Hydrobiologia 341: 57-64, 1996. 57) 1996 Kluwer Academic Publishers. Printed in Belgium.

Comparisons among colonization of artificial substratum types and naturalsubstratum by benthic macroinvertebrates

Richard J. Casey & Sharon A. KendallAlberta Environmental Centre, Bag 4000, Vegreville, Alberta T9C 1T4, Canada

Received 28 February 1996; in revised form 28 August 1996; accepted 28 August 1996

Key words: Macroinvertebrates, colonization, artificial substrates, natural substrate, sediment, lotic

Abstract

A field study was designed to concurrently evaluate differences in colonization by benthic macroinvertebrates on arange of artificial substratum types (single particles of natural rock or clay brick and baskets of natural substratum)after three colonization periods (1, 8 and 29 days). Fauna on the artificial substrata were compared to naturalsubstratum and the effect of natural epilithic cover on colonization by zoobenthos was determined. Densities oftotal number of organisms and the seven most abundant taxa, total number of taxa and quantity of organic materialwere greater on the natural substratum than on the artificial substratum types. Relative abundances of taxa on pairsof the artificial substratum types, unlike pairs of each artificial substratum type and the natural substratum, werestatistically correlated. Among the artificial substratum types densities of total number of organisms and about one-half of the most abundant taxa, total number of taxa and quantity of organic material were greatest in the substratumbaskets. Natural epilithic cover on the single rock particles and substratum baskets affected the densities of totalnumber of organisms and two of the seven most abundant taxa. These taxonomic groups were at approximately twoto six-fold greater densities on the substrata with fine sediment. Consistent patterns in densities of the zoobenthoson the substrata were found after each colonization period. In our study all measures of the macroinvertebrateassemblages (densities of each taxon, total number of organisms, total number of taxa and relative abundancesof taxa), with few exceptions, were different between each artificial substratum type and natural substratum. Thisresult showed the abundance and composition of the macroinvertebrate fauna on artificial substratum types weredifferent from the natural substratum. Therefore, the choice of using artificial substrata instead of direct sampling ofthe natural substratum should be carefully made. Among the artificial substratum types relative abundances of taxawere similar on the single substratum particles and substratum baskets indicating single particles instead of basketsmight be used to sample the zoobenthos. Investigators should consider the potential effect of the natural epilithiccover of substratum particles on colonization by zoobenthos when choosing the type of artificial substratum.

Introduction

Artificial substrata are used to standardize the sam-pling of benthic macroinvertebrates in similar habitatsof lotic systems (Rosenberg & Resh, 1982; Cairns &Pratt, 1993). An important disadvantage of artificialsubstratum samples is that the macroinvertebrate fau-na often are not representative of the zoobenthos onnatural substratum (e.g., see citations in Rosenberg &Resh, 1982). The natural substratum is best sampleddirectly. Artificial substrata, however, are still used forsampling aquatic systems in national biomonitoring

programs (e.g., De Pauw et al., 1986; Klemm et al.,1990; Cuffney et al., 1993; Gibbons et al., 1993), inrivers when it is not possible to sample the natural sub-stratum (Rosenberg & Resh, 1982; Voshell et al., 1989;Resh & McElravy, 1993) and in experimental studieswhere the effect of treatments are more easily deter-mined using a standard substratum type (Buikema &Voshell, 1993).

Numerous types of artificial substrata used in fresh-water systems have included components of the naturalsubstratum (e.g., mixtures of natural substratum parti-cles in containers and mesh bags of leaves) and stan-

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dardized substrata (e.g., clay bricks and tiles, synthet-ic panels and rope) (Flannagan & Rosenberg, 1982).More recently single natural rock particles were usedas artificial substrata per se (Lake & Doeg, 1985;Lamberti & Resh, 1985). Natural substratum parti-cles used as artificial substrata were prepared usingtwo main procedures. Investigators either removed thenatural epilithic cover from substratum particles (Lake& Doeg, 1985; Lamberti & Resh, 1985) or they leftthe epilithic cover intact (Ciborowski & Clifford, 1984;Clements, 1991). Epilithic material (including algae,bacteria, fungi, detritus, sand and silt) on the sub-stratum is known to affect colonization by zoobenthos(Minshall, 1984; Mackay, 1992).

