Biodivers Conserv (2007) 16:26952713 DOI 10.

1007/s10531-006-9081-2 ORIGINAL PAPER

Assessing riparian quality using two complementary sets of bioindicators

Jenny Smith Michael J. Samways Stuart Taylor

Received: 18 February 2005 / Accepted: 29 May 2006 / Published online: 12 July 2006 Springer Science+Business Media B.V. 2006

Abstract Biological indicators are being increasingly used to rapidly monitor changing river quality. Among these bioindicators are macroinvertebrates. A shortcoming of macroinvertebrate rapid assessments is that they use higher taxa, and therefore lack taxonomic resolution and species-specic responses. One subset of invertebrate taxa is the Odonata, which as adults, are sensitive indicators of both riparian and river conditions. Yet adult Odonata are not necessarily an umbrella taxon for all other taxa. Therefore, we investigated whether the two metrics of aquatic macroinvertebrate higher taxa and adult odonate species might complement each other, and whether together they provide better clarity on river health and integrity than one subset alone. Results indicated that both metrics provide a similar portrait of large-scale, overall river conditions. At the smaller spatial scale of parts of rivers, Odonata were highly sensitive to riparian vegetation, and much more so than macroinvertebrate higher taxa. Odonate species were more sensitive to vegetation structure than they were to vegetation composition. Landscape context is also important, with the odonate assemblages at point localities being affected by the neighbouring dominant habitat type. Overall, benthic macroinvertebrates and adult Odonata species provide a highly complementary pair of metrics which together provide large spatial scale (river system) and small spatial scale (point localities) information on the impact of stressors such as riparian invasive alien trees. As adult Odonata are easy to sample and are sensitive to disturbance at both small and large spatial scales, they are valuable indicators for rapid assessment of river condition and riparian quality.

J. Smith School of Botany and Zoology, University of KwaZulu-Natal, P/Bag X01, Pietermaritzburg, South Africa M. J. Samways (&) S. Taylor Department of Conservation Ecology and Entomology and Centre for Agricultural Biodiversity, University of Stellenbosch, P/Bag X1, Matieland 7602, South Africa e-mail: samways@sun.ac.za

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Keywords Riparian ecosystems Bioindicators Benthic macroinvertebrates Adult Odonata Complementarity

Introduction River quality throughout the world is deteriorating, with stream biotas being altered in numerous ways (Davies and Day 1998). Yet aquatic ecosystems are highly complex, and incorporate interactions between physical, chemical and biological entities. This makes them difcult and expensive to monitor by traditional physico-chemical means. In contrast, organisms, being biological endpoints, are good indicators of river quality, and reect the overall ecological integrity of their environments (Wright et al. 1984; Rosenberg and Resh 1993; Metcalf-Smith 1994; Smith et al. 1999) and enable management decisions to be made (Karr 1991; Norris and Norris 1995; Karr and Chu 1999; Mancini et al. 2005). However, not all organisms are equally sensitive to disturbance (Lammert and Allen 1999; Dovciak and Perry 2002; Heino et al. 2005). Among the biological indicators that have been used for assessing river quality in southern Africa, as elsewhere, are benthic macroinvertebrates (Dallas 1997; Brown 2001; Dickens and Graham 2002). Macroinvertebrate assemblages have been used for comparing river systems, as well as for monitoring long-term trends. However, these macroinvertebrate metrics are a coarse method, as they are intended to be a rapid bioassessment method that is eld based to reduce the time needed to process samples. Furthermore, the taxonomic resolution of samples is limited to taxonomic levels above species (Dickens and Graham 2002). They generally do not provide a measure of ecological integrity at the species level and therefore would not be able to give information relating to conservation issues of concern at this level (Brown 2001). In particular, as named species are not used, macroinvertebrate higher taxa do not generate assessments of the ways in which endemic species are being affected relative to more geographically widespread species. Monitoring abundant resident species may be important for detecting the early decline of a habitat (Hawking and New 2002). However, monitoring rare species is also important as they can be indicative of relict or undisturbed conditions and used to rate the importance of any site within its habitat groups (Eyre et al. 1986). It is also important to identify species that are restricted to a narrow range of conditions as they may be good indicators of change. One subset of aquatic macroinvertebrates is the Odonata, an insect order which occupies a spectrum of aquatic habitats (Corbet 1999). Odonates are sensitive to changes in water quality and to landscape disturbance and thus they reect to some extent the ecological conditions of their habitats (Samways and Steytler 1996; Chovanec and Waringer 2001). Odonata are relatively well studied, and there is a sufcient number of species in most localities to give manageable number of species for assessments (Samways 1993). Adults are large and conspicuous, and most species are easily identied in the eld, even by relative non-experts. These odonate characteristics, coupled with their long ontogenetic development, suggest they could be valuable for medium- or long-term monitoring. However, using only Odonata as indicators of ecological integrity does not necessarily offer a wide enough taxonomic umbrella on which to base sound biological conservation decisions. As a single taxon, they may not expose what is happening at higher community levels of

