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Characteristics of Macroinvertebrates Food Webs affected by Dry Channel in an Intermittent Stream System of the Echi River in Japan
Abstract
The purpose of study is to identify trophic pathways from organic matter to macroinvertebrates in terms of the consumer and to characterize the food webs in an intermittent stream system of the Echi River in Japan. The δ13C values of macroinvertebrates and their potential food sources indicated the scraper (Psephenoides spp., Ecdyonurus levis) and collector-gatherer (Ephemera strigata, Paraleptonphlebia chocolata) feed on periphyton and POM (particulate organic matter) in situ. Davidius lunatus, and Hexatoma spp., which were identified as predators, may feed upon Ephemera strigata and Stenelmis larvae, respectively. At station characterized by seepage water, the δ15N values of Ecdyonurus levis, Lymnaea auricularia, and Rhyacophila nigrocephala larva probably showed relatively lower values according to its diets. Even in homogenous species, the trophic pathways of macroinvertebrates in situ exhibited considerable variation; this reflected the trophic pathways from organic matter to the consumer depending on habitat characteristics in stream.
Keywords:
Functional Feeding Groups, Potential Food Sources, Trophic Pathway1. INTRODUCTION
Lotic food webs mainly derive their energy from allochthonous and autochthonous (algae) organic sources (e.g. Vannote et al., 1980; Thorp and Delong, 1994; Ishikawa et al., 2010). Food webs in adjacent habitats and ecosystems may be strongly linked by fluxes of nutrients, detritus, or organisms (Polis et al., 1997). The spatial and temporal scales of connections between food webs were known only fragmentary knowledge. Such information is crucial to understanding the processes that control the dynamics of local populations, communities, and ecosystems, as well as the fate of fluxes of materials and individuals across habitat, ecosystem, and landscape boundaries (Polis et al., 1997; Laurance et al., 2001). The mobility of limiting nutrients, organic matter, and organism characteristic of lotic environments suggests that such linkages are especially strong in river food webs. For example, detrital carbon inputs from terrestrial to stream food webs are important in many stream ecosystems (Hynes, 1975). Organic carbon sources for lotic food webs may be derived from multiple sources, including local algal production and particulate and dissolved organic matter transported from upstream habitats. Consequently, the spatial scales of trophic interactions in rivers are largely unknown (Cooper et al., 1997). Furthermore, relatively few studies have been conducted on food webs related to spring ecosystems. Spring streams are closed ecosystems and arise from seepage areas; in addition, primary production is relatively high in these small spring streams, which are exposed to sunlight, algae-rich, and contain adequate concentrations of nitrogen and phosphate (Allan, 1995).
The aims of this study were to identify the trophic pathways from organic matter to macroinvertebrates in terms of consumers, using stable isotopes (carbon and nitrogen); and to characterize the food webs in an intermittent stream system of the Echi River in Japan.
2. MATERIALS AND METHODS
2.1 Study Stations
The Echi River (35°0´N, 136°0´E), one of the major rivers flowing into Lake Biwa, is 50 km long and has a catchment area of approximately 204 km2 (Fig. 1b). For land use, the proportion of forest occupied more than 80% of the river basins, and those of paddy fields and other farmland are 8.5%, and 0.5%, respectively (these values were calculated using GIS; Yamada et al., 2011). The upstream area is a steep mountainous area while the downstream area is flat land. During the dry season, the Echi River dries up in an area located 11∼17 km from the river mouth (Fig. 1c). We selected four random sampling stations along the river. Marked seepage was observed at the end of the dry channel. We established four stations (ES: Echi River Station; i.e. ES 1, ES 2, ES 3, and ES 4) according to horizontal distribution. This study was conducted in two stations upstream (ES 1 and ES 2) and two stations downstream (ES 3 and ES 4) of the dry channel area in the Echi River (Fig. 1).
![Fig. 1. Fig. 1.](/xml/05046/JCCR_2015_v6n3_167_f001.jpg)
(a) Map of the study area in Japan, (b) Map of the study stations along the Echi River, (c) Longitudinal section of the Echi River. ES 1 and ES 2 are upstream, while ES 3 and ES 4 are downstream of the dry channel in the river (modified by Shin et al., 2013).
