Aquatic Coleoptera (beetles) play a key role in freshwater ecosystems and are considered as a suitable bioindicator. Despite being widely distributed in China, there are few aquatic Coleoptera-based methods to assess ecological quality and environmental conditions. Changbai Mountain, with its distinct temperate and boreal forest ecosystems, provides an excellent opportunity to explore the influence of environmental features on aquatic beetles along altitude gradients. The objectives of the study were to investigate community structure and to determine the dominant factors controlling aquatic beetles in the montane environment. Study results showed that there were 8 families, 40 genera, and 72 aquatic beetle species on Changbai Mountain, and that Dytiscidae, Hydrophilidae and Haliplidae were the dominant families. Seven sensitive species of aquatic beetles could be considered as the candidate of indicator for environmental monitoring. Canonical correspondence analysis showed that water pH, concentrations of total organic matter and total phosphorus in sediment, water conductivity and water temperature had a significant impact on the community structure of aquatic beetles, and that water pH was the most important factor. Our results suggested that water quality played a key role in species richness of aquatic beetles, and that therefore they could be considered as an indicator organism of freshwater ecosystem health.

Introduction

Freshwater is one of the most diverse and threatened components of global biodiversity (Sala and Jackson, 2006). Despite their potentially high conservation value, freshwater ecosystems are constantly lost and degraded by the intensification of forest management or agricultural activities (Margherita et al., 2010). The conservation of freshwater biodiversity demands better information on indicators of ecological-environmental quality. Aquatic Coleoptera (beetles) play a key role in linking primary production, allochthonous input and top predators in freshwater ecosystems (Heino et al., 2008; Ifigenia et al., 2006). Furthermore, they have been considered suitable indicator species for several decades both in Europe and the USA (Eyre et al., 1986), because of their high species diversity, and narrow tolerance to ecological conditions of some species.

Aquatic beetles are very sensitive to environmental conditions (Miserendino and Archangelsky, 2006). The composition of the aquatic beetle community can be affected by various environmental factors, including pH (Eyre et al., 1986), electrical conductivity (Eyre et al., 1990), land use, vegetation cover and water chemistry (Armin et al., 2009). More knowledge of the tolerances and habitat requirements of aquatic beetles is needed for evaluation of the health of stream and river basin ecosystems. Most aquatic beetles are confined to special habitats by their size, shape and swimming ability. The riffle beetles (Elmidae) are sensitive to pollution but diving beetles (Dytiscidae) tolerate intensely polluted habitats (Foster, 2004, 2005). Using beetles alone, it is feasible to encompass within one analysis all wetland habitats, including those without vegetation. Moreover, beetles are mostly long-lived and can be found in many habitats, thus permitting data collection and evaluation of some wetlands over much of the year. In addition, aquatic beetles are generally easily sampled, and relatively well-known for their taxonomy and ecology (Nilsson and Holmen, 1995).

Aquatic beetles are widely distributed in China, but their value for assessing ecosystem health is not yet fully recognized. The first study of aquatic beetles in China was conducted in the early 19th century and focused on taxonomy (Jäch and Ji, 2003). From 1993 to 2009, the species distribution has been surveyed in twenty provinces in China, though only a few study results have been reported (Dong, 2008), and the aquatic Coleoptera-based methods available to assess the ecological qualities are still limited.

The goal of this study is to determine how the key environmental factors, including water pH, total organic matter (TOM) and total phosphorus (TP) in sediment, and conductivity and temperature of water control diversity and community composition of aquatic beetles on Changbai Mountain. Results are presented here from two perspectives to develop strategies for ecological restoration. First, the distribution and community structure characteristics of aquatic beetles in different habitats were ascertained and second, the key factors that contribute to aquatic beetle community structure were analyzed, and the indicator species for environmental monitoring were determined.

Methods

Study area

Changbai Mountain, located in northeastern China, is the highest mountain in the eastern Eurasian Continent with the richest biodiversity, including 1250 seed plants, 251 fungi, 148 lichens, 339 bryophytes, 87 pteridophytes and numerous birds, insects, and mammal species. The cone-shaped mountain is characterized by relatively gentle slopes covered with altitudinal vegetation zones, including mixed forest (<1,100 m), coniferous forest (1,100–1,700 m), Erman's birch forest (1,700–2,000 m) and tundra (>2,000 m) from the bottom to the top (2,744 m). The mountain has a temperate, continental climate, with cold and long winter and warm summer. Annual mean temperature varies from 2.8°C at the bottom to −7.3°C at the highest elevation (Shao et al., 2001). The wide range of climatic conditions has also allowed plant and animal species of different climate zones to co-exist on the mountain. In the light of these environmental features, it is an excellent place for studying aquatic beetles.