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organization. Conversely, not all benthic macroinvertebrate taxa can be monitored at the species level as this would be too time consuming, labour intensive, expensive and often the individual species cannot be identied. Determination of the habitat requirements of Odonata species allows development of characteristic assemblages of Odonata species, which can be used to monitor changes in the environment (Clark and Samways 1996; Osborn and Samways 1996). Environmental disturbances alter odonate assemblages in terms of both species composition and abundance. If the habitat preferences of certain species are known, a change in species composition is likely to be an indication of a type of disturbance. Species with more specic habitat preferences are more susceptible to certain types of disturbance (Clark and Samways 1996). In this regard, rare and threatened sunloving species are likely to be very indicative of invasion by alien woody plants with a dense canopy. As no single indicator can give a full picture of the particular environmental state of a river, it is necessary to look for complementarities among indicator metrics, and to identify indicators of change in structural, functional and compositional diversity at a range of scales and levels of organization (Rogers and Biggs 1999). One solution would be to combine a metric of higher benthic macroinvertebrate taxa, as a measure of ecosystem health, with the Odonata as a measure of ecological integrity at the species level. This is done here in an attempt to provide a more comprehensive picture of river health and conservation status. Special emphasis is given to the structure and composition of the riparian canopy, an ecosystem that is being severely modied in many parts of the world. The results are then used to assess the merits of using both or either metric for determining the effects of alien vegetation change upon the stream fauna. Sites and methods Sites and vegetation sampling units This study was done on three permanent rivers, the Msunduzi, Dorpspruit and Townbush in the Pietermaritzburg basin, South Africa 3020E, 2936S (660690 m a.s.l.). A sampling unit (SU) was 10 m of river together with the 1 m wide strip of vegetation on either bank. Within each 10 m stretch, was a glide and a rife to ensure that all habitats were included, minimizing variation (Dickens and Graham 2002). River depth was < 0.75 m. SUs along each river included extremes of structural diversity (shaded versus sunlit) and compositional diversity (alien versus indigenous plants). It was hypothesized that using such a range of environmental conditions would place extreme demands on the assemblages at point localities, while the three different river systems provided variation on a broader scale. Our aim was to stretch the two metrics as far as possible, and to see whether they both responded in the same or in different ways to a spectrum of environmental conditions. To this end, 14 SUs were along the Msunduzi (M), 28 SUs along the Townbush (T) and 28 SUs along the Dorpspruit (D) giving 70 SUs in all. Each SU was divided into four categories according to its combination of vegetation structure and composition characteristics. Vegetation structure was dened as open (<30% of river bank with tree canopy) or closed (>70% of river bank with tree canopy), and riparian vegetation composition as either principally indigenous, or principally alien vegetation along the rivers bank.

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Sampling of benthic macroinvertebrates and Odonata adults Sampling of benthic macroinvertebrates was standardized according to the South African Scoring System (SASS5) protocol, and included as much microhabitat variation as possible within each SU (Dickens and Graham 2002). Both emergent marginal and submerged vegetation were sampled. Samples were obtained using the kick-method, where rocks and other benthic material were disturbed by foot to ow downstream into a soft, 1 mm mesh net, 30 cm square. The content of each sample was washed to the bottom of the net and then tipped into a water-lled, white tray. Macroinvertebrates were identied to family level or above, while for the sensitive families Baetidae and Hydropsychidae, the number of species within each family was also recorded. Identication of the macroinvertebrates in white, plastic trays was for <15 min (Gerber and Gabriel 2002). However, during this 15 min, if no new organisms were found within the rst 5 min, identication was ended and samples returned to the river. Abundance of organisms within each taxon was estimated: a single individual was recorded as 1, 210 organisms were allocated 2 and 10100 organisms were allocated 3. Each taxon was allocated a sensitivity score between 1 and 15 (Dickens and Graham 2002), according to their sensitivities to anthropogenic impacts. The total of these scores gives the macroinvertebrate (SASS5) score. ASPT (Average Score Per Taxon) was calculated by dividing the macroinvertebrate score by the number of sampled taxa (Dickens and Graham 2002). Sampling of Odonata adults was between February and May 2002, the height of their ight season (Suh and Samways 2005). No major changes or uctuations in ow rates, which can affect Odonata population levels and macroinvertebrate scores (Dallas 1997, Stewart and Samways 1998; Hawkins et al. 2000), were detected. Along the 10 m stretch of each SU, all adult male Odonata individuals within 1 m either side of the waters edge were recorded on sunny days using close-focus binoculars. Those individuals that could not be identied on the wing were netted for later identication. As the Odonata adults gave such categorical results, odonate larvae might have done the same. However, as only 10% of species could be identied, the rest being too young, it meant that odonate larvae at the species level were not a suitable metric. Data analyses The non-parametric KruskalWallis test (Minitab ver. 14.10) was used for comparing differences in Odonata abundance or species richness with macroinvertebrate scores or abundance, between the three river systems. Canonical Correspondence Analysis (CCA) (CANOCO version 2.1) was used to relate the abundance of Odonata adults and macroinvertebrate taxa to the structure (open or closed canopy cover) and composition (indigenous or alien) of the vegetation. Statistical signicances of the effects of environmental variables was evaluated using Monte Carlo tests (ter Braak 1986), at 5% level of acceptance. The data were analysed further using cluster analysis (PRIMER-E), to investigate the similarities between SUs in terms of both adult Odonata assemblages (abundance and species richness) and macroinvertebrate assemblages (abundance and family richness). A Bray-Curtis similarity measure was used. Prior to the cluster analysis,