In terms of the general environmental parameters, WT and pH concentrations were greatly higher at ES 4 (28℃, pH 8.6) than at ES 1∼ES 3 (24∼25℃, pH 7.1∼7.2), DO concentrations at ES 3 (6.5 mgL-1) were relatively lower than those at the other stations (9.0∼9.9 mgL-1)(Shin et al., 2013).
2.2 Sample Collection and Preparation
Benthic macroinvertebrates were collected at the 4 stations in August 2008. We conducted sampling with three replicates, using a square Surber net sampler (250 μm mesh; size, 0.25 m2). All biota were separated from other material and sorted in the laboratory. Identification was mostly performed using a stereoscopic microscope at 10∼40×magnification.
Macroinvertebrates were identified primarily at the species and genus level. Among the collections from sampling stations, common taxa were analyzed and distributed widely in order to provide a better comparison at each station. The taxa included Psephenoides spp., Ecdyonurus levis, Ephemera strigata, Davidius lunatus, Lymnaea auricularia, Paraleptophlebia cho-colata, Stenelmis spp., Rhyacophila nigrocephala, Hexatoma spp. Based on their relatively high abundance, these macroinvertebrates were selected for the following analyses.
2.3 Analysis of Stable Isotope Ratios
Macroinvertebrates were collected from all of the sampling stations. The macroinvertebrates were maintained in filtered river water at 5℃ for 24 h to allow them to eliminate their gut contents. The samples were defatted in a solution of chloroform and methanol (2:1) according to the method of Folch et al. (1957). Defatting was carried out in order to avoid variations in the δ13C because of the differences according to species in the concentration of isotopically lighter lipids (Focken and Becker, 1998), and the samples were then freeze-dried and stored in a freezer at -20℃ until the stable isotope ratios were analyzed.
The potential food sources included suspended particulate organic matter (SPOM), benthic particulate organic matter (BPOM), and periphyton. For the analysis of stable isotopes, SPOM was collected by filtering the river water through GF/F glass fiber filters, BPOM was collected from the streambed using sieves with mesh sizes: <250 μm, and periphyton was collected by scouring the surface of stones with quadrat (5 cm × 5 cm) using a brush. SPOM, BPOM and periphyton samples were acidified with 1 N HCl to remove carbonates. All the samples were freeze-dried and stored in a freezer at -20℃ until the stable isotope ratios were analyzed.
Three replicate measurements of the carbon and nitrogen isotope ratios were taken for each sample. Generally 2 to 250 individuals of the same species were compiled in each sample. The value of all species were measured as an average of compiled individuals (Psephenoides spp.: 15∼50, Ecdyonurus levis: 20∼140, Ephemera strigata: 60∼90, Davidius lunatus: 2∼3, Lymnaea auricularia: 2∼4, Paraleptophlebia chocolate: 190∼250, Rhyacophila nigrocephala: 15∼30, and Hexatoma spp: 6∼10 individuals / 1 sample).
The carbon and nitrogen stable isotope ratios of the samples were measured with an elemental analyzer EA1108 (Fisons) connected to a mass spectrometer (Delta S, Finnigan MAT) with an interface (Conflo II, Finnigan MAT) with three replicates. The results are reported using delta notation calculated as: δ13C or δ15N (‰) = (Rsample / Rstandard - 1) × 1000. The R is the 13C/12C or 15N/14N ratio for δ13C or δ15N, respectively. The standards for δ13C or δ15N were used Pee Dee Belemnite (PDB) and air nitrogen, respectively. The analysis errors for δ13C or δ15N were within ± 0.2‰.
Analysis of trophic relationships using stable isotope ratio is generally based on the premise that δ13C enrichment during trophic transfer is slight (0.8 ± 1.1‰, mean ± SD), whilst that of δ15N is substantial (3.4 ± 1.1‰) (DeNiro and Epstein, 1978; Minagawa and Wada, 1984; Post, 2002).
