Missing:
Springer 2005
Hydrobiologia (2005) 539:121–130 DOI 10.1007/s10750-004-3914-3
Primary Research Paper
Characterizing macroinvertebrate assemblage structure in relation to stream size and tributary position Jani Heino1,*, Juha Parviainen2, Riku Paavola3, Michael Jehle2, Pauliina Louhi4 & Timo Muotka2,5 1
Finnish Environment Institute, Research Programme for Biodiversity, P.O. Box 413, FIN-90014 University of Oulu, Finland 2 Department of Biology, P.O. Box 3000, FIN-90014 University of Oulu, Finland 3 Department of Zoology, University of Toronto, Toronto, ON M5S 3G5, Canada 4 Finnish Game and Fisheries Research Institute, Tutkijantie 2 A, FIN-90570 Oulu, Finland 5 Finnish Environment Institute, Research Department, P.O. Box 140, 00251 Helsinki, Finland (*Author for correspondence: E-mail: jani.heino@ymparisto.fi) Received 25 September 2003; in revised form 27 August 2004; accepted 28 September 2004
Key words: assemblage structure, benthic macroinvertebrates, biodiversity conservation, functional feeding groups, lotic communities, streams
Abstract We examined the variability of macroinvertebrate assemblage structure, species identities, and functional feeding group composition in relation to stream size, tributary position, and in-stream factors in a boreal watershed in Finland. Our study included three riffle sites in each of three stream sections in each of three stream size classes. Multi-response permutation procedure, indicator value method, and canonical correspondence analysis revealed clear differences in assemblage structure among the stream size classes, with a gradual increase of species richness as the stream size increased. Significant differences in assemblage structure were also found among the tributary river systems. The functional feeding group composition broadly followed the river continuum concept, i.e., headwaters were dominated by shredders, gatherers, or filterers, whereas scrapers increased in relative abundance with stream size. There was, however, considerable variation in the functional feeding group composition both among and within the headwater stream sections. Our findings refer to a strong influence of stream size on macroinvertebrate assemblages, but also factors prevailing at the scale of individual riffles should be considered in biodiversity conservation of lotic ecosystems.
Introduction Successful conservation of biodiversity requires the identification of regionally representative sets of key habitats and associated biological communities, thereby creating a need for extensive biodiversity inventories. Extensive inventories of biological communities in several regions are, however, costly in terms of money and effort. A cost-effective alternative for extensive surveys is to develop predictive models of community–
environment relationships in a few well-examined regions, and to apply such information for conservation planning in more poorly-known regions (Angermeier & Winston, 1999). Such predictive models should incorporate information on both taxonomic and functional components of biodiversity. In this regard, streams are particularly challenging, given that their biodiversity is affected by (i) longitudinal processes along the stream size gradient, (ii) lateral interactions with the surrounding landscape, and (iii) within-stream vari-
122 ability at the scale of stream sections and microhabitats (Allan, 1995; Ward, 1998). Viewing stream communities in the holistic context of drainage systems has been a major research approach in stream ecology, and it has led to the generation of many influential hypotheses about the organization of stream communities. The river continuum concept (RCC) (Vannote et al., 1980; Minshall et al., 1985) in particular has attained a central position in stream ecology, although its global applicability has also been questioned (Winterbourn et al., 1981; Statzner & Higler, 1985). The RCC predicts, for example, that the functional feeding group composition of macroinvertebrate assemblages should shift