Sampling of aquatic beetles and laboratory analysis

Thirty streams (Figure 1) ranging from 646 m a.s.l. to 1414 m a.s.l. were selected. Sampling was carried out monthly between May and October from 2004 to 2007. Aquatic beetles were trapped by an O framed net with a 250 μm mesh size. At each stream, three sets of 20 sweeps were carried out per visit, covering all microhabitats visually detected in the littoral zone of the sample sites. Samples (60 sweeps) from each stream were combined and then preserved in 70% ethanol. In the laboratory, samples were sorted under a stereomicroscope and identified to the lowest taxonomic level (species when possible), and the number of species was calculated as the sum of recorded species in each sampling site, regardless of the time of collection.

Measurement of environmental variables

Abiotic variables were measured at each sampling site (Table 1), including altitude (Alt), air temperature (At), water and sediment metrics. Water variables were measured monthly, and the sediment samples were measured yearly at each sampling site. Water variables, including temperature (Wt), depth (Wd), electrical conductivity (Wc) and pH were measured at each sampling site in situ. Water depth was measured with a ruler calibrated in millimeters. Electrical conductivity was measured with a portable conductivimeter WTW, model LF90. The value of pH was measured by a portable potentiometer WTW, model pH90. Temperature near the bottom was measured by a portable Oxymeter YSI, model 55. Air temperature was measured by a Modular Weather Station, Model M260278. Altitude was measured by GPS navigator, GARMIN 1455.

A sediment sample was last collected from the top 5 cm of the surface at each site. Sediment variables, including TOM, total nitrogen (TN) and TP were measured. TOM, TN and TP of sediment were analyzed in the laboratory following standard methods detailed in Jin and Tu (1990).

Data analysis

  • (i) Four biodiversity metrics were calculated for each sampling site: the species richness (S, number of species per sample), species diversity (the Shannon-Wiener diversity index, H; Shannon and Weaver, 1949), Pielou (1969) evenness index (E) and Simpson (1949) dominance index (D).

  • (ii) Canonical correspondence analysis (CCA) was used to examine the influence of environmental variables on the structure of aquatic beetle communities. All parameters were log10-transformed to ensure normal distribution and standardization. The CCA was computed with the software CANOCO 4.5 (Ter Braak and Šmilauer, 2002).

  • (iii) Linear regression analysis was used to verify the relationship between biodiversity index and pH at the sampling sites. All statistical analysis was performed by SPSS version 18.0 (SPSS, Inc.).

Results

Environmental features

The values of nine environmental factors in each sampling site are listed in Table 1. Water pH ranged from 5.04 to 6.18, with the average of 5.65, while the maximum was found in site S19 and the minimum in site S6 near the road. Water conductivity ranged from 29.6 μs cm−1 to 72.8 μs cm−1. Water temperature varied from 5.7 to 21.3, showing differences among the sampling sites as the expected gradient pattern. The water depth ranged from 2 to 32 cm, with the average of 14.6 cm. The maximum of TOM in sediment was detected in site S7 (73.67 g kg−1), the lowest in site S6 (12.43 g kg−1). TP concentrations in sediment was strikingly different among sites, ranging from 0.11 to 0.92 g kg−1. TN concentrations in sediment ranged from 1.01 to 2.19 g kg−1, with the average of 1.17 g kg−1. In general, water and sediment chemistry showed strong difference in all sites.

Distribution and biodiversity of aquatic beetles

We recorded a total number of 1572 specimens of aquatic beetles, which belonged to 8 families, 40 genera and 72 species (see Appendix in the online supplemental information; Figure 2). In the course of the investigation, we recorded known China species of the families Hydroscaphidae, Hydraenidae, Amphizoidae, Elmidae and Helophoridae (Appendix). The highest number of individuals was Dytiscidae (638), followed by Haliplidae (240) and Hydrophilidae (184). Dytiscidae and Hydrophilidae (both species and individuals) were the dominant families in the study areas. Dytiscidae, including 17 genera and 39 species, had the highest dominance on the mountain.

Amphizoa Sinica Yu and Stork, a distinctive species, was found only on Changbai Mountain without record in other areas around the world. Each of four species, including Optioservus sp., Agabus kholini Nilsson, Noterus japonics Sharp and Dytiscus dauricus Gebler, was observed only at one of sampling sites, respectively; and only one individual was found from Noterus angustulus Zaitzer and Nebrioporus hostilis Sharp.