3. RESULTS
The mean δ13C and δ15N values of macroinvertebrates (ranging from -28.7 to -19.4‰ and 2.3 to 9.9‰, respectively) differed among stations and species (Table 1). The consumers such as Psephenoides spp., Ecdyonurus levis, Ephemera strigata, Rhyacophila nigrocephala, and Davidius lunatus were common to both ES 1 and ES 2. The mean δ13C values of these species showed gradually increasing pattern from ES 1 to ES 2 (Psephenoides spp.: -23.1 to -21.2‰, Ecdyonurus levis: -28.7 to -25.1‰, Ephemera strigata: -25.6 to -23.3‰, R. nigrocephala: -23.8 to -21.1‰, and Davidius lunatus: -24.5 to -23.9‰). Although the mean δ15N values of Psephenoides spp., Ecdyonurus levis, and Ephemera strigata did not differ among stations (ranging from 2.3 to 2.7‰, 4.5 to 4.9‰, and 5.2 to 5.9‰, respectively), those of R. nigrocephala and Davidius lunatus displayed increasing from ES 1 to ES 2 (5.4 to 6.9‰ and 5.2 to 6.1‰, respectively). Psephenoides spp. and were also observed at ES 4. The mean δ13C values of Psephenoides spp. at ES 2 were relatively higher, whilst those of R. nigrocephala at ES 4 were relatively higher than at the other stations.
The δ13C values of Ecdyonurus levis and Lymnaea auricularia little differ at ES 2 and ES 3 (ranging from -26.1 to -24.6‰ and -22.0 to -21.7‰, respectively), whilst the mean δ15N values of these species tended to decrease from ES 2 to ES 3 (4.9 to 2.5‰ and 5.6 to 2.5‰, respectively). The δ13C and δ15N values of Paraleptophlebia chocolata showed increasing pattern from ES 3 to ES 4 (-23.9 to -19.4‰ and 3.1 to 6.1‰, respectively). Moreover, the δ15N values of macroinvertebrates at ES 3 (ranging from 2.4 to 3.1‰) were relatively lower, whilst those at ES 4 (ranging from 4.2 to 9.9‰) were relatively higher than at the other stations. We used data of Shin et al. (2013) in relation to carbon and nitrogen stable isotope ratio for SPOM, BPOM, and periphyton, in order to reveal relationship between macroinvertebrates and their food sources (Fig. 2).
![Fig. 2. Fig. 2.](/xml/05046/JCCR_2015_v6n3_167_f002.jpg)
Mean carbon and nitrogen stable isotope plots of macroinvertebrates and their potential food sources at the respective stations along the Echi River. The square frames indicate the classification of aquatic insects according to functional feeding groups. The open triangles indicate ES 1, gray triangles indicate ES 2, open squares indicate ES 3, and black squares indicate ES 4. SPOM: suspended particulate organic matter, BPOM: benthic particulate organic matter, 1: Rhyacophila nigrocephala 2: Ecdyonurus levis 3: Paraleptophlebia chocolata 4: Ephemera strigata 5: Lymnaea auricularia 6: Psephenoides spp.; 7: Davidius lunatus 8: Hexatoma spp.; 9: Stenelmis spp. SPOM, BPOM, Periphyton data from Shin et al. (2013).
4. DISCUSSION
The potential food sources of macroinvertebrates included suspended particulate organic matter (SPOM), benthic particulate organic matter (BPOM), and periphyton (Allan, 1995). Commonly, even in the mean δ13C value of 0.8‰ and mean δ15N value of 3.4‰ in the isotopic fractionation (DeNiro and Epstein, 1978; Minagawa and Wada, 1984; Post, 2002) between macroinvertebrates and their food sources (SPOM, BPOM and periphyton) were considered, our results showed slightly difference between macroinvertebrates and their food sources. In this study, δ13C value of macroinvertebrates showed more than 5‰ of difference with periphyton of potential food sources(Fig. 2). The large difference between macroinvertebrates and periphyton can be explained by below reasons.
First, the macroinvertebrates has body with an exoskeleton made of chitin during growth. Lee et al. (2002) reported that water mite which sucks only body blood from organisms will assimilate the organic matters the value of which is higher than the whole body of the prey organism. In this study, δ13C value of macroinvertebrates mainly feeding on periphyton can be lower than those of food sources because chitin is isotopically lighter than muscle in organisms (Schimmelmann and DeNiro, 1986).
Second, Ephemeroptera may have feeding habit as scraper, as well as collector-gatherer according to around food environment (Shin et al., 2011; Merritt and Cummins, 1996).