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abundance data were log transformed to down-weight the more abundant species and allow the rarer species to exert more inuence on the similarity calculation (Clarke and Warwick 2001). An additional cluster analysis, using the same coefcient and transformation, was carried out to determine the role of both vegetation structure and composition on SU similarity in terms of adult Odonata, macroinvertebrate assemblages and their different sensitivity scores. To ascertain whether Odonata abundance and species richness varied in the same direction and to the same extent as macroinvertebrate scores, a regression analysis was carried out. A similar comparison was done by regressing weighted Odonata scores against macroinvertebrate scores. Odonata were weighted using a rating based on their national abundance and endemism status (Samways 1999). For approximate abundance, the criteria were: 15 national records scored 5; 610 records scored 4; 1120 records scored 3; 2130 records scored 1; 41 + records scored 0, while the criteria used for endemism status were the largest areas for all records combined: recorded from <1000 km2 scored 5; from <10,000 km2 scored 4; from <100,000 km2 scored 3; from <1,000,000 km2 scored 2; from southern Africa scored 1; pan-African, and possibly also European and/or Asiatic scored 0. For the purpose of this study, these scores were reversed (5 = 0; 4 = 1; etc) so that integers Pincreased positively with area size. The weighted rating for each SU was calculated (ai + ei), for i = species 1, species 2,..., species n, where a = abundance score and e = endemism score. Results Taxa sampled A total of 749 individual Odonata adults were recorded belonging to 20 species (Table 1). Only nine individual Odonata larvae could be identied to species level, and these were a subset of the 51 macroinvertebrate taxa included in the macroinvertebrate samples (Table 2). Benthic macroinvertebrate assemblage variation and co-variation There were signicant differences in mean benthic macroinvertebrate scores between Msunduzi and the Dorpspruit and between Msunduzi and Townbush, but not between Townbush and Dorpspruit (Z = 0.19, df = 2) (Table 3). Similarly, there were signicant differences in mean macroinvertebrate abundance between Msunduzi and Townbush and between Msunduzi and Dorpspruit SUs but not between Townbush and Dorpspruit (Table 3). Also, there were signicant differences in macroinvertebrate taxa richness between Msunduzi and Townbush and between Msunduzi and Dorpspruit but not between Townbush and Dorpspruit (Table 3). Vegetation composition (indigenous versus alien) signicantly accounted for variation in macroinvertebrate assemblages (abundance and family richness) (F = 3.00, P = 0.005). In contrast, vegetation structure (open versus closed canopy cover) did not signicantly account for the variation (F = 0.81, P = 0.77). Using cluster analysis, Msunduzi SUs clustered together, with 65% similarity (Fig. 1). Townbush SUs clustered into two separate groups, with 45% similarity. Msunduzi, Dorpspruit and half of the Townbush SUs clustered together with a 54% similarity. However, T22T30 were dissimilar from this large cluster. SUs that were

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Table 1 Odonata species sampled in the three river systems Msunduzi river Zygoptera Synlestidae Chlorolestes tessellatus (Burmeister, 1839) Platycnemididae lys, 1836 Allocnemis leucosticta Se Coenagrionidae Ceriagrion glabrum (Burmeister,1839) Pseudagrion hageni Karsch, 1893 cker, 1869) Pseudagrion kersteni (Gersta Pseudagrion salisburyense Ris, 1921 Pseudagrion sublacteum (Karsch, 1893) Ischnura senegalensis (Rambur, 1842) Chlorocyphidae lys, 1853) Platycypha caligata (Se Anisoptera Gomphidae rster, 1898) Crenigomphus hartmanni (Fo Paragomphus cognatus (Rambur, 1842) Aeshnidae Anax imperator Leach, 1815 Anax speratus Hagen, 1867 Libellulidae Orthetrum julia Kirby, 1900 , 1832) Crocothemis erythraea (Brulle Trithemis arteriosa (Burmeister, 1839) Trithemis dorsalis (Rambur, 1842) Trithemis furva Karsch, 1899 Trithemis stictica (Burmeister, 1839) Zygonyx natalensis (Martin, 1900) A = Adult, L = Larva L L L L Townbush river Dorpspruit river

A A A A A

A A L A A A A L L

A A A

A L L A A A A A L A A L L A A A A A A L

geographically closest together, overall had the most similar macroinvertebrate assemblages. The Dorpspruit SUs clustered with 60% similarity. However, three Dorpspruit individual SUs clustered with other river systems (Fig. 1). The macroinvertebrate assemblages at these SUs differed from the other Dorpspruit SUs by lacking Oligochaeta and Tricorythidae. Signicantly, D49 had an open canopy, but was between two closed indigenous canopy SUs. These results illustrate that the context of the SU is important in addition to its individual features. Msunduzi, Dorpspruit and half of the Townbush SUs clustered together, with 54% similarity. However, T22T30 were separate from this large cluster. Most of these SUs were in the highest stretch of the river, emphasizing again that physical closeness of sites results in similar macroinvertebrate assemblages. SUs with similar vegetation structure did not cluster clearly, although the open canopy SUs of the Msunduzi clustered at a similarity of 65%. Thus, SUs had similar macroinvertebrate assemblages, even though vegetation structure differed, indicating that vegetation structure had a minimal effect on these assemblages.

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Biodivers Conserv (2007) 16:26952713 Table 2 Benthic macroinvertebrate taxa sampled in the three river systems Msunduzi river Coelenterata Turbellaria Oligochaeta Hirudinea Crustacea Amphipoda Potamonautidae Atyidae Palaemonidae Hydracarina Plecoptera Perlidae Ephemeroptera Baetidae Caenidae Heptageniidae Leptophlebiidae Oligoneuridae Tricorythidae Odonata Chlorocyphidae Synlestidae Coenagrionidae Platycnemidae Aeshnidae Corduliidae Gomphidae Libellulidae Hemiptera Belostomatidae Corixidae Gerridae Naucoridae Nepidae Notonectidae Pleidae Veliidae Megaloptera Corydalidae Trichoptera Hydropsychidae Philopotamidae Hydroptilidae Leptoceridae Pisuliidae Coleoptera Dytiscidae Elmidae Gyrinidae Hydraenidae Hydrophilidae Diptera Athericidae Ceratopogonidae Chironomidae Culicidae Townbush river

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Dorpspruit river

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Townbush river

Dorpspruit river

Table 3 Mean ( 1 SE) benthic macroinvertebrate score, macroinvertebrate abundance and macroinvertebrate taxa richness per sampling unit in the three river systems Mean macroinvertebrate score Msunduzi Townbush Dorpspruit 24.21 2.57 77.64 4.74 78.89 2.91 Z Score Mean invertebrate abundance 40.00 0.94 24.50 1.34 28.79 1.20 Z Score Mean invertebrate family richness 20.71 0.40 13.42 0.74 14.14 0.53 Z Score

