Effects of instream restoration measures on the physical habitats and benthic macroinvertebrates in an agricultural headwater stream

Ecological Engineering 122 (2018) 252–262

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Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng

Effects of instream restoration measures on the physical habitats and benthic macroinvertebrates in an agricultural headwater stream

T

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Kun Lia,b, Zhenxing Zhanga,b, Haijun Yanga,b, , Hongfeng Biana,b, Haibo Jianga,b, Lianxi Shenga,b, ⁎ Chunguang Hea,b, a

State Environmental Protection Key Laboratory of Wetland Ecology and Vegetation Restoration, School of Environment, Northeast Normal University, Changchun 130117, Jilin Province, China b Key Laboratory of Vegetation Ecology, Ministry of Education, Institute of Grassland Science, Northeast Normal University, Changchun 130024, Jilin Province, China

A R T I C LE I N FO

A B S T R A C T

Keywords: Instream structure Agricultural stressor Streambed substratum Phaeozem region Zoobenthos

The effectiveness of instream restoration measures in improving habitats has been extensively examined; however, the evidence is inadequate to infer that these measures have positive effects on benthic macroinvertebrates. In this study, we compared the effects of the instream wetland (IW), groin (GR), artificial drop (AD) and boulder placement (BP) measures on the physical habitat and benthic macroinvertebrates. On a fiveyear scale (two to six years after the implementation of the restoration project), the sample sites treated with the four restoration measures and the unrestored upstream control sample site were compared. The results show that the instream restoration measures had significant positive effects on the physical habitat and benthic macroinvertebrates in the agricultural headwater stream, that the physical habitat quality was a key factor affecting the restoration of the benthic macroinvertebrates, and that the restorative effects were affected by the interaction between the restoration measure and time. The five-year observation period showed continuous improvement in the habitat quality as well as a continuous increase in the taxon richness and diversity of the benthic macroinvertebrates at the restored sample sites. The AD and BP measures had the most significant positive effects on the richness and diversity of the benthic macroinvertebrates. The density of the benthic macroinvertebrates in the habitat at the sample site treated with the IW continuously remained at a high level. The benthic macroinvertebrates in the habitat at the sample site treated with the GR exhibited outstanding durability against and resilience to a flood. Schemes involving densely placed instream restoration measures had continuous positive effects on the physical habitat and benthic macroinvertebrates in agricultural headwater streams on a medium time scale (six years).

1. Introduction Intensive agriculture is one of the main causes of ecological degradation in streams worldwide (Allan, 2004; Riseng et al., 2011; Vörösmarty et al., 2010), particularly in China (Liu et al., 2003; Sun et al., 2012). Streams in agricultural watersheds are facing many grave problems, such as excess fine-grained sediment and changes in hydrological conditions (e.g., Murphy et al., 2015; Wagenhoff et al., 2011). How to scientifically cope with the degradation of agricultural streams is a challenge around the world (Hering et al., 2015; Robertson and Swinton, 2005). To cope with ecological degradation in streams, ecological

restoration is widely conducted across the world to repair river and stream ecosystems (Bernhardt et al., 2005; Wortley et al., 2013). Streambed substratum conditions play a pivotal role in the life cycle of numerous aquatic species and the maintenance of their diversity (Geist, 2011; Palmer et al., 1997). Therefore, physical habitats have become one of the core targets of ecological stream restoration projects (Pander et al., 2015). Recent years have seen a continuous increase in financial investment and time spent on streambed substratum habitat restoration projects (e.g., Pander et al., 2013; Pulg et al., 2011). Changes in natural flow conditions (Mueller et al., 2011) and increases in fine sediment (Dudgeon et al., 2006) caused by agricultural activity are a major cause of degradation of streambed substratum habitats in agricultural

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Corresponding authors at: State Environmental Protection Key Laboratory of Wetland Ecology and Vegetation Restoration, School of Environment, Northeast Normal University; Key Laboratory of Vegetation Ecology, Ministry of Education, Institute of Grassland Science, Northeast Normal University, Changchun 130117, Jilin Province, China. E-mail addresses: [email protected] (H. Yang), [email protected] (C. He). https://doi.org/10.1016/j.ecoleng.2018.08.007 Received 2 January 2018; Received in revised form 9 August 2018; Accepted 11 August 2018 0925-8574/ © 2018 Elsevier B.V. All rights reserved.

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restoration is the weak area of relevant research. In this study, the effects of several instream restoration measures on the physical habitat quality and benthic macroinvertebrate community in a headwater stream in the black-earth agricultural region in Northeast China were analyzed. The black-earth agricultural region in Northeast China is a major commodity grain base in China. In this region, the pressure placed on river and stream ecosystems by agricultural activity is a prominent problem. The damage of a headwater stream flowing into a reservoir in the black-earth agricultural region was repaired within a 1-km range. The stream is a typical representative of agricultural headwater streams. An evaluation was conducted after the restoration project was implemented on a five-year scale (i.e., two to six years after the implementation of the restoration project). The objectives of this study were (1) to evaluate the restorative effects of densely placed instream restoration measures on the damaged agricultural headwater stream and (2) to compare the effects of four instream habitat restoration measures (instream wetland (IW), groin (GR), artificial drop (AD), and boulder placement (BP) measures) on the benthic macroinvertebrate community.