from the shredder-dominated headwaters via scraperdominated middle reaches to the collector-dominated lower reaches of large rivers (Vannote et al., 1980; Minshall et al., 1983). Furthermore, species richness should peak in the middle reaches of large rivers, where high environmental heterogeneity enables the co-occurrence of species with widely differing niche requirements (Minshall et al., 1985; Grubaugh et al., 1996; Vinson & Hawkins, 1998). While the RCC mainly relates biotic changes to parallelling variation in the productivity base, other conceptual approaches associate such changes to stream hydraulics (e.g., Statzner & Borchardt, 1994), or stress the effects of stream position in terms of downstream confluences on biotic patterns along the river continuum (e.g., Osborne & Wiley, 1992). The spatial position and in-stream/riparian characteristics of a riffle site may also have considerable effects on macroinvertebrate assemblage structure. For instance, sites in different tributaries within a drainage system may differ sharply in water chemistry and physical habitat characteristics, leading to corresponding differences in stream biota (Townsend et al., 1983; Ormerod & Edwards, 1987; Carter et al., 1996; Paavola et al., 2000). Furthermore, even neighbouring riffles within a stream may differ considerably in habitat conditions and benthic assemblage structure (e.g., Downes et al., 1993). However, although several studies have reported predictable patterns in the distribution of biota along the river continuum, the degree to which variation in macroinvertebrate assemblage structure among and within streams confounds longitudinal patterns within a drainage
system has gained little attention (Li et al., 2001; Wright & Li, 2002; Parsons et al., 2003; Heino et al., 2004). Our objective was to examine the degree to which macroinvertebrate assemblages in a boreal drainage system correspond to predictions of the RCC, and whether different stream size classes and tributary river systems differ in faunal attributes, i.e., assemblage structure, species identities, and functional feeding group composition. Furthermore, we examined the relationships between assemblage structure and riffle-scale environmental variables to determine whether local riffle characteristics could confound longitudinal patterns along the river continuum.
Materials and methods Study area and study design The study was conducted in the River Kiiminkijoki drainage system (65 N, 26 E) in Finland (Fig. 1). Bedrock in the study area mainly consists of greywacke, mica schist, and quartzite. The forests are dominated by coniferous trees, mainly Scotch pine (Pinus sylvestris L.) and Norwegian spruce (Picea abies L.). Typical deciduous vegetation along river courses consists of birch (Betula pubescens Ehrh. and Betula pendula Roth), buckthorn (Rhamnus frangula L.), alder (Alnus incana L.), willows (Salix spp.), birdcherry (Prunus padus L.), and aspen (Populus tremula L.). Due to the extensive occurrence of peatlands in the watershed, stream water is slightly acidic, with high concentrations of humic substances and nutrients (Table 1). Our study incorporated samples from 27 riffle sites (Fig. 1). The sites were divided into three size classes: we thus sampled three riffles from each of three headwater streams (1st and 2nd orders), three riffles in each of the three mid-sized rivers (3rd order), and three riffles in each of three main channel sections (5th order). The 18 riffles in the headwater streams and mid-sized rivers represented three separate tributaries (Fig. 1). Field and laboratory procedures Sampling was conducted in late September 1999. We randomized the order in which the streams
123
Figure 1. Location of the study sites in the Kiiminkijoki drainage system. MCa, MCb, and MCc refer to main channel sections. Riffles of different size classes are denoted by different colours: black squares ¼ large (5th order); dark grey squares ¼ mid-sized (3rd order); light grey squares ¼ small (1st and 2nd orders).