5.081 5.232

5.631 4.052

5.291 4.982

Statistically signicant (P < 0.05) Z scores from KruskalWallis tests are also shown. Differences between Msunduzi and Townbush are indicated by superscript 1 and superscript 2 indicates differences between Msunduzi and Dorpspruit, df = 2. There were no signicant differences found between Townbush and Dorpspruit

Nevertheless, there was also a tendency for SUs in close proximity to group together. Vegetation structure did, however, have some effect on macroinvertebrate assemblages on the Msunduzi, with similar vegetation structures and macroinvertebrate assemblages clustering together. Further cluster analyses were done, but this time of vegetation composition on macroinvertebrate assemblages. The results were non-signicant. The Msunduzi SUs M14M12, clustered with a similarity of 65%. Despite, similar vegetation composition, there were two clusters of Townbush SUs. Also, the Msunduzi and Dorpspruit SUs were similar despite differences in vegetation composition, with site location and canopy structure being important. The Townbush clusters, T42T24, (with a 55% similarity) and the Dorpspruit clusters, D64D52 (with a 60% similarity) were all characterized by alien vegetation. The SUs with the highest percentage similarity (D61(0) and D58(0); M11(0) and M5(0); D67(1) and D45(0); D66(1) and D60(0); T42(0) and T18(1)) differed in vegetation composition again indicating that vegetation composition had a minimal effect on these assemblages. Along the Townbush, overall there was no discernable clustering of SUs with similar vegetation composition. Results thus indicate that clustering of macroinvertebrate assemblages did not depend strongly on indigenous versus alien vegetation. Similarly, along the Dorpspruit there was no distinct clustering. Thus, on this river too, indigenous versus alien vegetation composition was not signicant for determining macroinvertebrate assemblages. Benthic macroinvertebrate scores and habitat types The most discernable clustering was among SUs of the same river system. One was the Msunduzi SUs, which clustered with 65% similarity and another was T39T23 with 35% similarity, as well as D46D56 with 60% similarity. The Townbush cluster was also least similar to the clusters of SUs along the other river systems (35%

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D
D49(1) T25(0) T19(0) T41(1) T20(0) T15(0) T36(1) D50(1) T35(0) T33(0) T32(1) T42(0) T18(0) T27(0) T21(0) T39(0) T26(0) T40(0) T37(0) T31(0) T24(0) T38(1) D63(1) D62(1) D59(1) D48(1) D61(0) D58(1) D54(0) D47(1) D43(1) D46(1) D66(0) D60(1) D70(0) D68(0) D67(0) D45(1) D44(1) D64(0) D57(0) D56(0) D53(0) D55(0) D69(0) D65(0) D52(0) M14(1) M13(1) M9(1) M10(1) M1(1) M2(1) M8(1) M3(1) M7(1) M11(1) M5(1) M4(1) M6(1) M12(1) D511() T22(0) T16(0) T34(1) T23(0) T28(0) T29(1) T17(0) T30(1)

T D

D T

40

60

80

100

Similarity %

Fig. 1 Cluster analysis of benthic macroinvertebrate assemblages at all 70 sampling units in the three rivers. M = Msunduzi river, T = Townbush river, D = Dorpspruit river

similarity), which were 57% similar to each other. There was no discernable clustering of SUs with similar vegetation structure or with vegetation composition. Thus, macroinvertebrates with similar sensitivity scores occurred in the same river systems rather than at sites with similar vegetation structure and composition, which may or may not be in different systems. In other words, for macroinvertebrates, the particular river system at the larger spatial scale overrides the vegetational features at the smaller, local scale along the rivers. Variation in adult Odonata assemblages There were signicant differences in mean adult Odonata abundance between Msunduzi and Townbush and between Msunduzi and Dorpspruit, but not between Townbush and Dorpspruit (Table 4). There were signicant differences in Odonata species richness between the Msunduzi and Townbush and between Msunduzi and Dorpspruit), but not between the Townbush and Dorpspruit (Table 4). The Monte Carlo test from the CCA indicated that the vegetation structure (open or closed canopy) signicantly accounted for most of the variation among Odonata adult assemblages (abundance and species richness) (F = 10.53, P 0.005). Additionally, and again using CCA, vegetation composition (indigenous versus alien) was also

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Table 4 Mean ( 1 SE) Odonata abundance and species richness per sampling unit in the three river systems Mean Odonata abundance Msunduzi Townbush Dorpspruit 21.86 1.76 7.57 0.83 8.14 0.97 Z Score Mean Odonata species richness 6.07 0.35 2.46 0.18 3.21 0.25 Z Score

5.171 4.892

5.741 4.252

Statistically signicant (P < 0.05) Z scores from KruskalWallis tests are also shown. Differences between Msunduzi and Townbush are indicated by superscript 1 and superscript 2 indicates differences between Msunduzi and Dorpspruit, df = 2. There were no signicant differences found between Townbush and Dorpspruit

signicant in accounting for variation among the adult Odonata assemblages (abundance and species richness) (F = 3.59, P 0.005) although not to the same extent as vegetation structure. Msunduzi SUs clustered together, M6 being the exception, with a similarity of approximately 45% (Fig. 2). M6 was one of the SUs with the least vegetation along its bank compared to the other Msunduzi SUs, making conditions for Odonata species less favourable at this site. Townbush and Dorpspruit SUs were interspersed

D55 D53 D51 D49 D54 D52 D50 D59 T39 T38 D44 D58 D60 T41 D61 T32 T31 D48 D43 D47 T34 T29 T36 T30 T37 T18 D45 M6 D63 T33 T42 T40 D62 T35 D57 D46 M10 M4 M5 M12 M11 M9 M8 M3 M14 M2 M13 M7 M1 D68 T15 D67 T21 D69 D66 D56 T19 D70 D65 T24 T20 T27 D64 T28 T26 T17 T25 T22 T16 T23