watersheds. However, most research on the restoration of degraded physical habitats focuses on channelized streams (e.g., Baumgartner and Robinson, 2017; Erwin et al., 2017) and, in regard to ecological targets, this research concerns mainly fish (Kurth and Schirmer, 2014; Louhi et al., 2016) and special species (e.g., endangered, threatened, or native species). Because there are few types of fish of special economic value and ecological significance in agricultural headwater streams, most research investigating the management and restoration of agricultural streams focuses on the nitrogen, phosphorous, pesticides, agricultural activity management, and land-use efficiency (e.g., Flavio et al., 2017; Williams et al., 2015). Research on the degradation and restoration of physical habitats in agricultural headwater streams is severely lacking. Physical streambed substratum conditions in a stream are one of the major factors that affect the aquatic community (Sheldon, 1968) and, particularly, have a significant direct impact on the benthic macroinvertebrates (Mazão and da Conceição, 2016). Benthic macroinvertebrates are the middle link of the food chain and the integral components of food webs in stream ecosystems. By playing a central role in energy flow and matter circulation (e.g., decomposition of organic matter), macroinvertebrates directly influence the survival and reproduction of other taxa and are regarded as the foundation of a stable stream ecosystem (Covich et al., 2004; Townsend et al., 1998). They are sensitive to environmental changes such as disturbance, deterioration, and improvement (Sharley et al., 2008; Townsend et al., 2009). Different macroinvertebrate taxa have different sensitivities and tolerance capabilities to environmental conditions (Milošević et al., 2016; Murphy et al., 2014). Meanwhile, their life cycles are relatively longer than algae, but their migration ability is relatively weaker than fish (Balderas et al., 2016; Bonada et al., 2006). Therefore, macroinvertebrates can reflect the comparatively long-term temporal and spatial changes of stream ecosystems and can predict future problems (Herman and Nejadhashemi, 2015; Karr, 1999; Koperski, 2011). Some studies have indicated that benthic macroinvertebrates are ideal indicator organisms for research on the effectiveness of habitat restoration projects (Jähnig et al., 2010; Li et al., 2015). However, far less attention is paid to benthic macroinvertebrates than fish in research on the effectiveness of stream habitat restoration. The available research shows variable results with respect to the relations among stream restoration projects, changes in streambed substratum habitats, and benthic macroinvertebrate communities. Some studies find that stream habitats and benthic macroinvertebrate communities noticeably recovered after streambed substratum restoration projects were conducted (Frainer et al., 2018; Kail et al., 2015; Miller et al., 2010; Verdonschot et al., 2016), whereas more studies demonstrate that physical streambed substratum habitat restoration projects had limited positive effects on the benthic macroinvertebrate communities in the streams (e.g., Feld et al., 2011; Friberg et al., 2014; Jähnig et al., 2010; Lepori et al., 2005; Louhi et al., 2011; Negishi and Richardson, 2003; Palmer et al., 2010). The low effectiveness of restoration on macroinvertebrates can be attributed to insufficient restoration intensity (Suding, 2011), inappropriate design or measures (Lepori et al., 2005; Lorenz et al., 2009; Verdonschot et al., 2016), the limited scale (Bernhardt and Palmer, 2011; Jähnig et al., 2010; Sundermann et al., 2011), and a lack of geographically adjacent source populations for species colonisation (Brederveld et al., 2011; Kitto et al., 2015; Nilsson et al., 2015; Parkyn and Smith, 2011). While a wide variety of streambed substratum habitat restoration measures have been used extensively, they are mostly set up and implemented based on experience, and scientific evidence on their restorative effects is scant (Pedersen et al., 2009; Sarriquet et al., 2007). These apparent discrepancies in the results from empirical case studies limit our ability to understand the restoration process and improve the restorative effects. Therefore, studies of the various types of stream restoration cases and examinations of the effects of physical habitat restoration measures on biotic communities are necessary. Agricultural stream habitat

2. Material and methods 2.1. Study area The Yinma River is a primary tributary of the Second Songhua River. The Shitoukoumen Reservoir situated in the middle reaches of the Yinma River. The stream restored in this study is a 3.2-km-long agricultural headwater stream (43°53′N, 125°45′E; Fig. 1) that flows from west to east into the Shitoukoumen Reservoir. Before restoration, the headwater stream had a longitudinal gradient of 5‰, a width of 1–2 m, and a water depth of 0.1–0.2 m in normal seasons. The small watershed of the headwater stream has a valley-alluvial floodplainterrace landform, with black earth and leached soil as the main soil types. To the north bank of the stream are highways and residential areas; to the south bank of the stream is a sloping cornfield with some remaining forestland at the top. This area has a northern temperate semi-humid monsoon climate, with an annual average temperature of 4.8 °C and an annual average precipitation of 522–615 mm. Most precipitation in this area falls in summer, and the precipitation from July to September accounts for 75% of the total annual precipitation. 2.2. Restoration scheme Our restoration scheme increased the instream flow dynamics and the diversity of flow patterns by implementing instream measures and achieved a redistribution of the substratum and habitat quality restoration by means of diversified water flows, thereby restoring aquatic communities, such as benthic macroinvertebrates, and eventually restoring stream ecosystem functions (e.g., the self-cleaning capability). To address the existing problems facing the agricultural headwater stream (e.g., unstable banks, discontinuous hydrological conditions, physical habitat degradation and water quality deterioration; Fig. 1B), our research team designed a ecological stream restoration scheme and restored a 1000-m-long segment of the stream (3200 m in total length) in its middle reaches in 2008 (Table 1). Four instream measures—IW, GR, AD and BP measures—were implemented to help rehabilitate the stream to near-natural conditions relating to erosion, transport, and sedimentation, with a focus on improving its ecological conditions (hydrological and habitat quality) and a goal of ultimately increasing the diversity of the flow patterns, stream habitat quality, and biodiversity. 2.3. Restorative effects The physical habitat quality and benthic macroinvertebrate communities in the microhabitats were monitored at the same time at five 253

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Fig. 1. Location of the study area and the main instream measures used in the restoration project. (A) Location of the study area; (B) Unrestored control reach; (C) Instream wetland in the upstream; (D) Groin in the straight subsegments; (E) Artificial drop; (F) Boulder placement in the straight subsegments.