Relationship between macroinvertebrates and their food sources are shown in Fig. 2. Although the δ13C and δ15N values of SPOM and BPOM did not differ between ES 1 and ES 2, those of Psephenoides spp., and Ephemera strigata in the upper reaches changed in parallel with those of periphyton in situ (Fig. 2). Moreover, the δ13C and δ15N values of Paraleptophlebia chocolata in the lower reaches were also changed in parallel with those of periphyton. This indicates that these macroinvertebrates assimilated the food sources having much more periphyton than POM. However, the δ13C and δ15N values of Ecdyonurus levis were close to those POM at each station (ES 1, ES 2, and ES 3). Merritt and Cummins (1996) reported that Ecdyonurus levis belong to either the scraper or collectorgatherer group. However, our results indicate that may be closer to the collector-gatherer group than the scraper group. Moreover, they reported that R. nigrocephala, Davidius lunatus, and Hexatoma spp. belongs to the predator group. The δ13C values of Davidius lunatus were similar to, and particularly appeared to change in parallel with, those of Ephemera strigata, suggesting that the larvae of Davidius lunatus may feed on Ephemera strigata in the upper reaches. Furthermore, the δ13C values of Hexatoma spp. at ES 4 were similar to those of Stenelmis spp., indicating that the larvae of Hexatoma spp. may feed on Stenelmis spp. larvae at ES 4. These results were similar to the result of the Inukami River reported by Shin et al. (2011), who studied on variation in trophic pathways and food web characteristics in an intermittent stream system. The δ13C values of macroinvertebrates and periphyton tended to increase from the upstream to the downstream reaches (Fig. 2). They (Shin et al., 2013) reported that the water temperature and pH at ES 4 showed the relatively higher (WT 28.3℃, pH 8.6) than those at the other stations (WT 23.7 to 24.9℃ pH 7.1 to 7.2). Presumably, these results suggested that the enriched δ13C values at ES 4 reflect a shift from CO2 to bicarbonate as a substrate for algal photosynthetic activity according to these parameters.
The δ15N values for Ecdyonurus levis and Lymnaea auricularia considerably decreased from ES 2 to ES 3 (Table 1). The δ15N values of their potential food sources at ES 3 ranged from 0.3 to 2.2‰ (Fig. 2), indicating that relatively lower stable isotope signal of Ecdyonurus levis and Lymnaea auricularia reflected those of its diet in situ. In general, denitrification between ES 2 and ES 3 may be show heavy δ15N values of periphyton and then also macroinvertebrates. However, ES 3 influenced by seepage water showed relatively lower δ15N values of macroinvertebrates according to its diets. These results suggested that the diminished δ15N values of the same food sources originated from periphyton, which assimilated by light δ15N associated with relatively low ammonium concentration (Shin et al., 2013), may directly influence low trophic level of macroinvertebrates. Shin et al. (2013) reported that although ES 3 was characterized by groundwater derived from seepage water, the physicochemical parameters did not differ among stations. Probably seepage water would be little influenced by the industrial activities such as the inflow of contaminants from the surrounding watershed (Verbanck et al., 1989), and consequently ES 3 showed relatively lower chloride, sulfate, and sodium ions (Shin et al., 2013).
In conclusion, our results revealed that the macroinvertebrates and periphyton tended to get enriched δ13C values from the upper to lower reaches in relation to the physicochemical parameters such as water temperature and pH for longitudinal distribution in the Echi River, except for ES 3. Thus, in this study, habitat such as the seepage water region in streams reflects the change in habitat of organisms. The stable isotopic analysis of macroinvertebrates may be use as indicator to reflect stream states in relation to the trophic pathways according to in situ food source in the dry or wet stream.
Acknowledgments
We thank Prof. I. Tayasu and Ph.D. N. Ishikawa from the Center for Ecological Research, Kyoto University, for their assistance with the stable isotope analytical facilities and their incisive suggestions. We also are indebted to T. Akatsuka, H. Azumi, and L. Ao from the Limnological Laboratory, University of Shiga Prefecture, for their generous assistance with the field work. The present study was conducted using the Cooperative Research Facilities (Isotope Ratio Mass Spectrometer) of the Center for Ecological Research, Kyoto University.
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