D&T

M D&T

D&T

20

40

60

80

100

Similarity%
Fig. 2 Similarities between adult Odonata assemblages at all 70 sampling units in the three rivers. M = Msunduzi river, T = Townbush river, D = Dorpspruit river

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among each other. Three Townbush SUs (T22, T16 and T23) separated out, and were 95% dissimilar from the other SUs (Fig. 2). These SUs were geographically isolated from other Townbush SUs in a relatively forested area. Another cluster, D55D50 was 85% dissimilar from the other SUs (Fig. 2). These SUs were next to each other on the same stretch of river. Overall, Odonata were thus sensitive to both the larger spatial scale of river system type and smaller spatial scale effects, such as vegetation structure and composition. To further determine the role of vegetation structure on Odonata assemblages, SU characteristics (i.e. whether a SU had an open or closed canopy) were incorporated into Fig. 2. Adult Odonata assemblages along the three river systems were clearly affected by vegetation structure with tight clusters of SUs. D55D50 (with a 25% similarity) were closed canopy sites, D59M1 (with a 50% similarity), were open canopy sites and D68T23 (with 50% similarity) were all closed canopy sites. These closed canopy sites were divided into two groups which were less than 20% similar. However, the outlier Townbush SUs (T16, T22 and T23) had open canopies. The cluster of dissimilar Dorpspruit SUs (D55D50) was characterized by closed canopies except for the outlier D49, which was positioned between these SUs. This indicates that vegetation structure has a greater inuence on Odonata assemblages than does river system. D49, an open canopy, and T18, a closed canopy site, were also outliers. They clustered with SUs of different vegetation structure. D49 was an open canopy SU was between closed canopy SUs and was therefore inuenced by their characteristics. A few SUs (T22 and T16; T26 and T17; D64 and T28) were 100% similar with each pair having the same vegetation structure. This indicates that vegetation structure has a major edge-effect or halo effect on Odonata assemblages, indicating that landscape context is important. Adult Odonata assemblages did not respond to differences in vegetation composition, although there were two clusters. One was composed of alien vegetation (D68T23), with 50% similarity, and the other was composed of indigenous vegetation (Msunduzi SUs) with 50% similarity. A few SUs were 100% similar (T22 and T16; T26 and T17; D64 and T28). These pairs all had the same vegetation composition. The cluster of dissimilar Dorpspruit SUs (D55D50) had different vegetation compositions, as did the cluster of dissimilar Townbush SUs (T16, T22 and T23). Overall, vegetation composition at the ne scale of alien or indigenous vegetation has a small affect on adult Odonata assemblages, but not as great as that of vegetation structure. Benthic macroinvertebrate scores in relation to adult Odonata assemblages Benthic macroinvertebrate scores were positively and highly signicantly correlated with adult Odonata abundance (r2 = 0.486, df = 68, P < 0.005) (Fig. 3) and with Odonata species richness (r2 = 0.402, df = 68, P < 0.005) (Fig. 4). Variation in macroinvertebrate scores was in a similar direction to that of the Odonata indices, suggesting that both were responding in a similar way to environmental variables along the river system. Benthic macroinvertebrate scores were also positively and highly signicantly correlated with adult Odonata abundance (r2 = 0.373, df = 68, P < 0.005), Odonata endemism (r2 = 0.409, df = 68, P < 0.005) and with the total of these two scores

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Odonata abundance

25 20 15 10 5 0 0 50 100 150

Macroinvertebrate score
Fig. 3 Linear regression of adult Odonata abundance in each sampling unit against benthic macroinvertebrate score. Y = 6.850 + 0.2002x

10 9 8

Odonata species richness

7 6 5 4 3 2 1 0 0 50 100 150

Macroinvertebrate score
Fig. 4 Linear regression of adult Odonata species richness in each sampling unit against benthic macroinvertebrate score. Y = 0.2639 + 0.4287x

(r2 = 0.393, df=68, P < 0.005) (Fig. 5). Variation in macroinvertebrate scores were in a similar direction to that of the weighted Odonata indices, again suggesting that they are responding in a similar way to environmental variables along the river system.

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Weighted total endemism and abundance

70 60 50 40 30 20 10 0 0 50 100 150

Macroinvertebrate score
Fig. 5 Linear regression of total weighted adult Odonata endemism and abundance in each sampling unit against benthic macroinvertebrate score. Y = 3.592 + 0.4110x

Taxonomic groups and variation in benthic macroinvertebrate scores Of the 51 benthic macroinvertebrate taxa in the three river systems, 41 were in the Msunduzi, 37 in the Townbush and 35 in the Dorpspruit. About 10 of the 51 higher taxa were unique to the Msunduzi river (Table 2). Five of these ten taxa had high sensitivity scores (Palaemonidae (10); Hydracarina (8); Heptageniidae (13); Oligoneuridae (15) and Corduliidae (8)), the other ve had low sensitivity scores (Hirudinea (3); Belastomatidae (3); Pleidae (4); Culicidae (1) and Tabaenidae (5)). Three of the taxa were unique to the Townbush river (Table 2). These taxa (Hydroptilidae (6); Dyticidae (5); Hydraenidae (8)) had average to low sensitivity scores. Only, two of the taxa were unique to the Dorpspruit river (Table 2). These taxa included Coelenterata (1) and Hydrophilidae (5) which had low sensitivity scores. Macroinvertebrate scores were high along the Msunduzi river, because of greater numbers of taxa present at each SU and because certain families (Perlidae, Heptageniidae, and Chlorocyphidae) with very high sensitivity scores (10) were at very few SUs (Table 5). Heptageniidae, (at 85.7% of the SUs) were only along the Msunduzi river. Perlidae (at 85.7% of the SUs along the Msunduzi) and Chlorocyphidae (at 78.6% of the SUs along the Msunduzi) were also along the Townbush river, but at very few of the SUs (3.6% and 25.0% respectively). The Msunduzi SUs were all characterized by open canopies and indigenous vegetation. Perlidae were at one Townbush SU, which had a closed canopy and alien vegetation. Chlorocyphidae, along the Townbush river, was at two SUs with open canopies and indigenous vegetation, two SUs with open canopies and alien vegetation and three SUs with closed canopies and alien vegetation.