information of benthic macroinvertebrate communities are complete and typical in spring (Huo et al., 2012). Therefore, monitorings were conducted in the second year (May 2010), in the third year (May 2011), and in the sixth year (May 2014) after the restoration project was implemented to evaluate the restorative effects of instream restoration measures. In addition, heavy rainfall occurred in July 2010, which led to a 30-year flood. This flooding event provided a valuable opportunity for examining the effectiveness of the project in stream ecosystem durability and resilience. We added three monitorings in 2010 (August, September, and October) to compare the effects of the flood on benthic

kind of sample sites: the four kind of sample sites (the IW slow-flow zone, the inter-GR slow-flow zone, the riffle downstream of the AD, and the riffle downstream of the BP; Fig. 1C–F) that had been restored by the aforementioned four instream habitat restoration measures (hereinafter referred to as the IW, GR, AD, and BP sample sites), differing from the stream habitat before restoration, and the habitat at an upstream unrestored control sample site (hereinafter referred to as the UC sample site). The habitats were simple and homogeneous (fine-grained substratum and slow flow) in the UC sample sites. There were no riffle or pool in the UC reaches. In our study area, the diversity and Table 1 Main measures used in the restoration project. Main measure

Goal

Spatial range

Ecological bank protection Instream wetland (IW)

To stabilize the banks To improve hydrologic continuity and purify water To stabilize the banks and provide sheltering habitats To alter the flow pattern and increase water aeration To diversify instream habitats

Entire, continuous restoration area (1000 m) One IW in each of the upstream, midstream, and downstream restoration areas (150 m)

Groin (GR) Artificial drop (AD) Boulder placement (BP)

Cut banks of the curved subsegments and two sides of the straight subsegments (upstream and midstream restoration areas, 400 m) Set up in a scattered manner (upstream and midstream restoration areas, 700 m) Set up in various locations in the straight subsegments (downstream restoration area, 300 m)

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macroinvertebrates at the five kind of sample sites.

evenness index (Pielou, 1966).

2.3.1. Physical habitat measurements When monitoring the physical habitat quality, the streambed substratum was sampled at the five kind of sample sites (four kind of restored sample sites and one UC sample site) using a fixed-area frame, a square frame made of a thin iron plate. This frame had a sampling area of 1/16 m2 and was equipped with a peg at each of the four corners, which was used to fix the frame onto the stream bed. During the sampling process, the fixed-area frame was placed on the streambed substratum, and the corner pegs were inserted into the substratum. Afterwards, a shovel was used to excavate the substratum within the fixed-area frame to a depth of 20 cm. Every kind of sample sites consisted of three sample sites (n = 3). Three duplicate samples were collected from each sample site at the same time. The substratum samples were transported back to the laboratory and sieved using standard sieves with various mesh sizes after nature drying. The substratum was classified into four classes based on the particle size: class I (> 5 mm), class II (2–5 mm), class III (0.45–2 mm), and class IV (< 0.45 mm). Subsequently, each class of the substratum was weighed and subjected to a particle-size distribution analysis. Then, the physical habitat suitability index (K) was calculated (Peng and Zhang, 2005).

2.4. Data analysis All the data were subjected to Levene's normality test. If the data were found not to conform to normality, they were then subjected to a logarithmic transformation. A two-way analysis of variance (ANOVA) was performed to analyze the effects of the restoration measure, time, and restoration measure × time interaction on the physical habitat quality (K and proportion of the substratum belonging to each particlesize class) and the benthic macroinvertebrate community indices (taxon richness, density, Shannon–Wiener diversity index and Pielou's evenness index). The restoration measure (IW, GR, AD, or BP) and time (year and month) were treated as independent variables. One-way ANOVA with post hoc multiple comparison tests (Tukey’s tests) was performed to further analyze the differences in the physical habitat quality and benthic macroinvertebrate community indices caused by different lengths of time for the same measure as well as the differences caused by different measures that occurred after the same length of time after implementation. Pearson's correlation analysis was performed to examine the relation between benthic macroinvertebrates and physical habitat quality. The results were shown in the form of the Pearson's correlation coefficient r. The significance level P was set to 0.05. All analyses were performed using SPSS 18.0.

n

ϕ ∑ Ni × Pi K=

i=1

10

(1)

3. Results

where K is the physical habitat suitability index; φ is a flow velocity correction factor (flow velocities in normal seasons are classified into four ranges, namely > 1.5 m/s, 1–1.5 m/s, 0.5–1 m/s, and < 0.5 m/s; φ is set to 1, 2, 3, and 4 when one, two, three, and four flow velocity ranges exist in the target subsegment, respectively); i is the particle-size class; n is the total number of particle-size classes; Ni is the weight of class i (Ni = 6, 3, 1 and 0 for class I (> 5 mm), class II (5–2 mm), class III (2–0.45 mm), and class IV (< 0.45 mm), respectively); and Pi is the mass percentage of the substratum belonging to class i.

3.1. In-stream habitat changes Within the five-year observation period, the K was significantly affected by the restoration measure (F4,30 = 60.66, P = 0.000), time (F2,30 = 30.73, P = 0.000), and restoration measure × time interaction (F8,30 = 4.09, P = 0.002), as shown in Fig. 2A. Compared with the UC sample site, the physical habitat quality at each restored sample site was significantly higher in each of the three monitoring years. In 2010, only the AD and BP measures significantly improved the K (by 221% and 201%, respectively; F2010 (4,10) = 16.458, P = 0.000) compared with the UC sample site. In 2011, the AD and BP measures still had the most significant ameliorating effects on the substratum (they improved the K by 403% and 298%, respectively; F2011 (4,10) = 8.924, P = 0.002). In 2014, the four restoration measures all significantly improved the K, but the restorative effects varied drastically among them (F2014 (4,10) = 182.311, P = 0.000). The K was the highest at the AD sample site, followed by the BP, IW, GR, and UC sample sites (Fig. 2A). In 2014, the physical habitat quality at the AD sample site was 6.54 times that at the UC sample site. As the restoration time increased, the variation in the K at the sample sites restored by the different measures exhibited different trends (Fig. 2A). The K at the AD (FAD(2,6) = 19.276, P = 0.002) and BP (FBP(2,6) = 14.632, P = 0.005) sample sites improved significantly as the restoration time increased. The K at the IW (FIW(2,6) = 3.989, P = 0.079) and GR (FGR(2,6) = 1.038, P = 0.410) sample sites improved slowly as the restoration time increased, but not statistically significant. The K at the UC sample site first improved and then deteriorated, exhibiting no significant uniform trend in variation (FUC(2,6) = 2.923, P = 0.130). Water flow and substratum particle-size composition were found to significantly affect the benthic macroinvertebrate habitat quality in the stream. In this study, the flow conditions varied with the restoration measure and the year. In 2010, the flow rates in the habitats at all sample sites fell within one range (< 0.5 m/s), whereas in 2011 and 2014, the flow rates in the habitats at the AD and RP sample sites were found to fall in two different ranges (< 0.5 m/s and 0.5–1.0 m/s). Coarse substratum (> 5 mm), the factor with the largest weight affecting the K for the benthic macroinvertebrate community, was significantly affected by the restoration measure (F4,30 = 243.86,

