Biologia, Bratislava, 62/5: 600—606, 2007 Section Zoology DOI: 10.2478/s11756-007-0118-0
Benthic macroinvertebrates associated with four species of macrophytes ´, Goran Palijan & Dubravka Čerba Irella Bogut, Jasna Vidakovic Department of Biology, University of J. J. Strossmayer, Trg Ljudevita Gaja 6, HR-31000 Osijek, Croatia; e-mail: ibogut@ffos.hr
Abstract: Benthic macroinvertebrates associated with four species of macrophytes (Nymphoides peltata, Ceratophyllum demersum, Polygonum amphibium and Carex sp.) were investigated during two growing seasons (2001 and 2002) in the slow-flowing Čonakut Channel in the Kopački rit Nature Park in Croatia. A total of 31 macroinvertebrate taxa were found. C. demersum, a submerged plant with dissected leaves, supported the highest macroinvertebrate abundance, almost seven times more than N. peltata, a floating plant with undissected leaves, which harboured the lowest abundance during the research period. Chironomidae larvae (50–83%) and Oligochaeta (14–46%) were the most abundant groups recorded on all macrophyte species. Water-level fluctuation, because of its influence on the appearance and growth of aquatic vegetation, and the trophic state of water within the macrophyte stands seemed to be the main factors which affected the taxonomic composition and abundance of macroinvertebrates. Key words: macroinvertebrates; macrophytes; leaves morphology; slow-flowing channel
Introduction It is generally known that aquatic plants provide a physically and chemically complex habitat in aquatic ecosystems, and architectural features of this habitat can affect invertebrate species diversity, density and distribution (Carpenter & Lodge 1986). Macrophyte structure and abundance depend on different factors of which water trophic state, depth, light penetration, and water movement are most important (Królikowska 1997; Cenzato & Ganf 2001; Herb & Stefan 2006). Submerged vegetation significantly modifies the water flow, while emerged species stabilise the sediment and shoreline zone and thus improve water quality (Krischik et al. 1999). In shallow waters, macrophytes provide shelter for fauna from disturbance and predation, as well as a large surface for colonisation of algae that represent a food source for the majority of invertebrates (Soszka 1975; Dvořák & Best 1982; Jacobsen & Sand-Jensen 1992; Monahan & Caffrey 1996; Zirk & Goldsborough 1996; Pinowska 2002; Tessier et al. 2004). Submerged and floating-leaved macrophytes differ in structure, offering diverse opportunities for phytophilous organisms (Cattaneo et al. 1998). Macroinvertebrates abundance is often higher on macrophytes with dissected leaves than on those with undissected leaves, because the latter have a larger surface with periphyton for grazing macroinvertebrates and because additional complexity provides a better refuge from predators (Cheruvelil et al. 2002). However, according to Cyr & Downing (1988) and Irvine et al. (1990), macro-
c 2007 Institute of Zoology, Slovak Academy of Sciences
phytes with complex broad leaves can be a better refuge from predators than macrophytes with dissected leaves. Macrophytes like Ceratophyllum demersum and Myriophyllum spp. generally do not support higher macroinvertebrates abundance per unit of plant biomass in relation to macrophytes with broad leaves. This study was conducted to investigate the variation of macroinvertebrate community structure in association with pure stands of four macrophyte species with different plant morphology: Nymphoides peltata (S. Gmelin.) Kuntze, Ceratophyllum demersum L., Polygonum amphibium L. and Carex sp. Study area Field-work was carried out in the Čonakut Channel within the Kopački rit Nature Park, which is a flooded area in the narrow belt between the Drava and Danube rivers, in the north-eastern part of Croatia (45◦ 34 N, 16◦ 24 E) near the town of Osijek. Water-level fluctuation of the Čonakut Channel is primarily determined by the fluctuation of the Danube River, and much less by changes in the water-level of the Drava River or of groundwater-level (Mihaljevi´c et al. 1999). A long-term monitoring investigation (1998–2004) confirmed that the Čonakut Channel is a eutrophic to hypereutrophic, slow-flowing channel, which is not navigable during the periods of low flow (Vidakovi´c et al. 2005). The hydroperiod is one of the dominant controls affecting the types of macrophytes that germinate and grow in the Channel. Irregular patterns of wetting and drying at the edge of shallow water bodies allow the development of different macrophyte communities.