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Table 5 Percentage of sampling units (along the three river systems) which had very high (10) benthic macroinvertebrate sensitivity scores Taxon Amphipoda(13) Palaemonidae(10) Perlidae(12) Heptageniidae(13) Oligoneuridae(15) Chlorocyphidae(10) Platycnemididae(10) Philopotamidae(10) Pisulidae(10) Athericidae(10) Msunduzi 7.1 85.7 85.7 7.1 78.6 21.4 14.3 Townbush 21.4 3.6 25.0 28.6 32.1 3.6 32.1 Dorpspruit 3.6 10.7 3.6 35.7

Taxonomic groups and variation in adult Odonata assemblages Odonata assemblages (abundance and species richness) varied signicantly between river systems. Mean abundance and species richness per SU were both higher along the Msunduzi river (Table 5). Seventeen Odonata species were along the three river systems. Of these, 11 were along the Msunduzi river, with Pseudagrion sublacteum, Crenigomphus hartmanni, Anax speratus, Trithemis arteriosa and Zygonyx natalensis being unique to this river. Nine species were along the Townbush river (Ceriagrion glabrum being the only species unique to this river), and 11 species were along the Dorpspruit river (P. hageni and Ischnura senegalensis were the two species unique to this river) (Table 1). The differences in abundance and species richness scores from one river to another was because of the frequency at which the species were found at each SU along them. Most species along the Msunduzi river, occurred at most of the SUs, whereas along the other two river systems most of the species occurred at few SUs (Table 6). P. kersteni, Platycypha caligata and T. furva, were found at most of
Table 6 Percentage of sampling units (along the three river systems) where focal Odonata species occurred Odonata species Chlorolestes tessellatus Allocnemis leucosticta Ceriagrion glabrum Pseudagrion hageni P. kersteni P. salisburyense P. sublacteum Ischnura senegalensis Platycypha caligata Crenigomphus hartmanni Paragomphus cognatus Anax speratus Orthetrum julia Crocothemis erythraea Trithemis arteriosa T. furva Zygonyx natalensis Msunduzi 100 64.3 78.6 85.7 28.6 14.3 78.6 7.1 35.7 92.9 7.1 Townbush 25.0 10.7 3.6 89.3 3.6 17.9 17.9 71.4 7.1 Dorpspruit 14.3 35.7 28.6 78.6 10.7 7.1 50.0 46.4 3.6 25.0

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the Msunduzi SUs. At the SUs along the Townbush and Dorpspruit rivers, P. kersteni was the most common species (Table 6). Of the 47 SUs along the Townbush and Dorpspruit rivers where P. kersteni occurred, 19 had closed canopies and alien vegetation, nine had open canopies and alien vegetation and 19 had open canopies and indigenous vegetation. P. caligata occurred at 17 SUs along the Townbush and Dorpspruit rivers. Seven of these had closed canopies and alien vegetation, six had open canopies and alien vegetation and four had open canopies and indigenous vegetation. Chlorolestes tessellatus and Allocnemis leucosticta, both of which are South African endemics, were along both the Townbush and the Dorpspruit rivers, but not along the Msunduzi river. C. tessellatus was only at SUs with closed canopies where there was never more than two other species present. A. leucosticta occurred at 13 SUs along these two rivers. Two of these 13 SUs had open canopies, the others were all composed of closed canopies and all but two of these had two or less other species present.

Discussion Spatial scale: variation between and within river systems A biological monitoring technique should reveal whether any anthropogenic impact is causing deterioration in river condition, and should provide some indication of the severity of this impact. Use of several different techniques may enhance the interpretation of data collected as part of a biological monitoring programme, as it is unlikely that any single technique will full all the above criteria on its own (Brown 2001). Our study showed that spatial scale (river system versus point localities) was a signicant variable for both the benthic macroinvertebrate and adult Odonata metrics. At the large spatial scale of a river, macroinvertebrate abundance and species richness, as well as Odonata abundance and species richness, responded similarly to the different river systems. In short, at the large spatial scale, the macroinvertebrate metric and adult dragony metric were comparable. Habitat quantity, quality and diversity all affect macroinvertebrate scores, with Odonata species richness and abundance affected similarly. Odonata scores were high along the most sunlit river (Msunduzi), probably because adult Odonata are known to have strong and species-specic sunlight versus shade preferences (Clark and Samways 1996; Stewart and Samways 1998), with most South African Odonata species avoiding closed canopy riparian vegetation (Pinhey 1984; Kinvig and Samways 2000). Aquatic macroinvertebrates, which are less vagile than adult Odonata, were mostly affected by the overall canopy cover. In contrast, Odonata adults are highly sensitive to local environmental conditions, and respond rapidly using ight to seek suitable habitat (Samways et al. 1996). Thus, these vagile insects reect the immediate structure of the habitat along the river, as well as the general condition of the river. Mancini et al. (2005) showed that land use condition strongly affects macroinvertebrate assemblages. Brown (2001) commented that higher-taxon level data provided a good indication of the effects of overall anthropogenic impact on the