were sampled. At each riffle site, we quantified habitat variables at 40 plots. Each plot had a surface area of 0.04 m2 (20 · 20 cm). We measured depth and current velocity (0.4 · depth), and estimated the cover of macrophytes and mosses in each plot. Furthermore, the sizes of two randomly selected stones were recorded for each plot. Substratum size was determined by measuring three perpendicular dimensions of each stone, and stone surface area was subsequently calculated following Graham et al. (1988). Ten benthic invertebrate samples were taken at each riffle site. Samples were taken using a stratified random sampling protocol: transects were placed regularly across the riffle, and two to five plots were placed randomly in each transect, depending on stream width. Sampling was conducted using a Surber sampler (20 · 20 cm, net mesh size 0.3 mm). All samples from a riffle site were pooled, and thus variability at smaller, within-riffle scales will not be considered here. The invertebrates sampled were identified to the lowest possible taxonomic level, mainly species or genus level, and invertebrates were subsequently classified into functional feeding groups according to Merritt & Cummins (1996) and our own observations of invertebrate gut contents (J. Heino et al., unpublished data). Data analysis Overall differences in assemblage structure among riffles of different stream size classes and among
different tributaries were examined using multiresponse permutation procedure (MRPP). MRPP is a non-parametric alternative to discriminant function analysis, aiming to reveal whether a priori determined groups [in this case, (i) size classes and (ii) tributaries when the main channel sites were omitted] differ in assemblage structure (McCune & Mefford, 1997). The null hypothesis of no difference among groups was tested by a Monte Carlo randomization test. Following MRPPs, we used the indicator value method (IndVal) of Dufrene & Legendre (1997) to identify species discriminating among the a priori groups. The indicator value varies from 0 to 100, attaining its maximum value when all individuals of a species occur at all sites of a single group (Dufrene & Legendre, 1997). The significance of the indicator values for each species was tested by the Monte Carlo randomization test. For both MRPP and IndVal, 1000 Monte Carlo permutations were run using PC-Ord (McCune & Mefford, 1997). Canonical correspondence analysis (CCA) was used to examine which environmental factors best accounted for variation in assemblage structure among the riffles. CCA is one of the most commonly used constrained ordination methods that analyses both species and environmental data by combining ordination and multiple regression (Ter Braak & Prentice, 1988; Legendre & Legendre, 1998). Stepwise selection of environmental variables was used to obtain a reduced set of significant explanatory variables, and the significance of the relationship between environmental
124 Table 1. Average chemical and physical characteristics of the stream sections studied in the River Kiiminkijoki drainage system. R1, R2, and R3 refer to different tributary river systems. MCa, MCb, and MCc refer to different main channel sections (Fig. 1) Size
Small
Mid-sized
Section
Na¨sia¨oja Haaraoja Loukonoja (R1) (R2) (R3)
Juuanjoki
Jolosjoki
Onkamonoja
(R1)
(R2)
(R3)
Tributary Stream order Shading (%) Stream width (m)
2 44 2.0
Large MCa
MCb
1
2
3
3
3
5
5
61 2.3
73 1.0
22 4.3
24 6.8
42 5.0
0 52.0
0 67.0
0 83.0 12.0
Discharge (m3 s)1)
0.03
0.11
0.06
0.12
0.42
0.22
11.9
11.9
pH
6.5
5.7
6.1
6.6
6.2
5.9
6.5
6.5
Total N (lg L)1) Total P (lg L)1) Colour (mg Pt L)1)
600
750
610
820
790
13
26
20
15
32
200
280
240
160
280
3.4
6.4
Conductivity (mS m)1)
5.0
MCc
3.2
variables and species data was tested at each step using the Monte Carlo randomization test with 1000 permutations. Separate analyses were performed for the size class (27 sites) and tributary (18 sites, main channel sites omitted) comparisons. Species occurring only at a single site were omitted from both analyses. CCAs were run using CANOCO version 4.0 (Ter Braak, 1998). PC-ORD was used to plot the abundance variation of significant indicator species found by IndVal on the CCA ordination biplots.
4.3
520
460
17 200 2.8
5
6.6
460
450
26
26
24
150
150
160
3.1
3.1
3.7
Results A total of 101 operational macroinvertebrate taxa (hereafter called species) were found from the riffle sites sampled. MRPP revealed significant differences in assemblage structure among the size classes (R ¼ 0.233, p < 0.001). Pairwise tests indicated significant differences between riffles in smalll and mid-sized (R ¼ 0.141, p < 0.001), small and large (R ¼ 0.220, p < 0.001), and midsized and large streams (R ¼ 0.204, p < 0.001).