Species richness (S) was between 10 and 20 at most of the sampling sites, and was highest at site S8 (S = 37), and the lowest at site S2 and S6 (S = 0) (Figure 2). The Shannon-Wiener diversity indexes were 1.416 to 2.941 at most of the sampling sites (except S1, S2, S3, S6 and S19; Figure 2). Simpson dominance values (D) showed large variations in sampling sites and ranged from 0.052 to 1.0 (Figure 2). The highest evenness index (E) was close to 1, while the lowest was at sites S1 and S3 (only recorded one species; Figure 2).

Relationship between aquatic beetles and environmental features

Ordination analysis of the species-environmental dataset showed that six environmental factors (pH, TOM, TP, altitude, Wt and Wc) were good predictors of water beetle community composition within the stream habitats (Figure 4). The value of pH proved to be much stronger than other variables.

The CCA-Biplots showed that the first four axes of this CCA had relatively high eigenvalues and species-environmental correlation, suggesting a close relationship between the environmental variables selected and beetles (Table 2). The main environmental gradient (axis 1) was determined by pH, TOM and TP, suggesting the existence of trophic gradient. The second axis showed an environmental gradient associated mainly with temperature, a variable more related to stream magnitude along the altitude gradient. The third axis was closely correlated with water conductivity, and the fourth axis seemed to represent altitude gradient (Table 2).

Among selected environmental variables, pH was an important determinant of the composition of aquatic beetle community. Curve fitting showed that the Shannon diversity (H), evenness (E) and richness (S) were significantly correlated with pH, and the ideal fitting curves were cubic and quadratic functions, respectively (Figure 4). The figure illustrated that pH negatively influenced on H, S and E. The fitting curve between Simpson dominance index (D) and pH was exponential function, and the positive relativity was not significant as others (Figure 4).

Discussion

Six environmental parameters were found to be related to diversity and distribution of aquatic beetles in Changbai Mountain streams. The pH of water was the most important one, while nutrient concentrations (TOM and TP of sediment), altitude, water temperature and water conductivity can be taken as complementary and also important variables.

This study showed that Changbai Mountain aquatic beetles were dominated by Dytiscidae, Hydrophilidae and Haliplidae. Agabus spp. and Ilybius spp. (Dytiscidae), were the most tolerant Changbai Mountain aquatic beetle species. These two species were the most frequent and extensive in all the sampling sites; the two genera, with a wide geographical range, were widely recorded in China (Jäch and Ji, 2003).

Optioservus, (Elmidae), was found only at one sampling site, perhapes because TOM and TP concentrations at this site were lower than at other sites. Most literature supports the fact that Elmidae is quite sensitive to the degradation of streams and may be useful as an indicator due to its long life cycle in cold regions (Miserendino and Pizzolon, 2000; Kodada and Jäch, 2005). The genus, Noterus, (Noteridae), was also only observed at one site, probably due to the site having the highest pH. These sensitive species could be looked at as the “rarity” of Changbai Mountain, based on the arrangement described by Hessen and Walseng (2008). Therefore, the rarity of aquatic beetles could be considered as a candidate for indicator of environmental monitoring in the district.

In the study areas, the diversity of aquatic beetles varied remarkably with pH in a specific range (Figure 4). This result indicated that the range of pH that water beetles could tolerate (>5 units) was lower than that of freshwater fish (>6.5 units) (Larsson et al., 2006). The pH of a water body may be influenced partly by plants in riparian areas. The plants, however, are often disturbed by human activities, such as afforestation, deforestation and other agricultural and industrial activities.

Conclusions

In summary, this study showed that pH was the most dominant factor on aquatic beetle diversity and distribution, along with other environmental factors, including altitude, TOM in sediment, water conductivity and water temperature. Dytiscidae, Hydrophilidae and Haliplidae were the dominant families. The rarity of aquatic beetle, including Amphizoa Sinica Yu and Stork, Optioservus sp., Agabus kholini Nilsson, Noterus japonics Sharp, Dytiscus dauricus Gebler, Noterus angustulus Zaitzer and Nebrioporus hostilis Sharp, could be considered as the candidates of indicator for environmental monitoring in the district.

Our results have implications in defining correlation of biodiversity-environment in such forest, and demonstrate, in relation to promoting species richness, richness of endangered species, or both, that key environmental factors are prominent parameters for selected species or groups. Further studies are required to discern more distinctly the effects of environmental variables such as climate, latitude, vegetation and predators.

Funding

This research was supported by the National Natural Science Foundation of China (Grant No. 41230744), the Major Projects on Control and Rectification of Water Body Pollution (Grant No. 2012ZX07101-010) and State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences (Grant No. Y052010026).

Supplemental material

Supplemental data for this article can be accessed on the publisher's website.

The text of this article is only available as a PDF.

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Supplementary data