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system, whereas species data are more sensitive to specic patterns in environmental variables. Macroinvertebrate assemblages here were similar along whole river systems, with little response to closed versus open vegetation, nor to alien versus indigenous vegetation. Therefore, macroinvertebrates were responding to average habitat character (i.e. riparian zone vegetation) as well as likely to water quality. Odonata assemblages, in contrast, were particularly sensitive to vegetation changes, particularly structure over composition, as well as reecting overall character of the river. Nevertheless, the context of the habitat at individual point localities was important, especially where there was high contrast from one point locality to the next in vegetation structure. Where closed canopy dominated, with only short stretches of river with open canopy, the Odonata assemblage was largely of the closed canopy type. These results also support those from elsewhere, where structures inhibited linear movements of Odonata (Schutte et al. 1997) and riparian habitats were not necessarily movement corridors (Rosenberg et al. 1997). Thus, the two metrics (benthic macroinvertebrates and adult Odonata) together provide a relatively comprehensive synthesis of the biological conditions of a particular river system (or point locality at the smaller spatial scale). Adult male Odonata can be used to characterize a habitat (Hawking and New 2002). Furthermore, resident adults are likely to be more affected by changes in the immediate environment than would transitory species, and therefore should have the greatest value as indicators. Here, most Odonata larvae were too young to identify to species level, meaning that resident status could not be categorically determined. However, by inference at the generic level, the species encountered here were all likely to be resident. Indeed, the two most sensitive species, Chlorolestes tessellatus and Allocnemis leucosticta, are both national endemics requiring natural forest. Benthic macroinvertebrates and individual species We highlighted here the difculty of using Odonata larvae at the species level, principally because they could not be identied. Furthermore, Hawking and New (2002) found that the diversity and abundance of larvae varies considerably, even on consecutive dates. This shortcoming is partly overcome by using a macroinvertebrate metric which species the habitats to be sampled, so that there is no chance sampling of different substrates. Nevertheless, it is still important to be aware that the larvae present in a single sample may not be a true representation of the full spectrum of local species. Knowledge of the life histories of the macroinvertebrates used in the bioassessment could help interpret the state of the water body and its environment. This was suggested by this study, where taxa with high sensitivity scores were more numerous along one river yet poorer in the other two. This compares with taxa with low sensitivity scores which were more common in these two other rivers, suggesting perhaps some degradation of these two systems. This degradation was probably mostly due to alien trees shading the habitat. A cautionary note, which parallels the ndings of Kinvig and Samways (2000), is that it is essential to compare like with like. When alien trees invade, there is an impoverishment of Odonata assemblages, and this impact has a similar effect on assemblages as do well-developed indigenous

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tree canopies. Nevertheless, when the invasive alien canopy becomes very dense, it extirpates sun-loving endemic odonate species (Samways and Taylor 2004). Sensitivity scores of benthic macroinvertebrates can be an early indicator of whether or not rivers and their canopies are changing in quality. Along streams in the USA, early signs of degradation were shown in the loss of intolerant and longlived taxa. This was followed by an overall decrease in taxa richness. Heavily affected sites were dominated by a few, highly-tolerant taxa (Morley and Karr 2002). It is important to note the composition of macroinvertebrate assemblages in each sample, as macroinvertebrate scores could still be relatively high if many highlytolerant taxa are still present, despite degradation of the stream. It is important therefore, to also include the average score per taxon (ASPT), to give a more accurate picture of the true health of the river (Dickens and Graham 2002). With a better understanding of the life histories of macroinvertebrates and their responses to specic stressors, the diagnosis of causes of degradation, and not just the warning of degradation, might be possible. This will greatly enhace restoration and conservation efforts. Recommendations arising from this study Our results support the ndings from other continents (Wright et al. 1984; Rosenberg and Resh 1993) that benthic macroinvertebrates are sensitive indicators of river condition, in this case overall character of the riparian zone. Furthermore, our results support those of Dickens and Graham (2002) and others, that the average score per taxon (ASPT) is a more consistent metric than the benthic macroinvertebrate score or number of macroinvertebrate taxa. Furhtermore, Odonata species richness and abundance both supported the ASPT, suggesting that both metrics (benthic macroinvertebrate ASPT and adult Odonta) are equally good responders to the general character of the riparian zone, and are highly complementary. Additionally, adult Odonata species richness and abundance, and certain species in particular, were highly sensitive to point localities along the riparian corridor. Odonata species richness, abundance and assemblage composition were especially sensitive to vegetation structure rather than composition. However, in the case of riparian trees, the effects of vegetation composition and structure are compounded when the alien trees form a dense canopy. Furthermore, the odonate assemblages were so sensitive that they also responded to small-scale (only a few metres) fragmentation of the riparian corridor. As adult odonates are relatively easy to sample (and only requiring close-focus binoculars), they make an excellent metric for rapid assessment of both river condition and riparian quality.
Acknowledgements Financial support was from the Working for Water Programme.

References
Brown CA (2001) A comparison of several methods of assessing river condition using benthic macroinvertebrate assemblages. Afr J Aquat Sci 26:135147 Chovanec A, Waringer J (2001) Ecological integrity of river oodplain systems assessment by dragony surveys (Insecta: Odonata). Regulated Rivers: Res Manage 17:493507