Benthic macroinvertebrates associated to macrophytes
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cm 600 Grow ing season 2001
500
Grow ing season 2002
400 300 200 100 0 -100
J01
M01
M01
J01
S01
N01
J02
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M02
J02
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-200
Drava
Danube
Fig. 1. Water-levels of the Drava and the Danube rivers during the investigation period.
Material and methods Macroinvertebrates were investigated with four species of macrophytes in the Čonakut Channel. Water temperature and depth were measured monthly during two growing seasons at sites with four species of macrophytes. These abiotic variables were selected to represent the most important parameters for macrophyte appearance and growth. Waterlevel fluctuation data for the Danube and the Drava rivers were supplied by the Croatian Water Resource Management at Osijek (Fig. 1). Water-level fluctuations in the mentioned rivers significantly influenced sampling opportunities in the channel under investigation. Namely, the decreasing waterlevel during autumn 2001 caused drying out of the shallow bankside of the channel, whereas extremely high water-level, following sudden water inflow, in summer 2002 prevented sampling because the vegetation was submerged on the bottom of the channel. In 2002, the water-level began receding at the end of August, but the submerged macrophytes did not recover during the autumn, probably due to low temperatures. From June to October 2001 and from April to July 2002, the shallow bankside of the Čonakut Channel was occupied by four dominant monospecific macrophytes for a length of ca. 1.5 km: (1) floating-leaved Nymphoides peltata, a bottomrooted macrophyte with circular leaves; (2) unrooted submerged Ceratophyllum demersum, with fine dissected leaves; (3) amphibian Polygonum amphibium, with undissected, willow-like leaves; the stands of these species were under water during the investigation period; (4) emerged Carex sp. with undissected leaves, which were also under water during the investigation period. To evaluate trophic status, chlorophyll-a concentration (as an estimate of phytoplankton biomass), total phosphorous and total Kjeldahl’s nitrogen were measured from water samples collected inside the macrophyte stands using standard methods (APHA 1985; Carlson & Simpson 1996). The Winkler method was used to determine the level of dissolved oxygen in water samples collected between 9 and 10 a.m. The choice of the method for sampling macrophytes with their associated fauna depended on the macrophyte type, density, and height in the water column. Quantitative samples were collected by hand using a wood floating frame (0.5 × 0.5 m), which was separated into four quadrants of 0.25 × 0.25 m (Soszka 1975; APHA 1985). Macrophytes were cut inside the frame quadrants at the depth of 1 m or
less below the water surface, and trapped into a nylon bag. This method was adequate because of low water depth at the sampling sites. During both growing seasons, for each date when stands of macrophytes were examined, four samples were gathered at each site. In the laboratory, each sample of macrophyte stems was sieved through a 60 µm sieve and rinsed with water to detach fauna. Macroinvertebrates were sorted under a stereoscopic microscope and preserved in a solution of 310 ml distilled H2 O, 585 ml 96% ethanol, 100 ml 4% neutralised formaline, and 5 ml glycerin. The macrophytes were dried at 60 ◦C for 24 h in an oven and weighed to estimate plant dry biomass (Hann 1995; Cattaneo et al. 1998). Macroinvertebrates were counted and identified according to keys by Nilsson (1996, 1997), Streble & Krauter (2002) and Engelhardt (2003). The macroinvertebrate community structure was characterised based on the total number of individuals (N) per 100 g dry weight (d.w.) of macrophytes, and total number of macroinvertebrate taxa (S). Correlations (Pearson’s coefficient, r) were calculated to examine the relationships between macroinvertebrate abundance and macrophyte biomass (Parker 1979). Densities of taxa were compared among various stands of macrophytes during the two growing seasons using one-way analysis of variance (ANOVA) with a LSD post-hoc comparison. The graphic analyses were displayed as Box-and-Whisker plots based on trophic indices values and macroinvertebrate abundance was used to evaluate whether there was a significant difference between macrophyte stands, using the PAST program (Hammer et al. 2001).