Table 2. Summary of indicator value analysis for the stream size class comparison. Shown are the 14 species with highest indicator values. Indicator values were calculated based on the relative abundance and frequency of occurrence of each species among the a priori groups. All indicator values were significant at p < 0.001 Species
Small
Mid-sized
Large
Baetis niger (Linnaeus)
6
71
0
Baetis digitatus Bengtsson
0
6
80
Leptophlebia marginata (Linnaeus)
74
0
2
Ephemerella mucronata Bengtsson
0
3
82
Caenis rivulorum Eaton Leuctra hippopus Kempny
0 0
0 81
67 5
Capnopsis schilleri (Rostock)
0
66
0
Hydropsyche siltalai Do¨hler Arctopsyche ladogensis (Kolenati)
0
2
95
0
0
77
Cheumatopsyche lepida (Pictet)
0
0
100
Psychomyia pusilla (Fabricius)
0
0
97
Agapetus ochripes Curtis
0
13
79
Lepidostoma hirtum (Fabricius) Ancylus fluviatilis (Linnaeus)
0 0
7 0
90 100
125
Figure 2. Biplot of CCA for the relationship between environmental variables and assemblage structure of the riffle sites: size-class comparison. Riffles of different size classes are represented by different colours: black squares ¼ large (5th order); dark grey squares ¼ mid-sized (3rd order); light grey squares ¼ small (1st and 2nd orders). Abbreviations: PS ¼ particle size, MC ¼ moss cover, MP ¼ macrophyte cover, W ¼ riffle width. Also shown are selected indicator species found by IndVal analysis for each size class, and their relative abundance variation among the riffles. The smallest squares denote the absence of a species at a site.
Similarly, macroinvertebrate assemblage structure exhibited significant, albeit weaker, differences among the three tributaries (R ¼ 0.126, p ¼ 0.002). Pairwise tests showed that tributary 1 differed significantly from tributary 2 (R ¼ 0.109, p ¼ 0.019) and from tributary 3 (R ¼ 0.129, p ¼ 0.007), whereas tributary 2 did not differ significantly from tributary 3 (R ¼ 0.059, p ¼ 0.068). IndVal yielded further insight into the differences among the a priori groups. No species appeared confined to small streams, whereas several
species discriminated the riffles of the mid-sized and the large rivers from the others (Table 2, Fig. 2). For instance, the mayfly Baetis niger and the stoneflies Leuctra hippopus and Capnopsis schilleri had high indicator values for the mid-sized rivers. The mayflies Baetis digitatus, Ephemerella mucronata, and Caenis rivulorum, the caddisflies Hydropsyche siltalai, Arctopsyche ladogensis, Cheumatopsyche lepida, Psychomyia pusilla, Agapetus ochripes, Lepidostoma hirtum, and the snail Ancylus fluviatilis had high indicator values and
126 Table 3. Summary of indicator value analysis for the tributary comparison. Shown are the eight species with the highest indicator values. All indicator values were significant at p < 0.05. R1, R2, and R3 refer to different tributary river systems (Fig. 1) Species
R1
R2
R3
Baetis vernus group
0
3
56
Heptagenia sulphurea (Mu¨ller) Ephemerella mucronata Bengtsson Nemoura cinerea (Retzius)
0
21
69
0 6
0 92
67 0
Isoperla difformis (Klapalek)
3
9
84
Rhyacophila nubila (Zetterstedt)
14
54
33
Lepidostoma hirtum (Fabricius)
3
66
8
Atherix ibis (Fabricius)
2
16
79
showed strong preference for the large river riffles. Only the mayfly Leptophlebia marginata had a high indicator value for small streams, but this species also occurred in some large river riffles (Table 2). By contrast, only eight species had significant indicator values in the tributary river system comparison. Most of these species were either absent from or had low abundances in tributary 1. Only the mayfly Ephemerella mucronata was restricted to a single tributary, whereas all other indicator species also occurred in low abundance/low frequency in the other two tributaries (Table 3, Fig. 3). CCA with all 27 sites included had eigenvalues of 0.257, 0.076, and 0.074 for the first three axes, respectively (Table 4). Four environmental variables were selected by the forward selection procedure. Thus, variation in species composition along axis 1 was strongly related to riffle width, mirroring the overriding influence of stream size. The second axis was related to particle size and macrophyte cover (Fig. 2), and the third axis to particle size and moss cover. The relationship between assemblage structure and environmental variables was significant for both the first CCA axis and the overall analysis (Monte Carlo test with 1000 permutations, p ¼ 0.005). When the riffles of the largest size class (main channel, 5th order sites) were omitted from the analysis, the eigenvalues were 0.262, 0.094 and 0.059 for the first three axes, respectively (Table 5). Three variables were significantly related to the assemblage structure in this analysis. The first axis was strongly related to riffle width, the second one to
moss cover (Fig. 3), and the third one to particle size and moss cover. Both the first axis and the overall analysis were significant (Monte Carlo test, 1000 permutations, p ¼ 0.005). In the CCA biplot, riffles in mid-sized rivers (3rd order streams) were clearly separated from riffles in small stream (1st and 2nd order stream) (Fig. 3). Relative abundances of functional feeding groups showed considerable variation within and among size classes and tributaries (Fig. 4). Along the size gradient, the clearest pattern was the increase in the proportion of scrapers from headwaters to large river riffles. Headwater assemblages were generally variable, being dominated by either shredders, filterers, or gatherers. No clear differences were observed among the tributaries, mainly due to the inclusion of two size classes from each tributary and the variation among riffles within each section (Fig. 4).