2.3.2. Benthic macroinvertebrates sampling While collecting streambed substratum samples, three duplicate benthic macroinvertebrate samples (n = 3) were also collected from each sample site at the same time. Various sampling methods were used based on the streambed substratum type and the flow conditions. A 1/ 16-m2 Peterson grab sampler was used to collect samples from finesandy and silty habitats (e.g., the IW and inter-GR slow-flow zone). A fixed-area frame (25 cm × 25 cm) was used to collect samples from riffle habitats covered by a large amount of gravel (Zhang et al., 2007). During the sampling process, the fixed-area frame was placed on the streambed substratum, and its corner pegs were inserted into the substratum to prevent the fixed-area frame from moving under the impact of the water flow. Then, a handheld net was placed downstream of the fixed-area frame to prevent the benthic macroinvertebrates from drifting away as the substratum was being excavated within the fixedarea frame (to a depth of 20 cm), which would affect the results. The substratum sample and the sample in the handheld net were subsequently rinsed in a bucket and then sieved using a 40-mesh sieve. Afterwards, the benthic macroinvertebrate–organic detritus mixture was placed in a sealable bag, and 95% alcohol was added to the bag to fix and store the mixture. The mixture samples were transported to the laboratory and then sorted and stored. In the laboratory, the benthic macroinvertebrates were identified to the lowest practicable taxonomic level (i.e., genus and species level) under a stereomicroscope (Morse et al., 1994; Thorp and Covich, 2009), with the exception of Diptera (family, subfamily or tribe level) and Oligochaeta (family level). Individuals within each taxon were then counted. The following benthic macroinvertebrate community structure indices were used: taxon richness, density (individuals/m2), Shannon–Wiener diversity index (Shannon and Weaver, 1949), and Pielou's 255

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Fig. 2. The benthic physical habitat quality at five kind of sample sites. (A) The physical habitat suitability index and (B) the substratum particle-size composition in 2010, 2011, and 2014. UC: unresotred control site. IW: instream wetland site. GR: groin site. AD: artificial drop site. BP: boulder placement site. Different lowercase letters signify the significant differences among the different measures in the same year. Different uppercase letters signify the significant differences among the different years for the same measure. Error bars represent ± SE.

appeared at the riffles downstream of the BP and AD sample sites in 2011 and 2014, whereas mollusks only appeared in the fine-sandy and muddy habitats in the slow-flow zones at the IW and GR sample sites.

P = 0.000), time (F2,30 = 87.89, P = 0.000), and restoration measure × time interaction (F8,80 = 13.31, P = 0.000), as shown in Fig. 2B. In 2010, no significant difference was observed in the proportion of the substratum belonging to the > 5-mm-particle size class among the habitats at the UC, IW, and GR sample sites, whereas the proportion was much higher in the habitats at the BP and AD sample sites than at the other three sample sites (F2010(4,10) = 127.61, P = 0.000). In 2011 and 2014, the proportion of the substratum belonging to the > 5-mmparticle size class was significantly higher in the habitat at each of the four restored sample sites than the habitat at the UC sample site (F2011(4,10) = 42.68, P = 0.000; F2014(4,10) = 110.67, P = 0.000; Fig. 2B).

3.2.2. Density In 2010, the density of the benthic macroinvertebrates at each of the IW and GR sample sites was significantly higher than the density at the UC, AD, and BP sample sites (F4,10 = 145.529, P = 0.000; Fig. 3B). In 2011, the density of benthic macroinvertebrates was the highest at the IW sample site, with a significant difference among the sample sites (F4,10 = 814.974, P = 0.000; Fig. 3B). In 2014, the density of benthic macroinvertebrates was the highest as the IW sample site, followed by the density at the GR, AD, BP, and UC sample sites (Fig. 3B). Because of the contribution of the taxa of Tubificidae and Chironomidae, the density of benthic macroinvertebrates was the highest at the IW sample site in each of the three years. During the five-year observation period, the density of benthic macroinvertebrates first increased and then decreased at the UC and BP sample sites, first decreased and then increased at the IW and GR sample sites, and only slowly, but continuously, significantly increased at the AD sample site (Fig. 3B).

3.2. Benthic macroinvertebrate community changes During the five-year observation period, 4311 benthic macroinvertebrates were collected, belonging to 49 taxa (including five taxa of Oligochaeta, four taxa of Hirudinea, five taxa of Ephemeroptera, four taxa of Hemiptera, four taxa of Coleoptera, four taxa of Odonata, 18 taxa of Diptera, one taxon of Hydrachnidia, and four taxa of molluscs). The taxa of Oligochaeta and Diptera (Chironomidae and Tipulidae) were the dominant taxa. The taxon richness, density, Shannon–Wiener diversity index, and Pielou's evenness index of the benthic macroinvertebrate community were significantly affected by the restoration measure, time, and the restoration measure × time interaction (P < 0.001 for all cases, Fig. 3).