Results and discussion Changes in water-level and temperature in the Čonakut Channel were the main variables determining the location of investigated sites with different macrophyte stands and the periods of sampling from June to October 2001 and from April to July 2002. The depth at the sites with macrophyte stands primarily depended on the water inflow from the Danube River through the Hulovo Channel. The so-called edge effect was evident; this resulted from the shallowness of the Čonakut Channel, which is not navigable during the periods of low water levels and becomes isolated from the Hulovo Channel. Water velocity at the shal-
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Table 1. Means (± standard deviation) of selected variables of water in various types of macrophyte stands in the Čonakut Channel. Parameter
Depth (cm) Temperature ( ◦C) Dissolved oxygen (mg O2 ) Oxygen saturation (%) Kjeldahl’s N (mg L−1 ) Total P (mg L−1 ) Phytoplankton Chl-a (µg L−1 ) Macrophyte dry weight (g m−2 )
Nymphoides peltata n=3 145 23.5 4.9 59 0.49 0.3 25.4 126
± ± ± ± ± ± ± ±
Ceratophyllum demersum Polygonum amphibium n=5 n=4
36 3.1 0.5 10 0.1 0.06 13.5 63
low bankside of the channel and inside the macrophyte stands was not measurable, therefore the channel can be compared with the littoral zone of shallow lakes. Recorded temperatures were between 15.5 and 30 ◦C, as expected for the seasons during which the investigation was conducted. The measured physical, chemical and biological water characteristics in the four macrophyte stands were not significantly different and were similar to the data in monotype stands of Ceratophyllum demersum, Myriophyllum sibiricum, and Potamogeton spp. in the channels and bays of Delta Marsh in Manitoba (Zirk & Goldsborough 1996), as well as for C. demersum, M. spicatum, Najas marina, and Trapa natans in the small shallow Lago di Canadia lake in Italy (Cattaneo et al. 1998) (Table 1). Furthermore, the data presented in this paper and the trophic state at the investigated sites of the Čonakut Channel did not deviate from the data obtained at the standard monitoring site in the middle of the channel during the regular monitoring activities within the Water Protection of the Reserve Kopački rit project (Vidakovi´c et al. 2005). The lowest value of dissolved oxygen (DO) (2.91 mg L−1 ) was recorded in the Ceratophyllum demersum stand. During the investigation period, the values of DO concentration were not lower than 2 mg L−1 , below which the hypoxic conditions would jeopardise macrofauna existence. Oxygen saturation was between 34 and 164%. The Trophic State Index (TSI) values (>50) based on the concentration of Chl-a and total P indicated a high level of eutrophication with a tendency for hypereutrophication within the macrophyte stands (Fig. 2). There was no statistically significant difference in the TSI values among the various macrophyte stands. For N. peltata, a total of 12 samples of macrophyte with associated 5,452 macroinvertebrate individuals was collected (stands were examined on 13.VI and 5.VII.2001, and 19.VI.2002). Twenty samples with 104,772 ind. were taken in C. demersum stands (examined on 13.VI., 5.VII., 2.VIII. and 11.IX.2001, and 11.VII.2002). In P. amphibium stands (10,900 macroinvertebrate ind.), 16 samples were taken (on 13.VI., 5.VII.2001, and 21.V. and 19.VI.2002. Carex sp. stands (macroinvertebrate 13,224 ind.) were examined and sampled on 5.VII. and 4.X.2001, and 19.VI.2002, when a total 12 samples were taken.