Few studies have concurrently evaluated the col-onization of the more commonly used artificial sub-stratum types by benthic macroinvertebrates relative tothe fauna on the natural substratum. Results of thesestudies can be used to choose appropriate artificial sub-stratum type for sampling zoobenthos. This field studywas designed to determine differences in macroinver-tebrate colonization on a range of artificial substratumtypes (single particles of natural rock or clay brick andbaskets of natural substratum) after three colonizationperiods (1, 8 and 29 days). Studies using artificialsubstrata have reported approximate times for the den-sities of 'all taxa' to reach equilibrium levels on thesubstratum ranged from 9 to 35 days (Rosenberg &Resh, 1982). Three colonization periods were usedto determine if the same colonization patterns consis-tently occurred after different times. The fauna on theartificial substrata were compared to direct samplesof natural substratum to determine if the zoobenthosassemblages were the same on these substratum types.Finally, the effect of the natural epilithic cover on col-onization by zoobenthos was determined.

Description of the study area

The study was conducted in the McLeod River (54 °

01' N, 115° 50' W) a small-medium sized (4th order)river in Alberta, Canada. The substratum was mostlycobble and a mixture of pebble and gravel. Upper sur-faces of the substratum were covered with a thin layerof sand and silt (< 1 mm) and filamentous biofilm. Dur-ing the study mean water velocity (n = 8) ranged from0.40 to 0.52 m s-1 (measured at 0.4 x water depth witha Price AA meter) and mean water depth (n = 8) rangedfrom 25 to 33 cm.

Materials and methods

Types of artificial substratum used in the study weresingle clay brick and natural rock particles and bas-kets of natural substratum. The clay bricks wererectangular (18.9 x 9.1 x 5.6 cm) with three circularholes (diameter= 3.5 cm) through the brick and a totalsurface area of 0.0785 m2 . The natural rock parti-cles were oval-shaped, laterally flattened, maximumlength = 5-15 cm and a mean surface area of 0.0539 m2

(SDEV = 0.0825 m2, n = 30). Surface area of each rockparticle was calculated using the following formula(derived from equations in Perry & Chilton, 1992):

Surface area = (6/Diameter) x Volume of substratum.

Diameter of each rock was calculated fromfour measurements of circumference (where diam-eter= mean circumference of substratum x 0.31831).Circumferences were measured along equally spacedlines at 45 to each other through pre-marked mid-points on the upper and lower surfaces of each rock.Volume of the rock was calculated by measuring thevolume of water displaced by the rock. The substra-tum baskets were constructed of 1.3 cm screen wire,25 x 25 x 10 cm. Each basket contained a layer ofcobble, with the same physical characteristics as thesingle rock particles, on top of a layer of 3-5 cm ofpebble, gravel and sand. The natural substratum usedfor the single rocks and in the baskets were collect-ed along the shore where there was sufficient quantityof substratum types. Upper surfaces of the substratumat the shore had a thin layer of fine sediment similarto the submerged substratum but without the filamen-tous biofilm. The artificial substrata were thoroughlycleaned before they were positioned at the study sites.The clay bricks were washed in tap water and rinsed inriver water to remove inorganic material. Cobble, usedas the single rock particles and in the baskets, werecleaned in river water using wire brushes and a knifeto remove attached epilithic material. Organisms andorganic material were decanted from the pebble, graveland sand mixture by rinsing it numerous times in riverwater.

The study area was marked into two areas, Site 1and Site 2, of equal size (7 x 12 m). Composition ofthe undisturbed substratum in five 1 x 1 m quadrats atSite 1 and 2 was visually determined as percentage ofsubstratum sizes (boulder >26 cm, cobble = 6-26 cm,pebble-gravel = 0.2-6 cm and sand <2 mm). Mean sizeof the natural substratum at Site 1 and 2 was 62% and69% cobble and 25% and 26% pebble-gravel, respec-

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Table 1. Results of the two-way (substratum type and colonization period) ANOVA andStudent-Newman-Keuls (SNK) tests for the densities of the most abundant taxa andthe total number of organisms (n=5) on the single rock (R) and brick (K) particles,substratum baskets (B) and the natural substratum (N) at Site 1 and 2. Statisticaldifferences (P < 0.05) in the SNK test are separated into groups from the greatest toleast (High-Low) density.