123

2712

Biodivers Conserv (2007) 16:26952713

Clark TE, Samways MJ (1996) Dragonies (Odonata) as indicators of biotope quality in the Kruger National Park, South Africa. J Appl Ecol 33:10011012 Clark KR, Warwick RM (2001) Change in marine communities: an approach to statistical analyses and interpretation. 2nd edn. Primer-E, Plymouth, UK Corbet PS (1999) Dragonies: behaviour and ecology of Odonata. Harley, Colchester, UK Dallas HF (1997) A preliminary evaluation of aspects of SASS (South African Scoring System) for the rapid bioassessment of water quality in rivers, with particular reference to the incorporation of SASS in a national biomonitoring programme. South Afr J Aquat Sci 23:7994 Davies B, Day J (1998) Vanishing waters. University of Cape Town Press, Cape Town Dickens CWS, Graham PM (2002) The South Africa Scoring System (SASS) version 5 rapid bioassessment method for rivers. Afr J Aquat Sci 27:110 Dovciak AL, Perry JA (2002) In search of effective scales for stream management: does agroecoregion, watershed, or their intersection best explain the variance in stream macroinvertebrate communities? Environ Manage 30:365377 Eyre MD, Ball SG, Foster GN (1986) An initial classication of the habits of aquatic Coleoptera in North-east England. J Appl Ecol 23:841852 Gerber A, Gabriel MJM (2002) Aquatic invertebrates of southern Africa. Illustrations. Institute for Water Quality Studies. Department of Water Affairs and Forestry, Pretoria Hawkins CP, Norris RH, Houge JN, Feminella JW (2000) Development and evaluation of predictive models for measuring the biological integrity of streams. Ecol Appl 10:14561477 Hawking JH, New TR (2002) Interpreting dragony diversity to aid in conservation assessment: lessons from the Odonata assemblage at Middle Creek, north-eastern Victoria, Australia. J Insect Conserv 6:171178 Heino J, Paavola R, Virtanen R, Muotka T (2005) Searching for biodiversity indicators in running waters: do bryophytes, macroinvertebrates, and sh show congruent diversity patterns? Biodivers Conserv 14:415428 Karr JR (1991) Biological integrity: a long-neglected aspect of water research management. Ecol Appl 1:6684 Karr JR, Chu EW (1999) Restoring life in running waters: better biological monitoring. Island Press, Washington, DC Kinvig RG, Samways MJ (2000) Conserving dragonies (Odonata) along streams running through commercial forestry. Odonatologica 29:195208 Lammert M, Allen JD (1999) Assessing biotic integrity of streams: effects of scale in measuring the inuence of land use/cover and habitat structure on sh and macroinvertebrates. Environ Manage 23:257270 Mancini L, Formichetti P, Anselmo A, Tancioni L, Marchini S, Sorace A (2005) Biological quality of running waters in protected areas: the inuence of size and land use. Biodivers Conserv 14:351 364 Metcalf-Smith JL (1994) Biological water-quality assessment of rivers: use of macroinvertebrate communities. In: Calow P, Petts GE (eds) The rivers handbook, hydrological and ecological principles. vol. 2. Blackwell, Oxford, pp 144170 Morley SA, Karr JR (2002) Assessing and restoring the health of urban streams in the Puget sound basin. Conserv Biol 16:14981509 Norris RH, Norris KH (1995) The need for the biological assessment of water quality: Australian perspective. Aust J Ecol 20:16 Osborn R, Samways MJ (1996) Determinants of adult dragony assemblage patterns at new ponds in South Africa. Odonatologica 25:4958 Pinhey E (1984) A survey of the dragonies (Odonata) of South Africa Part 1. J Entomol Soc Southern Afr 47:147188 Rogers K, Biggs H (1999) Integrating indicators, endpoints and value systems in strategic management of the rivers of the Kruger National Park. Freshwater Biol 41:439451 Rosenberg DK, Noon BR, Meslow EC (1997) Biological corridors: form, function and efcacy. BioScience 47:677687 Rosenberg DM, Resh VH (eds) (1993) Freshwater biomonitoring and benthic macroinvertebrates. Chapman & Hall, New York, London, p 488 Samways MJ (1993) Dragonies (Odonata) in taxic overlays and biodiversity conservation. In: Gaston KJ, New TR, Samways MJ (eds) Perspectives on insect conservation. Intercept, Andover, UK, pp 111123 Samways MJ (1999) Diversity and conservation status of South African dragonies (Odonata). Odonatalogica 28:1362

123

Biodivers Conserv (2007) 16:26952713

2713

Samways MJ, Caldwell PM, Osborn R (1996) Spatial patterns for dragonies (Odonata) as indicators for design of a conservation pond. Odonatologica 25:157166 Samways MJ, Steytler NS (1996) Dragony (Odonata) distribution patterns in urban and forest landscapes, and recommendations for riparian management. Biol Conserv 78:279288 Samways MJ, Taylor S (2004) Impacts of invasive alien plants on Red-Listed South African dragonies (Odonata). South Afr J Sci 100:7880 Schutte G, Reich M, Plachter H (1997) Mobility of the rheobiont damsely Calopteryx splendens (Harris) on fragmented habitats (Zygoptera: Calopterygidae). Odonatologica 26:317327 Smith MJ, Kay WR, Edward PJ, Papas K, Richardson STJ, Simpson JC, Pinder AM, Carle DJ, Horwitz PHJ, Davids JA, Yung FH, Norris RH, Halse SA (1999) AusRivAS: using macroinvertebrates to assess ecological condition of rivers in Western Australia. Freshwater Biol 41:269 282 Stewart DAB, Samways MJ (1998) Conserving dragony (Odonata) assemblages relative to river dynamics in an Africa savanna game reserve. Conserv Biol 12:683692 Suh A, Samways MJ (2005) Signicance of temporal changes in designing a reservoir for conservation of dragony diversity. Biodivers Conserv 14:165178 ter Braak CJF (1986) Cononical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 65:11671179 Wright JF, Moss D, Armitage PD, Furse MT (1984) A preliminary classication of running-water sites in Great Britain based on macro-invertebrate species and the prediction of community type using environmental data. Freshwater Biol 14:221256 Yoder CO, Ranking ET (1995) Biological response signatures and the area of degradation value: new tools for interpreting multimetric data. In: Davis WS, Simon TP (eds) Biological assessment and criteria: tools for water resources planning and decision making. Lewis, Boca Raton Florida, pp 263286

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