141 23.6 7.4 90 0.71 0.21 34.6 132
± ± ± ± ± ± ± ±
102 4.1 2.9 39 0.39 0.1 16.8 55
111 24.3 6 74 0.75 0.15 20.6 79
± ± ± ± ± ± ± ±
Carex sp. n=3
65 3.7 2.4 26 0.6 0.02 4.6 43
68 22.7 6.3 75 0.54 0.16 14.85 130
± ± ± ± ± ± ± ±
7 4.3 2 28 0.2 0.12 3.5 91
100
TSI (Chl-a) 90 80 70 60 50
1
2
3
4
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Macrophyte species
100
TSI (P)
90 80 70 60 50
1
2
3
4
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Macrophyte species Fig. 2. Trophic state indices based on the concentration of Chl-a and total P in the water of Čonakut Channel in four macrophyte stands: 1 – Nymphoides peltata; 2 – Ceratophyllum demersum; 3 – Polygonum amphibium; 4 – Carex sp.
Thirty-one main taxonomic groups were found during the investigation period. The highest number (16) of recorded taxa belonged to insect larvae: 11 taxa in association with N. peltata, C. demersum and P. amphibium, and six with Carex sp. Sixteen taxa were recorded in association with the emerged Carex sp. with long undissected leaves, which were completely
Benthic macroinvertebrates associated to macrophytes
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Table 2. Macroinvertebrate taxa (mean number of individuals per 100 g dry weight of macrophytes ± standard deviation) in the examined four macrophyte species. Taxon
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Insect larvae and pupae Chironomidae Ceratopogonidae, Bezzia spp. Cylindrotomidae Ephydridae Dixidae Dytiscidae Donaciinae Ephemeroptera, Caenis spp. Sialidae Stratiomyidae Trichoptera, Polycentropodidae Plecoptera Odonata, Zygoptera Lepidoptera, Pyralidae Heteroptera, Nepomorpha Hydrophilidae
17 18 19 20 21
Insect adults Hydrophilidae Hemiptera unindet. Curculionidae Nepomorpha Gerromorpha, Vellidae
Nymphoides peltata n = 12
Other groups 22 Hirudinea 23 Gastropoda 24 Bivalvia, Dreissena polymorpha (Pallas, 1771) 25 Hydrozoa, Hydra sp. 26 Oligochaeta 27 Isopoda, Asellus aquaticus (L., 1758) 28 Amphipoda 29 Aranea, Argyroneta aquatica (Clerk, 1757) 30 Hydroacarina 31 Turbellaria Number of ind. 100 g−1 d.w. (N) Number of taxa (S)
1053 ± 854 126 ± 182 – 6 ± 11 2±3 21 ± 36 3±5 7 ± 12 1±2 9 ± 15 – 1±2 3±5 – – –
Ceratophyllum demersum n = 20
6173 11 1 1 30 62 1 40 33 3 6
20 ± 27 4±8 1±2 – –
1 2 1 1 1
± ± ± ± – ± – ± – ± ± – ± ± ± – ± ± ± ± ±
Polygonum amphibium Carex sp. n = 16 n = 12
5848 12 4 1 32 84 1 88 75 9 17
1 7 3 3 3
1846 ± 2346 37 ± 43 – 10 ± 22 – 5 ± 11 – 11 ± 21 10 ± 22 1±2 8 ± 14 1±2 23 ± 50 – – 25 ± 55
4758 ± 7893 35 ± 55 – 6±8 – 2±3 – 1±2 2±4 – – – – – – –
10 ± 22 – – – –
2±2 – 1±1 – – 28 ± 19 37 ± 68 1±2
12 ± 8 121 ± 139 –
38 ± 34 176 ± 243 101 ± 240
26 ± 32 69 ± 94 1±2
± ± ± ± ± ± –
– 5807 ± 9720 9 ± 24 – 1±1 – 5 ± 13
26 ± 32 597 ± 615 9 ± 14 – 1±2 – 2±4
12501 23
2718 20
1 320 164 1 5 1
2 379 284 2 9 2
1882 22
below the water surface during the sampling period. Twenty groups were found in association with the amphibian species P. amphibium, and 22 with the floating species N. peltata. The highest number of taxa (23) was recorded in association with C. demersum, a submerged species with dissected leaves (Table 2). There were no differences in macroinvertebrate abundance between the four types of macrophytes (Box-and-Whiskers plot: Fig. 3). In addition, no significant correlation between macroinvertebrate abundance and biomass of different macrophytes was found. The floating species with undissected leaves (N. peltata) harboured the lowest numbers of macroinvertebrates (1,750 ind. per 100 g d.w.) and the submersed C. demersum the highest abundance (12,500 ind. per 100 g d.w.). Macroinvertebrate communities associated with macrophytes in the Čonakut Channel were typically dominated by Chironomidae larvae: between 50% in C. demersum stands (6,170 ind. per 100 g d.w.) and 83% in association with Carex sp. (4760 ind. per 100 g d.w.), and Oligochaeta: between 14% (830 ind. per 100