Taxonomic Substratum type Colonization period(B, R, K, N) (1, 8, 29 day)

Group F value SNK F value SNK(High-Low) (High-Low)

Site 1Chironomidae 9.86* N-BKR 1.56Baetis 8.69* N-BKR 6.71* 8,29-1Hydropsyche 12.57* N-BKR 0.07Cheumatopsyche 21.75* N-B-KR 0.45Oecetis 48.96* N-BRK 2.30Acari 58.99* N-BRK 2.40Ameletus 8.75* BN-NK-R 2.42

Total no. of organisms 105.64* N-B-KR 8.17* 29, 8-1

Site 2Chironomidae 7.78* N-BRK 1.90Baetis 14.34* N-BR-K 12.78* 8, 29-1Cheumatopsyche 18.27* N-B-KR 2.71Acari 21.75* N-BRK 1.35Hydropsyche 11.42* N-B-KR 2.44Ameletus 7.14* B-NKR 7.30* 29-1, 8Oecetis 50.18* N-RBK 5.01* 8-1, 29

Total no. of organisms 136.64* N-B-R-K 20.67* 29-8-1

*=P<0.05

tively; remaining substratum was boulder and sand.Both Site 1 and 2 were subdivided into a 4 x 4 matrix,and the artificial substratum types were arranged ran-domly in 15 of the 16 matrix cells. Macroinvertebratecolonization was determined on five replicates of eachartificial substratum type after they were in situ for1, 8 and 29 days at Site 1 and 2. To determine theeffect of the natural cover of fine sediment on col-onization, the epilithic cover only was cleaned fromthe single rock particles and cobble and pebble in thesubstratum baskets at Site 1 and not at Site 2. To deter-mine the macroinvertebrate fauna on the undisturbednatural substratum five samples were taken after eachcolonization period in randomly selected sites 1-2 mdownstream of the artificial substrata at Site 1 and 2.The natural substratum was sampled with a modifiedNeill sampler (Neill, 1938), which is a stainless steelcylinder-shaped sampler (sample area= 0.091 m2 ) with

a net (pore size = 0.210 mm, length of net = 0.9 m) andsample bottle attached. Organisms and epilithic materi-al were removed by hand from the substratum enclosedby the Neill cylinder to a depth of about 10 cm.

Disturbance to the natural substratum at the studysites was minimized. Artificial substrata were installedfrom upstream to downstream sites and both artificialand natural substratum samples were taken beginningat downstream sites. The artificial substrata were posi-tioned, about 0.1 m apart so that the upper surfacewas flush with the surface of the natural substratum.The substrata were retrieved while holding a net (poresize=0.210 mm, net opening=30 x 30 cm, lengthof net = 1 m) immediately downstream. A three-sidedshovel (28 x 28 x 10cm) was scooped under each sub-stratum basket before it was removed. At the shore,organisms and detritus in the samples were removed

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from the net and substratum and the sample was pre-served in 85% ethanol.

In the laboratory, the samples were divided intocoarse (>1.18 mm) and fine (<1.18 to >0.210 mm)fractions using sieves. In the fine fraction, Chironomi-dae larvae were subsampled based on the subsamplingprocedure of Wrona et al. (1982). The larvae werecounted in a minimum of two subsamples until > 100organisms were obtained; number of larvae per sam-ple was estimated from the subsamples. Macroinverte-brates were identified and counted at >60 x magnifi-cation. Organic material (>0.210 mm) in each samplewas measured by separating it from the sample byelutrition and drying it to a constant weight at 60 C.

Statistical analyses

Numbers of macroinvertebrates per sample were con-verted to densities (no. of organisms m- 2 ) using sur-face area of each substratum particle or surface areasampled for the substratum baskets and Neill cylin-der sampler. Density data (x + 1) were log transformedto obtain equal variances; plots of mean and variancedemonstrated that dependence of the mean on variancewas eliminated or reduced. Two or three-way analysisof variance (ANOVA) tests were used to determine sta-tistically significant differences in the densities of themost abundant macroinvertebrate taxa and total num-ber of organisms among treatment factors (substra-tum type, colonization period and presence of epilithiccover). Interactions among the treatment factors in theANOVA tests were determined. The Student-Newman-Keuls multiple comparison test was used to determinethe levels of treatment factors that were statisticallydifferent. The Spearman rank correlation test was usedto determine similarities between the relative abun-dance of the 10 most abundant taxa on pairs of theartificial substratum types and natural substratum. Sta-tistical analyses were conducted using the SAS/STATsoftware package (SAS Institute Inc., 1988).