3.2.3. Diversity In 2010, 2011, and 2014, the Shannon–Wiener diversity index at each of the four restored sample sites was significantly higher than that at the UC sample site (P < 0.001 for all cases, Fig. 3C). In 2010 and 2011, a consistent trend was observed among the sample sites: the Shannon–Wiener diversity index at the AD and BP sample sites was the highest, followed by that at the IW and GR sample sites, and the Shannon–Wiener diversity index at the UC sample site was the lowest (Fig. 3C). In 2014, the Shannon–Wiener diversity index at the IW sample site further increased to a level significantly higher than that at the GR sample site (F4,10 = 142.932, P = 0.000; Fig. 3C). During the five-year observation period, the Shannon–Wiener diversity index of benthic macroinvertebrates increased significantly at all four restored sample sites (P < 0.01 for all cases, Fig. 3C). By 2014, the Shannon–Wiener diversity index had been the highest at the AD and BP sample sites (3.067 and 2.884, respectively), increased most (72%) at the IW sample site, and increased slightly at the UC sample site (Fig. 3C).

3.2.1. Taxon richness In 2010, the taxon richness of the benthic macroinvertebrates at the BP sample site increased most dramatically (F4,10 = 4.773, P = 0.004), whereas the effects of the IW and GR measures were not statistically significant (Fig. 3A). In 2011, the effects of the BP measure remained outstanding; in addition, the benthic taxon richness in the habitat at the IW sample site further recovered to a level significantly higher than that in the habitat at the UC sample site (F4,10 = 10.658, P = 0.001; Fig. 3A). In 2014, the benthic taxon richness in the habitat at each of the AD, BP, and IW sample sites was significantly higher than that in the habitat at the UC sample site (F4,10 = 24.567, P = 0.000; Fig. 3A). At the IW, AD, and BP sample sites, the benthic taxon richness continuously increased during the five-year observation period (P < 0.01 for all cases). The benthic taxon richness increased the most (by 238%) at the AD sample site (Fig. 3A). However, at the UC and GR sample sites, the benthic taxon richness exhibited no significant recovery trend. In regard to the specific taxa composition, taxa of Tubificidae and Chironomidae were the dominant taxa at each sample site in every year (Fig. 4). However, insects of Ephemeroptera (Heptageniidae and Oligoneuriidae) that require higher habitat quality and flow condition only

3.2.4. Evenness In 2010, the Pielou's evenness index at the IW sample site was significantly lower than that at the other four sample sites (Fig. 3D). In 2011, the evenness at each of the four restored sample sites increased considerably and was significantly higher than that at the UC sample site (by 35–63%; F4,10 = 100.237, P = 0.000; Fig. 3D). A similar trend was found among the evenness at the sample sites in 2014; in addition, 256

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Fig. 3. The (A) taxon richness, (B) density, (C) Shannon–Wiener diversity index, and (D) Pielou's evenness index of macroinvertebrates at five sample sites in 2010, 2011, and 2014. Monitoring data of benthic macroinvertebrates collected in spring in the second (May 2010), third (May 2011), and sixth (May 2014) years after the implementation of the restoration project. UC: unresotred control site. IW: instream wetland site. GR: groin site. AD: artificial drop site. BP: boulder placement site. Different lowercase letters signify significant differences among different measures in the same year; Different uppercase letters signify significant differences among different years for the same measure. Error bars represent ± SE.

3.2.5. Effects of the flood on benthic macroinvertebrates at the restored sample sites In 2010, the results derived from the four times of sampling show that the four indices of benthic macroinvertebrates were significantly affected by the restoration measure, month, and measure × month interaction (P < 0.001 for all cases, Fig. 5). The lowest taxon richness and diversity of benthic macroinvertebrates at the UC, IW, AD, and BP sample sites in 2010 occurred

the effects of the four restoration measures could be further notably distinguished: the evenness at the BP sample site was the highest, followed by that at the AD, GR, IW, and UC sample sites (F4,10 = 68.845, P = 0.001; Fig. 3D). During the five-year observation period, the Pielou's evenness index of the benthic macroinvertebrates generally decreased at the UC sample site and significantly but slowly increased at the four restored sample sites (P < 0.01 for all cases, Fig. 3D).

Fig. 4. The proportions of taxa in 2010, 2011, and 2014. UC: unresotred control site. IW: instream wetland site. GR: groin site. AD: artificial drop site. BP: boulder placement site. EPT: Ephemeroptera, Plecoptera, and Trichoptera. 257

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Fig. 5. Effects of the flood on the benthic macroinvertebrate communities in the habitat at each of the sample sites restored by various measures and the control sample site. (A) Taxon richness, (B) Density, (C) Shannon–Wiener diversity index, and (D) Pielou's evenness index of macroinvertebrates in May, August, September, and October 2010. Monitoring data of benthic macroinvertebrates collected in 2010; a 30-year flood took place on July 27. UC: unresotred control site. IW: instream wetland site. GR: groin site. AD: artificial drop site. BP: boulder placement site. Different lowercase letters signify the significant differences among different measures in the same month. Different uppercase letters signify the significant differences among different months for the same measure. Error bars represent ± SE.

in August, the month after a flood. In particular, benthic macroinvertebrates vanished completely at the UC and IW sample sites in August. In contrast, the data show significantly higher taxon richness and diversity of benthic macroinvertebrates at the GR sample site in August (the highest in 2010) than in May (Fig. 5A and C). By September, the taxon richness had recovered to the pre-flood level at each of the UC and IW sample sites. By October, the taxon richness had also recovered to the pre-flood level at each of the BP and AD sample sites. Moreover, the Shannon–Wiener diversity index had recovered to the pre-flood level by October at the BP sample site; in comparison, this index still had not recovered to the pre-flood level by October (three months after the flood) at each of the UC, IW, and AD sample sites. Compared with taxon richness and diversity, the density of benthic macroinvertebrates recovered more rapidly after flood. The density of benthic macroinvertebrates had reached or exceeded the pre-flood level (the level in May) by September at each of the five sample sites (Fig. 5B). The evenness of the benthic macroinvertebrate community at each sample site had reached or approached the pre-flood level (the level in May) two to three months after the flood (Fig. 5D).