74 828 9 3 2
± ± ± ± ± – –
159 1670 18 6 2
5789 16
3E4
2E4
1E4
1
2
3
4
Sample
Macrophyte species Fig. 3. Macrofauna abundance (ind. per 100 g dry weight) in four macrophyte stands in the Čonakut Channel: 1 – Nymphoides peltata (n = 12); 2 – Ceratophyllum demersum (n = 20); 3 – Polygonum amphibium (n = 16); 4 – Carex sp. (n = 12).
604
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Chironomidae
5%
9%
Oligochaeta Isopoda Ceratopogonidae
61%
18%
others Nymphoides peltata
3%
7%
Chironomidae Oligochaeta
22%
Gastropoda others 68% Polygonum amphibium
4%
Chironomidae Oligochaeta others 50% 46%
Ceratophyllum demersum
Chironomidae Oligochaeta others
14%
3%
Carex sp.
83%
Fig. 4. Representation of macroinvertebrate taxa in association with four macrophyte species in the Čonakut Channel.
g d.w.) in association with Carex sp. and 46% (5,800 ind. per 100 g d.w.) with C. demersum. The two taxa – Oligochaeta and Chironomidae larvae – represented 96% of the fauna associated with C. demersum, and 97% of that associated with Carex sp. (Fig. 4). During the investigation period, Carex sp., a normally emergent macrophyte, was completely submerged and covered with great amount of detritus. Chironomidae and Oligochaeta are generally the most successful aquatic macroinvertebrate taxa and they inhabit all freshwater bodies, including polluted and eutrophic waters (van der Berg 1999; Mackie 2001). One of the main reasons for the great abundance of
Chironomidae is that they exhibit all types of feeding behaviour and food preference (Lindegaard, in Nilsson 1997). Ceratopogonidae, mainly Bezzia spp., were the second most dominant group of insect larvae (Table 2), and they had the highest abundance in association with N. peltata. Larvae of Ceratopogonidae are common inhabitants of different types of aquatic and semiaquatic habitats. The shallow littoral zones of lakes and ponds are typical breeding places for Ceratopogonidae, and macrophytes are ideal places for their eggs depositions. Ceratopogonidae, which are primarily predators, feed on any small animals living in macrophyte stands: eggs and larvae of chironomids, nematodes, rotifers, annelids, protozoa, other biting midges etc. (Szadziewski et al., in Nilsson 1997). Members of Hydrozoa (Hydra sp.) were absent only in C. demersum stands (Table 2), which can be attributed to allelopathy of this macrophyte species. At the same time, Hydra sp. were recorded on Carex sp. (73 ind. per 100 g d.w.) and on Polygonum amphibium (26 ind. per 100 g d.w.). In contrast, Dreissena polymorpha (Bivalvia) had the highest abundance in association with C. demersum, while in association with P. amphibium and Carex sp. its abundance was <1 ind. per 100 g d.w., and it was never found in association with N. peltata. Gastropoda were constantly present in all macrophyte stands, with the largest numbers in association with C. demersum, because they use macrophytes as feeding source and as suitable surface to deposit eggs (Rooke 1984; Lodge 1985; Pinowska 2002). When comparing data for abundance of other groups, differences in the number of the Asellus aquaticus (Isopoda) were observed. This species was associated with the floating N. peltata. Abundance of other groups was too low to allow quantitative comparisons among macrophytes. The data on the number of recorded taxa in association with macrophyte species in the Čonakut Channel are similar to the results found elsewhere. Soszka (1975) observed similar taxonomic composition in association with Potamogeton lucens, P. perfoliatus, M. ´ spicatum and Elodea canadensis in Sniardwy, Warniak and Mikolajskie lakes in Poland, Hann (1995) in association with C. demersum, Potamogeton