Results

Comparisons among artificial substratum types andnatural substratum

Densities of total number of organisms and the sevenmost abundant taxa were statistically greater on thenatural substratum than on the artificial substrata atboth Site 1 and 2 (Table 1, Figure 1). Only two of

Table 2. Results of the Spearman rank correlationtests for the ten most abundant taxa between pairs ofthe natural and artificial substratum types.

Study site Substratum Spearman Rank

comparison CorrelationCoefficient (rs)

1 Brick-Natural 0.404

2 Brick-Natural 0.583

1 Rock-Natural 0.445

2 Rock-Natural 0.620

1 Basket-Natural 0.689*

2 Basket-Natural 0.602

1 Brick-Rock 0.619

2 Brick-Rock 0.905*

1 Brick-Basket 0.656*

2 Brick-Basket 0.979*

1 Rock-Basket 0.859*

2 Rock-Basket 0.854*

*=P<0.05

16 interactions between substratum type and coloniza-tion period were significant (Site 1: Baetis - P = 0.041,Ameletus - P =0.006) indicating the treatments wereindependent of each other for most taxonomic groups.Total number of taxa in all samples combined for eachsubstratum type (n = 15) were greater on the naturalsubstratum (Site 1 and 2 = 33 taxa) than on substratumbaskets (Site 1 = 27, Site 2 = 28 taxa) or the single rock(Site 1 = 14, Site 2 = 20 taxa) and brick (Site 1 = 20,Site 2 = 18 taxa) particles. Relative abundances of theten most abundant taxa on pairs of the artificial sub-stratum types, unlike pairs of each artificial substratumtype and the natural substratum, were statistically cor-related (with one exception) at Site 1 and 2 (Table 2).

Statistical differences among the densities ofmacroinvertebrates on the three artificial substratumtypes were analysed separately from the natural sub-stratum because of large differences in densities ofthe zoobenthos on these substrata (Figure 1). Colo-nization by total number of organisms and about one-half of the most abundant taxa were at greater den-sities on the substratum baskets compared to otherartificial substrata; three of these taxa, Chironomidae(Diptera), Cheumatopsyche (Trichoptera) and Amele-tus (Ephemeroptera) larvae, were at greater densities

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Table 3. Results of the two-way (substratum type and colonization period) ANOVA andStudent-Newman-Keuls (SNK) tests for the densities of the seven most abundant taxa and thetotal number of organisms (n=5) on the single rock (R) and brick (K) particles and substratumbaskets (B) at Site 1 and 2. Statistical differences (P < 0.05) in the SNK test are separatedinto groups from the greatest to least (High-Low) density.

Taxonomic Substratum type Colonization period(B, R, K, N) (1, 8, 29 day)

Group F value SNK F value SNK(High-Low) (High-Low)

Site 1

Chironomidae 5.93* B-KR 4.91* 29-8,1Baetis 1.05 6.36* 8,29-1Hydropsyche 3.00 0.09Cheumatopsyche 5.49* B-KR 1.38Oecetis 1.83 0.43Acari 1.80 3.40* 29,8-8,1Ameletus 13.04* B-K-R 4.46* 8,29-1

Total no. of organisms 15.26* B-KR 8.71* 29, 8-1

Site 2

Chironomidae 9.01* B-RK 11.67* 29-8,1Baetis 6.96* BR-RK 12.86* 8, 29-1Cheumatopsyche 9.24* B-RK 3.50* 29,1-1,8Acari 1.08 1.62Hydropsyche 5.35* B-KR 3.06Ameletus 11.30* B-KR 7.18* 29-8, 1Oecetis 1.68 2.83

Total no. of organisms 41.01* B-R-K 25.37* 29-8-1

* =P<0.05

on the substratum baskets at both Site 1 and 2 (Table 3).Only one of 16 statistical interactions between sub-stratum type and colonization period was significant(Site 1: Ameletus - P = 0.038).