Discussion The river continuum concept (RCC) predicts that macroinvertebrate assemblages change gradually from headwaters to large rivers downstream (Vannote et al., 1980). For instance, the relative proportions of functional feeding groups should change from the shredder-dominated headwaters to the collector-dominated lower reaches of large rivers. Furthermore, scrapers should attain highest abundances in the middle reaches of large rivers. These connotations broadly applied to our study system, considering that our largest sites were in a 5th order river. Headwater streams were either dominated by shredders, gatherers, or filterers, while scrapers occurred in only low abundance. By contrast, our 3rd to 5th order riffles were characterized by an increase of scraper abundance, likely following the decrease in canopy cover (see Vannote et al., 1980; Hawkins et al., 1982). Furthermore, in the large river sites (5th order), macroinvertebrate abundances were more evenly distributed among different functional feeding groups. Nevertheless, considerable variation in functional feeding group composition was found among riffles within a stream, especially in headwater streams, suggesting that the characteristics of a riffle site exert a strong control over functional
127
Figure 3. Biplot of CCA for the relationship between environmental variables and assemblage structure of the riffle sites: tributary comparison where the main channel sites were excluded. Riffles in different tributaries are represented by different colours as follows: black squares ¼ tributary 1; dark grey squares ¼ tributary 2; light grey squares ¼ tributary 3. Mid-sized riffles (3rd order) are encircled by a dashed line, others are headwater riffles (1st and 2nd orders). Also shown are the indicator species found by IndVal analysis for each river system, and their relative abundance variation among the riffles.
feeding group composition. The riffle sites varied with regard to the distance to upstream lakes, the retention capacity, and the amount of riparian inputs, thereby likely influencing filterer and shredder abundances. Furthermore, riffles differed greatly in moss cover, which also directly relate to the retention capacity of the streambed (Muotka & Laasonen, 2002). Such local effects may lead to deviations from the expectations of the RCC for streams of a certain
order (Naiman et al., 1987; Grubaugh et al., 1996). Stream size was the major factor influencing the taxonomic structure of macroinvertebrate assemblages in our study, concurring to earlier findings from both temperate and boreal streams (e.g., Hildrew & Giller, 1994; Malmqvist & Ma¨ki, 1994; Malmqvist & Hoffsten, 2000). In general, more taxa were added as stream size increased, and no species appeared to be restricted to the headwa-
128 Table 4. Results of CCA for the relationship between assemblage structure and riffle-scale environmental variables, with all 27 sites included. Total inertia was 1.320, and the sum of all canonical eigenvalues was 0.458. Coefficients of the intraset correlations among the environmental variables and the CCA axes are also shown Axis 1
Axis 2
Axis 3
Eigen value Variation explained %
0.257 19.5
0.076 5.7
0.074 5.6
Particle size
)0.139
0.686
)0.699
Riffle width
0.997
0.073
0.023
Moss cover
0.009
0.262
)0.887
Macrophyte cover
)0.099
)0.564
)0.374
ters. By contrast, mid-sized riffles had several mayfly species absent from the headwaters, a pattern likely related to the fact that most mayflies in our system were scrapers. Similarly, the large river sites harboured several species of filtering caddisflies and grazing snails that were absent from the headwaters and occurring only sporadically in mid-sized streams. A similar continual