Table 2 Relations between the benthic macroinvertebrate community indices and the physical habitat quality. The data presented are Pearson correlation coefficients. Habitat quality

Taxon richness

Density

Diversity

Evenness

K > 5 mm (%)

0.864* 0.729*

−0.128 −0.126

0.910* 0.855*

0.730* 0.775*

Note: K indicates physical habitat suitability index. “ * ” indicates that these two indices are extremely significantly correlated (p < 0.001).

4. Discussion Many uncertainties are associated with the restorative effects of instream measures on stream habitats and benthic macroinvertebrate communities, as well as with the involved restoration processes. In this study, a restoration project was designed for and conducted in a degraded agricultural headwater stream. Four different instream measures were implemented to restore both the flow pattern and substratum composition to a near-natural condition and thus to recover aquatic biocenosis. The results show that the instream restoration measures played a significant positive role in improving the physical habitat quality and benthic macroinvertebrate community in the agricultural headwater stream and that the restoration of the physical habitat quality significantly positively facilitated the recovery of the benthic macroinvertebrate community. During the five-year observation period, the habitat quality continuously improved at the restored sample sites. In addition, the taxon richness and diversity of benthic macroinvertebrates at the restored sample sites also continuously increased at the same time. The AD and BP measures had the most noticeable positive effects on the taxon richness and diversity of the

3.3. Relations between physical habitat quality and benthic macroinvertebrates A correlation analysis was performed based on the physical habitat quality and benthic macroinvertebrate community index data collected in 2010, 2011, and 2014. The results show that the K and the proportion of the coarse substratum (> 5 mm) were both significantly positively correlated with the taxon richness, diversity, and evenness of the benthic macroinvertebrates and negatively, albeit not statistically significant, correlated with the density of benthic macroinvertebrates (Table 2). 258

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agricultural headwater streams. Instream restoration measures have been demonstrated relatively extensively as positive effects in habitat restoration; however, these measures have varying effects on aquatic organisms. For example, they have been found to have significantly positive effects by some researchers (e.g., Miller et al., 2010) and insignificantly positive effects by others (e.g., Palmer et al., 2010). Jähnig et al. (2010) examined research results with respect to 26 restored streams in Europe and found that the restoration measures were significantly effective in restoring stream habitats (substratum and water flow) but had weak restorative effects on benthic invertebrates. Kail et al. (2015) found that instream restoration measures were noticeably effective in restoring the richness/diversity of benthic macroinvertebrates. Miller et al. (2010) found that increasing the habitat heterogeneity could help increase the taxon richness of the benthic macroinvertebrates but was negligibly effective in increasing the community density. During the five-year observation period of this study, the taxon richness and diversity of benthic macroinvertebrate at the four restored sample sites continued to recover, particularly at the BP and AD sample sites. However, the trends in the density and evenness of the benthic macroinvertebrates varied among the sample sites restored by the different measures. These findings are consistent with the research results obtained by Miller et al. (2010). Jähnig et al. (2010) believed that the small scale (several hundred meters) of restoration is the main cause of poor restorative effects on benthic invertebrates. Of the 26 target streams studied by Jähnig et al. (2010), eight were agricultural streams similar to the stream restored in this study; in addition, the restoration measures implemented on these eight streams were only able to recover their meandering. In this study, to address the main problem of the agricultural stream (substratum degradation), instream measures were densely placed in a 1000-m-long segment (Fig. 1 and Table 1), thereby allowing these measures to complement one another and generate significant positive effects. Champoux et al. (2003) found that when restoration structures were built sparsely and at improper locations, their rehabilitating effects were difficult to realize, and the structures were also prone to damage. In this study, the instream restoration measures were densely placed, which should be an important cause of their significant positive and restorative effects. The reconstruction of riffles with a substratum composed of coarse sediment is a major factor that affects the restoration of benthic macroinvertebrate communities in agricultural headwater streams. The control of fine sediment should be treated as a priority in ecological restoration and management of agricultural streams (Wagenhoff et al., 2012). Extensive field studies and control experiments have demonstrated the negative effects of fine suspended particle and sediment increment on benthic invertebrate communities in streams (e.g., Matthaei et al., 2006; Townsend et al., 2008; Larsen et al., 2011; Wagenhoff et al., 2012). An increase in the coarse substratum will enhance the exchange between the surface and interstitial water, thereby positively affecting the benthic macroinvertebrate communities (Gayraud and Philippe, 2003; Muotka et al., 2002). In particular, coarse riffles are necessary in habitats for some benthic species (e.g., some species of Ephemeroptera), which are not distributed in areas with a fine sedimentary substratum (Sarriquet et al., 2007). In this study, Heptageniidae and Oligoneuriidae were only found on the coarse riffles downstream of an AD and BP in the third and sixth years after the implementation of the restoration project, whereas Ephemeroptera were never found at the UC sample site (Fig. 4). A correlation analysis reveals that in the agricultural headwater stream investigated in this study, physical habitat restoration was a major factor that affected the restoration of benthic macroinvertebrates (Table 2), demonstrating that for an agricultural headwater stream, the streambed substratum type and composition also significantly affect the species composition, diversity, and abundance of benthic macroinvertebrates (Crosa and Buffagni, 2002; Leitner et al., 2015).