zosteriformis, and the macroalga Chara vulgaris in Crescent Pond (Manithoba), and Linhart (1999) in association with the floating species Stratiotes aloides. The majority of taxa recorded in association with macrophytes in the Čonakut Channel are fairly widespread and characteristic of eutrophic waters. Dominance of Chironomidae and Oligochaeta in associations with macrophyte stands was also noted by Soszka (1975), Hergeby et al. (1994) Hann (1995) and Pieczy´ nska et al. (1999). Cattaneo et al. (1998) emphasized the dominance of Gastropoda and Chironomidae, Linhart (1999) Chironomidae and Cladocera, van der Berg (1999) Mollusca, Chironomidae and Gammaridae, Cheruvelil et al. (2000) Chironomidae and Odonata. Tessier et al. (2004) found Ostracoda, Annelida, Gastropoda, and insect larvae,
Benthic macroinvertebrates associated to macrophytes with the predominance of Chironomidae, in association with the emergent species Schoenoplectus lacustris, submerged M. spicatum, and floating-leaved Trapa natans. The abundance of Chironomidae larvae in the Čonakut Channel is higher than that found by Soszka (1975) in association with Potamogeton lucens, P. perfoliatus, M. spicatum and Elodea canadensis in Mikolajskie Lake in Poland, but it is considerably lower than the abundance observed on Hydrilla verticillata and C. demersum in the Atchafalaya Basin swamp in Louisiana (Colón-Gaud 2003). The large number of macroinvertebrates on the submerged species C. demersum may be a due to the fact that submerged species represent a suitable well-illuminated substrate in the water column unlike the floating vegetation (N. peltata) that is less inhabitable for epiphytic organisms because of the emergence of upper sides of leaves and the shading caused by floating leaves (Cattaneo et al. 1998). According to Jackson (1997) and Cheruvelil et al. (2002) the architecture of macrophytes itself may significantly affect the colonisation by phytophilous invertebrates, the abundance of which is often greater on plants with dissected leaves than on plants with undissected leaves. In a small shallow lake (Lago di Candia, North Italy) Cattaneo et al. (1998) found larger numbers of macroinvertebrates associated with submerged vegetation that had dissected leaves (monotype communities of C. demersum and Myriophyllum spicatum, and polytype community of C. demersum + M. spicatum + Najas marina) than on floating vegetation or vegetation with undissected Trapa natans. Cheruvelil et al. (2000) found a significant difference in the abundance of macroinvertebrates according to leaf morphology of macrophyte species: higher density of macroinvertebrates was observed in association with macrophytes with dissected leaves (M. spicatum, Potamogeton pectinatus and Ranunculus spp.) than on macrophytes with undissected leaves (Potamogeton ilinoensis and P. richardsonii); differences in the abundance of macroinvertebrates on various macrophyte species of the same architecture were not significant. Van der Berg (1999) compared the composition and number of macroinvertebrates in pure stands of Potamogeton perfoliatus, P. pectinatus and Chara spp. in two shallow eutrophic lakes (Veluwemeer, Wolderwijd) in the Netherlands; the biomass of macrophyte vegetation, i.e., the size of macrophyte community had a greater effect on macroinvertebrates than the type of vegetation. In addition to the water-level fluctuation, due to its influence on the appearance and growth of aquatic vegetation, the trophic state of water within the macrophyte stands (eutrophy in the Čonakut Channel) seemed to be another important factor which affected the taxonomic composition and the abundance of macroinvertebrates, dominance of Chironomidae larvae and Oligochaeta.
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