’Universite du Quebec aTrois-Rivieres to Caroline Anderson.

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