benthic macroinvertebrates. The benthic macroinvertebrate community in the habitat at the GR sample site exhibited outstanding durability against an extreme hydrological event (a flood). The benthic macroinvertebrates in the habitat at the BP sample site recovered the most rapidly after the flood. 4.1. Effects of instream restoration measures on physical habitats Instream measures are capable of substantially improving the benthic physical habitat quality in agricultural headwater streams. During the five-year observation period, the physical habitat quality at the sample sites restored by the instream measures recovered noticeably, whereas no significant change occurred to the UC sample site (Fig. 2). By 2014, the AD measure had had the most significant positive effects on the physical habitat quality, followed by the BP measure, whereas the K at the IW and GR sample sites recovered slowly (Fig. 2). Measures involving the introduction of gravel have been extensively used in the improvement of spawning habitats for salmon (e.g., Pedersen et al., 2009; Pulg et al., 2011). In particular, medium-sized gravel is mainly introduced to artificially alter the streambed substratum particle size composition. In this study, boulders were placed in the stream to increase the number of rapids, thereby altering the streambed substratum particle size composition by relying on the selforganization process of the stream and eventually restoring riffle habitats with coarse sediment. In addition, boulder weirs can improve the stability of stream habitats and enhance their durability against extreme flood events (Danehy et al., 2016). In this study, the restorative effects of the instream boulder placement measure on the stream substratum conditions were close to those of the AD measure (Fig. 2). However, compared with the AD measure, the instream boulder placement measure was easier to implement and cost less. Therefore, consideration should be given to this measure when restoring agricultural headwater streams. Instream restoration measures are capable of continuously restoring degraded agricultural headwater stream habitats for more than six years after implementation. Research on the time required for a degraded stream to reach a new, more ideal, near-natural balanced state after a series of evolutionary processes following implementation of a restoration project remains inconclusive (Januschke et al., 2014). In addition, enormous uncertainties are associated with the biological effectiveness of instream habitat restoration measures (Miller et al., 2010; Stewart et al., 2009). Kail et al. (2015) found that a restoration project's age was the most important factor in its effectiveness. However, the time factor has a nonlinear effect. As time progresses, the restorative effects of a restoration project on a habitat may decline or even disappear (Kail et al., 2015). An interpretative hypothesis for this phenomenon is that a restored instream habitat structure is unable to last for a long period, resulting in a recurrence of the biodeterioration within several years after the implementation of the restoration project (Palmer et al., 2010; Whiteway et al., 2010). Kondolf and Micheli (1995) believed that monitoring is necessary for at least ten years to determine whether a restoration project is effective. However, due primarily to limited project financing that generally ceases soon after a project is completed (Buchanan et al., 2014; Champoux et al., 2003), few monitoring studies have examined a period longer than five years (Friberg et al., 2014). The results obtained from this study show that the habitat quality in the agricultural headwater stream was still undergoing the recovery process six years after the implementation of the restoration project (Fig. 2). This study provides valuable information on the restoration process of degraded agricultural stream habitats. 4.2. Effects of instream restoration measures on benthic macroinvertebrate communities Densely placed instream measures can effectively improve the taxon richness and diversity of benthic macroinvertebrate communities in 259

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4.3. Effects of floods in the restored stream

in restoring the ecological conditions of degraded agricultural headwater streams on longer time scales.

A combination of a variety of restoration measures has larger positive effects on the response of stream ecosystems to extreme hydrological events. Restoring the durability and resilience of the ecosystem is a key goal of an ecological restoration project (Lake, 2013; Palmer et al., 2005). A dynamic ecosystem changes constantly. As a result, the effectiveness of a stream restoration project may vary significantly over time (Lake et al., 2007). Therefore, a stream ecosystem restoration project should aim to restore the self-organizing capabilities of the stream to create and maintain habitats and bring about a near-natural process in the stream instead of creating a separate internal stream structure (Kristensen et al., 2014; Roni et al., 2008). Kondolf and Micheli (1995) believed that extreme climate events and flow conditions during the monitoring of the restored sample sites in the stream are essential in determining the effectiveness of a restoration project. In this study, the restoration project suffered a 30-year flood event in July 2010, which provided a valuable opportunity for monitoring the effectiveness of the restoration project. The effects of the GR measure on the habitat quality were found to be ordinary during normal seasons (Fig. 3). However, after the flood, the GR measure exhibited outstanding positive effects on the habitat (Fig. 5). After sustaining a direct impact from the flood, the GR sample site (sampled in August) was inhabited by more benthic macroinvertebrates in both number of taxa and quantity than any other sample site. In addition, the highest taxon richness and diversity of benthic macroinvertebrates of the year (2010) occurred in the habitat at the GR sample site (an inter-GR slow-flow zone) in August (the month after the flood). This indicates that the inter-GR slow-flow zone provided a major shelter for benthic macroinvertebrates during the flood, thereby providing a possibility for and ensuring the restoration of the benthic macroinvertebrate community in the entire stream after the flood. As microhabitats are important to the benthic macroinvertebrate community structure in a stream (Beisel et al., 1998), a single restoration measure may not be able to restore the key habitat elements or the spatial and temporal habitat sequences, which are closely related to the life cycle of the target organisms (Lepori et al., 2005; Lorenz et al., 2009). Therefore, a target-specific stream restoration scheme involving a combination of restoration measures is vital to successful stream ecosystem restoration. Finally, the major shortcoming of this study was that we couldn't collect data before the restoration project because of the adverse effects of project sponsor. Although other research indicates that owing to logistical and inancial constraints, before-after-control-impact (BACI) studies are rarely implemented (Rumps et al. 2007; Miller et al. 2010), the results of many case studies are still instructive to evaluate restorative effects and improve restoration project. Moreover, we are carrying out a further long-term monitoring and adding other control sites to make up for the shortcoming of experimental design in this study.