change in the species distributions for filtering caddisflies has been reported elsewhere, being related to the interaction of current velocity, food supply, and the mesh size of the filtering nets (e.g., Ross & Wallace, 1983). Based on the spatial proximity, one would easily envisage that macroinvertebrate assemblages in riffles from the same tributary river system or stream should resemble each other more than riffles in other systems (see Parsons et al., 2003). In our study, there was wide variation in benthic assemblages among the headwaters and the mid-sized sections within each tributary river system, and especially among riffles within the headwater streams (Fig. 3). These findings suggest that even riffles separated by a distance of only a few hundred metres may harbour macroinvertebrate assemblages with highly variable structure, thus cautioning against generalizations based on samples from a single riffle (see also Downes et al., 1993; Heino et al. 2004). Although neighbouring riffles within a stream are unlikely to exhibit considerable differences in species identities, the relative and absolute abundances of species may vary
Figure 4. Relative abundances of macroinvertebrate functional feeding groups in the three riffle sites of each stream section.
129 Table 5. Results of CCA for the relationship between assemblage structure and riffle-scale environmental variables, with the main channel sites excluded. Total inertia was 1.079, and the sum of all canonical eigenvalues was 0.416 Axis 1
Axis 2
Axis 3
Eigen value
0.262
0.094
0.059
Variation explained %
24.3
8.8
5.5
Particle size
0.560
)0.082
)0.825
Riffle width
)0.954
0.284
0.094
Moss cover
0.292
)0.736
)0.611
drastically according to local conditions. Thus, environmental filters (sensu Poff, 1997) prevailing at the reach-scale (e.g., stream size) may largely determine species distributions within a drainage system, while their ultimate success in terms of local abundance is determined at the among- and within-riffle scales. The gradual change in assemblage structure along the stream size gradient suggest that a satisfactory conservation of benthic fauna might be achieved by preserving large river riffles. Nevertheless, other factors should also be considered when planning for conservation programs at the level of whole drainage systems. For instance, headwater streams may act as source habitats for some species occurring also in large rivers (e.g., Angermeier & Winston, 1997). Thus, if headwaters remain unprotected from habitat degradation, several species may be threatened or even lost from the drainage system. Furthermore, although we found very few indicator species for the headwater streams in our study system, small streams often contain regionally rare species, and rare assemblage types not typically found in larger rivers (Wright et al., 1998; Furse, 2000; Malmqvist & Hoffsten, 2000). For example, chironomid midges are by far the most diverse group of benthic macroinvertebrates in boreal headwaters (Heino et al., 2003), yet little is known about their habitat requirements. Several chironomids and other ‘cryptic’ taxa may well be restricted to headwater streams, thereby increasing their potential conservation value. Furthermore, because headwaters contribute importantly to the ecological integrity of whole drainage systems, it has been suggested that headwaters should be regarded as key zones for focusing
conservation efforts in freshwater ecosystems (Saunders et al., 2002). In any case, it appears that stream conservation planning should be based on size-class stratification, because stream size is clearly a key environmental gradient determining the functional and taxonomic biodiversity of lotic macroinvertebrate assemblages.
Acknowledgements We thank P. Tikkanen for originally suggesting the study idea to us. The efforts of A. Huhta, J. Kurppa, T. Lahdenpera¨, and P. Tikkanen during the demanding field work are also greatly appreciated. J. Ylo¨nen organized the sorting of the invertebrate samples. This paper is part of the Finnish Biodiversity Research Programme (FIBRE). Financial support was also provided by Maj and Tor Nessling Foundation, North Ostrobothnia Fund of the Finnish Cultural Foundation, Oulun Luonnonysta¨va¨in Yhdistys, and Entomological Society of Helsinki.
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