Quantity of organic material (n=15) was great-est on the natural substratum (Site 1 and 2:mean=7.16, SDEV= 1.74 mg/sample) than on thesubstratum baskets (Site 1: mean = 3.21, SDEV = 1.93;Site 2: mean=4.66, SDEV=2.67 mg/sample) orthe single rock (Site 1: mean=0.13, SDEV=0.10;Site 2: mean=0.36, SDEV=0.24 mg/sample) andbrick (Site 1: mean=0.30, SDEV=0.31; Site 2:mean = 0.19, SDEV = 0.16 mg/sample) particles.

Effect of fine sediment on colonization

Total number of organisms and the most and least com-mon of the seven most abundant taxa (Chironomidaeand Ameletus larvae, respectively) were at about two

to six-fold greater densities on the substrata with finesediment compared to clean substratum. The effectof sediment, substratum type and colonization peri-od on densities of most taxa were mostly independentof each other. Only two of 33 statistical interactionswere significant (for Baetis - P = 0.014 and Ameletus- P = 0.001 between substratum type and colonizationperiod).

Comparisons among colonization periods

Densities of total number of organisms and about one-half or less of the taxa at Site 1 and 2 were statisticallydifferent among colonization periods (Tables 1 and 3).For most taxa there were greater densities on the sub-strata after 8 and 29 days than after 1 day (Tables 1 and3).

SITE 112000

10000

8000

E

z

z

UI

6000

4000

2000

0

1 8 29

SITE 2I ZUUU

10000

8000

6000

4000

2000

0

1 8 29

COLONIZATION PERIOD (DAY)

I I BRICKM BASKET

_ ROCKI NEILL

Figure 1. Mean density and standard error (n = 5) of total number oforganisms on artificial substratum types and natural substratum aftereach colonization period. See text for details.

Discussion

Comparisons among artificial substratum types andnatural substratum

Macroinvertebrate assemblages showed consistent dif-ferences on the artificial substratum types and naturalsubstratum. Greater densities of each taxon, total num-ber of organisms and total number of taxa were onthe natural substratum. Among the artificial substra-tum types these same characteristics of the zoobenthosassemblages were greater on the substratum basketsthan on the single rock or brick particles. These dif-ferences in zoobenthos densities were probably caused

by several factors, including the method of estimat-ing density of organisms, physical heterogeneity ofthe substrata and the quantity of organic material andepilithic cover on the substratum.

Densities of macroinvertebrates on the single brickand rock particles were based on the surface area ofeach particle. In contrast, densities of organisms onthe substratum baskets and natural substratum werebased on the area of substratum sampled and not thesurface area of individual particles. Therefore, densi-ties of organisms on the substratum baskets and naturalsubstratum were overestimates relative to the singlerock and brick particles. Other studies that comparedthe colonization of containers of substratum (baskets ortrays) to natural substratum have also reported densi-ties based on sample area (Minshall & Minshall, 1977;Shaw & Minshall, 1980; Ciborowski & Clifford, 1984;Clements, 1991). Investigators of these studies prob-ably did not measure surface area of each substratumparticle in the samples because of the considerable timeand resources required.

In our study there were few differences betweendensities, relative abundances, or total numbers of taxaon the single brick and rock particles. This result wasprobably caused by the similarity in the physical het-erogeneity and quantity of organic material on thesesubstrata. Similar results were found in other loticstudies. Lake & Doeg (1985) found few differencesbetween densities of most macroinvertebrate taxa andsimilar numbers of species after 29 days on singlerock particles from a river or quarry. Lamberti & Resh(1985) found similar macroinvertebrate densities andspecies after 28 days on single particles of natural rock,sterilized natural rock and unglazed clay tile.

No previous artificial substratum studies have com-pared colonization by macroinvertebrates on singleparticles to substrata of many particles. We found nodifference in relative abundances of the most abun-dant taxa and densities of almost one-half of the taxabetween the single substratum particles and substratumbaskets. This result indicates that single substratumparticles instead of substratum baskets might be usedto sample the zoobenthos. Using single substratum par-ticles would substantially reduce the time required toprepare the substrata and process samples in the fieldand laboratory.