Acknowledgments This work was supported by National Natural Science Foundation of China (grant numbers 41601576, 41501566, 31770508); China National Special Funds of Science and Technology for Control and Remediation of Water Pollution (grant number 2017ZX07101-003); Special Funds of the State Environmental Protection Public Welfare Industry (grant number 201509040); National Key Research and Development Program of China (grant number 2016YFC0500407); Foundation of Education Department of Jilin Province (grant number 2014B050); The Open Fund of the State Environmental Protection Key Laboratory of Wetland Ecology and Vegetation Restoration, Northeast Normal University (grant number 130026520); the National Geographic Air and Water Conservation Fund (grant number GEFC2113); and the Program of Introducing Talents of Discipline to Universities (grant number B16011). References Allan, J.D., 2004. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annu. Rev. Ecol. Evol. Sci. 35, 257–284. Balderas, E.C.S., Grac, C., Berti-Equille, L., Hernandez, M.A.A., 2016. Potential application of macroinvertebrates indices in bioassessment of Mexican streams. Ecol. Indic. 61, 558–567. Baumgartner, S.D., Robinson, C.T., 2017. Short-term colonization dynamics of macroinvertebrates in restored channelized streams. Hydrobiologia 784, 321–335. Beisel, J.N., Usseglio-Polatera, P., Thomas, S., Moreteau, J.C., 1998. Stream community structure in relation to spatial variation: the influence of mesohabitat characteristics. Hydrobiologia 389, 73–88. Bernhardt, E.S., Palmer, M.A., Allan, J.D., Alexander, G., Barnas, K., Brooks, S., Carr, J., Clayton, S., Dahm, C., Follstad-Shah, J., 2005. Synthesizing US river restoration efforts. Science 308, 636–637. Bernhardt, E.S., Palmer, M.A., 2011. River restoration: the fuzzy logic of repairing reaches to reverse catchment scale degradation. Ecol. Appl. 21, 1926–1931. Bonada, N., Prat, N., Resh, V.H., Statzner, B., 2006. Developments in aquatic insect biomonitoring: a comparative analysis of recent approaches. Annu. Rev. Entomol. 51, 495–523. Brederveld, R.J., Jähnig, S.C., Lorenz, A.W., Brunzel, S., Soons, M.B., 2011. Dispersal as a limiting factor in the colonization of restored mountain streams by plants and macroinvertebrates. J. Appl. Ecol. 48, 1241–1250. Buchanan, B.P., Nagle, G.N., Walter, M.T., 2014. Long-term monitoring and assessment of a stream restoration project in central New York. River Res. Appl. 30, 245–258. Champoux, O., Biron, P.M., Roy, A.G., 2003. The long-term effectiveness of fish habitat restoration practices: Lawrence Creek. Wisconsin. Ann. Assoc. Am. Geogr. 93, 42–54. Covich, A.P., Austen, M.C., BÄRlocher, F., Chauvet, E., Cardinale, B.J., Biles, C.L., Inchausti, P., Dangles, O., Solan, M., Gessner, M.O., Statzner, B., Moss, B., 2004. The role of biodiversity in the functioning of freshwater and marine benthic ecosystems. Bioscience 54, 767–775. Crosa, G., Buffagni, A., 2002. Spatial and temporal niche overlap of two mayfly species (Ephemeroptera): the role of substratum roughness and body size. Hydrobiologia 474, 107–115. Danehy, R.J., Moberly, E.R., Reber, P.L., Swanson, S., Liebhardt, S., Sheahan, J., 2016. Stability and thermal impacts of channel-spanning boulder weirs in Mosby Creek. Northwest Sci. 90, 411–420. Dudgeon, D., Arthington, A.H., Gessner, M.O., Kawabata, Z.I., Knowler, D.J., Lévêque, C., Naiman, R.J., Prieur-Richard, A.H., Soto, D., Stiassny, M.L.J., Sullivan, C.A., 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biol. Rev. 81, 163–182. Erwin, S.O., Jacobson, R.B., Elliott, C.M., 2017. Quantifying habitat benefits of channel reconfigurations on a highly regulated river system, Lower Missouri River, USA. Ecol. Eng. 103, 59–75. Feld, C.K., Birk, S., Bradley, D.C., Hering, D., Kail, J., Marzin, A., Melcher, A., Nemitz, D., Pedersen, M.L., Pletterbauer, F., Pont, D., Verdonschot, P.F.M., Friberg, N., 2011. From natural to degraded rivers and back again: a test of restoration ecology theory and practice. Adv. Ecol. Res. 44, 119–209. Flavio, H.M., Ferreira, P., Formigo, N., Svendsen, J.C., 2017. Reconciling agriculture and stream restoration in Europe: a review relating to the EU Water Framework Directive. Sci. Total Environ. 596, 378–395. Frainer, A., Polvi, L.E., Jansson, R., McKie, B.G., 2018. Enhanced ecosystem functioning following stream restoration: the roles of habitat heterogeneity and invertebrate species traits. J. Appl. Ecol. 55, 377–385. Friberg, N., Baattrup-Pedersen, A., Kristensen, E.A., Kronvang, B., Larsen, S.E., Pedersen, M.L., Skriver, J., Thodsen, H., Wiberg-Larsen, P., 2014. The River Gelså restoration revisited: habitat specific assemblages and persistence of the macroinvertebrate community over an 11-year period. Ecol. Eng. 66, 150–157. Gayraud, S., Philippe, M., 2003. Influence of bed-sediment features on the interstitial

5. Conclusions This study shows that a scheme involving densely placed instream restoration measures has significant positive effects on both the physical habitat quality and benthic macroinvertebrate community in an agricultural headwater stream. On the time scale used in this study (two to six years after the implementation of the restoration project), the instream restoration measures facilitated continuous, substantial restoration of the physical stream habitats, thereby bringing about continuous, significant improvements in the taxon richness and diversity of the benthic macroinvertebrate community. The effectiveness of habitat restoration projects in restoring stream ecosystems is affected by the interaction between the restoration measure type and time. Therefore, further research is necessary to determine whether various types of restoration measures and overall restoration schemes will be effective 260

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