Unlike the studies comparing single substratumparticles there were differences in the zoobenthosassemblages on the substrata of many particles (i.e.,with greater physical heterogeneity). In our study den-sities of each taxon (with the exception of Ameletus),

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total number of organisms and total number of taxawere greater on the natural substratum than on sub-stratum baskets. Other experimental studies compar-ing macroinvertebrate colonization of substratum con-tainers to natural substratum, however, have shownvarious results, depending on the characteristic of thezoobenthos assemblage measured. In contrast to ourresults, several studies have shown greater abundancesof macroinvertebrates on natural substratum in contain-ers than on the undisturbed natural substratum (Min-shall & Minshall, 1977; Shaw & Minshall, 1980;Ciborowski & Clifford, 1984; Clements, 1991). Inagreement with our results Clements (op. cit.) found agreater number of taxa on natural substratum than onsubstratum trays. Shaw & Minshall (op. cit.), howev-er, found similar numbers of taxa on substratum traysand natural substratum and Ciborowski & Clifford (op.cit.) found more taxa on substratum baskets. Final-ly, relative abundances of taxa on substratum contain-ers and natural substratum showed little correlation inmost studies (Minshall & Minshall, op. cit.; Shaw &Minshall, op. cit.; Ciborowski & Clifford, op. cit.),with the exception of one study (Clements, op. cit.).These results show macroinvertebrate assemblages onthe substratum containers, that had similar physicalcharacteristics to natural substratum, do not necessar-ily represent the fauna on the natural substratum andthat physical heterogeneity alone did not cause the dif-ferences in the fauna between substratum containersand natural substratum.

Greater quantities of organic material (approxi-mately 10-fold or greater increase) on the natural sub-stratum and substratum baskets relative to the singlebrick and rock particles was probably caused by thegreater surface area and physical heterogeneity of thesesubstrata. The organic material, that was mostly wholeand partially decomposed leaves, likely affected col-onization of the substrata by some macroinvertebratetaxa as a source of food or as a suitable habitat.

Effect offine sediment on colonization

The thin layer of fine sediment affected colonization ofthe substratum by two macroinvertebrate taxa. Resultsof other studies have shown various effects of light silt-ing (< 1 mm) on colonization by macroinvertebrates,whereas, heavy silting (> 1 mm) generally caused low-er insect species diversity and productivity (Minshall,1984). Cummins & Lauff (1969) found the additionof a thin layer of silt caused no effect on the abun-dance of most taxa and an increase in the abundance of

some taxa in the interstices. Rabeni & Minshall (1977)found the addition of a thin layer (about 1 mm) of siltreduced the number of only three macroinvertebratetaxa on the substratum. Unlike these other studies thesediment was already present on our substratum andit probably included a natural biofilm and fine detritusthat would provide food for some zoobenthos, such asChironomidae and Ameletus larvae in our study.

Comparisons among colonization periods

Increases in the densities of several taxa and total num-ber of organisms on the artificial substratum types werefound after longer colonization periods. Colonizationtime, however, did not affect our results because con-sistent patterns in densities of the zoobenthos on thesubstratum types were found after each colonizationperiod.

Conclusions

In our study all measures of the macroinvertebrateassemblages (densities of each taxon, total numberof organisms, total number of taxa and relative abun-dances of taxa), with few exceptions, were differentbetween each artificial substratum type and the nat-ural substratum. This result showed the abundance andcomposition of the macroinvertebrate fauna on the arti-ficial substratum types were different from the naturalsubstratum. Therefore, the choice of using artificialsubstrata instead of direct sampling of the natural sub-stratum should be carefully made. Among the artificialsubstratum types relative abundances of taxa were sim-ilar on the single substratum particles and substratumbaskets indicating single particles instead of basketsmight be used (if densities or number of taxa are notof concern) to sample the zoobenthos. Investigatorsusing artificial substrata should consider the potentialeffect of the natural epilithic cover on colonization byzoobenthos when choosing the type of substratum.

Acknowledgments

We are grateful to S. Melenka for measuring the dryweights of organic material in the samples and H. Clif-ford and J. O'Donovan for providing helpful commentson the manuscript.

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