ISSN 1995-0829, Inland Water Biology, 2017, Vol. 10, No. 4, pp. 405–414. © Pleiades Publishing, Ltd., 2017. Original Russian Text © I.A. Baryshev, 2017, published in Biologiya Vnutrennykh Vod, 2017, No. 4, pp. 50–60.
ZOOPLANKTON, ZOOBENTHOS, AND ZOOPERIPHYTON
Taxonomic Composition and Trophic Structure of Benthic Fauna in Rocky Rapids and Riffles in Rivers of the Republic of Karelia and Murmansk Oblast I. A. Baryshev Institute of Biology, Karelian Research Center, Russian Academy of Sciences, Petrozavodsk, Republic of Karelia, 185910 Russia е-mail:
[email protected] Received December 24, 2015
Abstract⎯The composition of bottom invertebrates in rocky rapids and riffles in rivers of the White, Barents, and Baltic seas in the territory of Eastern Fennoscandia is presented and analyzed. A total of 114 species (137 taxa of different ranks) have been identified. Most of them have Euro-Siberian (44%) and Palaearctic (36%) distribution. Regarding the feeding mode, collector–gatherers (32%) and collector–filterers (25%) dominate among trophic groups. Differences in the composition of zoobenthos between the southern and northern parts of the region can be explained not by the fauna genesis, but by latitudinal zoning. Keywords: fauna, bottom communities, composition, trophic groups, Fennoscandia, distribution DOI: 10.1134/S1995082917040034
INTRODUCTION Republic of Karelia and Murmansk oblast are located in Eastern Fennoscandia, a physicogeographical region of Northern Europe, most of which lies within the Baltic Shield. The common geological structure of the territory determines the hydrographical similarity of rivers, which made it possible to distinguish the Kola hydrobiological type for a description of watercourses [8], and the geological youth of the landscape determines a river channel full of rapids and the presence of a large number of running-water lakes. Rapid parts constitute a significant portion of watercourses; a special lithorheophilic community is formed in rapids [8]. Numerous studies on macrozoobenthos in rivers of the Republic of Karelia and Murmansk oblast have been conducted previously; data on benthic fauna are presented both in hydrobiological reports and in faunistic works [6, 22, 28, 29, 34, etc.]. However, publications devoted to the fauna consider only particular taxonomic groups or describe all fauna of the territory without the subdivision of river and lakes [20, 33, 37]. In hydrobiological papers which take into consideration the specific character of the river channel, the species composition is more frequently given for particular streams or small areas without areological analysis [7, 29, 32]. A considerable portion of zoobenthos is constituted by heterotopic insects whose larvae live in aquatic environments and imagoes inhabit air envi-
ronments. Entomologists studying imaginal stages of amphibiotic insects and other animals from the air (terrestrial) environment use the scheme of zoogeographical division of the land [4]. Hydrobiologists studying heterotopic insects and aquatic organisms follow the schemes of zoogeographical division of inland waters, among which the scheme of Starobogatov is the most detailed [24, 31]. The aim of this study is to determine the taxonomic composition and trophic structure of zoobenthos in rapid parts of rivers in the Republic of Karelia and Murmansk oblast. MATERIALS AND METHODS The samples (463 quantitative samples from 131 stations in 90 water courses) were collected in rapids and rocky riffles in rivers of the Republic of Karelia (64% of samples) and Murmansk oblast (35% of samples). Rivers in the basins of lakes Ladoga and Onega and the White (Pomorsky, Karelian, Kandalaksha, and Tersky coasts) and Barents seas were studied. Samples were collected in sites with current velocities of 0.2 to 0.6 m/s. Grounds consisted of a mixture of pebbles, gravel, and boulders, sometimes with a small (up to 10%) proportion of sand. Periphyton (Fontinalis sp., green algae) occupied from 0 to 70% of the projective cover. The samples were collected in the second half of the summer (the end of July–August), when the water
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level in rivers was stable (floods do not affect the results) and low, which made it possible to study the entire channel part. In addition, most species of amphibiotic insects are presented in zoobenthos in this time of year. Quantitative samples were collected using a frame of 0.04 m2 in area. A common logarithm of discharge was used for the size gradation of rivers; the following size classes were distinguished: 30 m3/s are large rivers, 68 samples. The following abbreviations were used to denote species distribution: (HA) Holarctic, (PA) Paleoarctic, (ES) European–Siberian, and (WW) worldwide. A common classification of animals for assessing the trophic macrozoobenthos structure has not been developed. The feeding spectrum of bottom invertebrates varies considerably [13, 34]; therefore, classification focusing on the mode of feeding was used as a basis. Active predators (P) were distinguished as a separate group. Shredders (Sh), scapers (S), collectors–filterers (CF), and collectors–gatherers (CG) are distinguished among nonpredatory hydrobionts [15, 27, 35]. RESULTS Representatives of seven types of invertebrate animals were found in macrozoobenthos; 114 species and 23 taxonomic groups of a higher rank were identified. The species with European–Siberian (44%) and Palearctic (36%) distribution prevail; species with Holarctic distribution are less frequent (18%). Only some representatives of Plathelminthes and Oligochaeta (2%) have a worldwide distribution. Among functional feeding groups, collectors–gatherers (32%) and collectors–filterers (25%) prevail in macrozoobenthos. The proportion of active predators is 17%, shredders constitute 14%, and scrapers constitute 11%. Oligochaeta. They can be referred to collectors– gatherers by the feeding mode. The frequency of their occurrence in samples was high (67%), but mass accumulations were not recorded. The maximum biomass was 11.5 g/m2, with an average of 0.3 g/m2 in small rivers and 0.6 g/m2 in medium and large rivers. Eiseniella tetraedra (Savigny, 1826) WW, Cognettia glandulosa (Michaelsen, 1888) HA, and Fridericia callosa (Eisen, 1878) HA are the most widespread. Ranges are presented according to Popchenko [22] and Timm [40]. Hirudinea. They are common dwellers of the river bottom, predators. Their occurrence is higher in large rivers, 40% vs. 15% in small rivers. Erpobdella octoculata (Linnaeus, 1758) PA, Glossiphonia complanata (Linnaeus, 1758) HA, and Helobdella stagnalis (Linnaeus, 1758) PA were found. The ranges are presented according to [18]. Gastropoda. The frequency of their occurrence was 35% both in small and large rivers. They are, mainly,
collectors–gatherers. Ancylus fluviatilis O.F. Müller, 1774 (river limpet) is a common inhabitant of rapids. Planorbis spp., Lymnaea stagnalis (Linnaeus, 1758) HA, L. ovata (Draparnaud, 1805) PA, Bithynia tentaculata (Linnaeus, 1758) HA, Anisus dispar (Westerlund, 1871) ES, A. stroemi (Westerlund, 1881) ES, A. stelmachoetius (Bourguignat, 1860) HA, A. albus (O.F. Müller, 1774) HA, and Armiger sp. were also recorded. The species of this group were identified by I.O. Nekhaev (Murmansk Marine Biological Institute, Kola Research Center, Russian Academy of Sciences). The distribution is presented according to Ya.I. Starobogatov [24]. Bivalvia. Collectors–filterers are widespread in rivers (occurrence 45%). Representatives of the family Euglesidae: Cyclocalyx obtusalis (Lamarck, 1818) ES, C. scholtzii (Clessin, 1873) ES, Cingulipisidium nitidum (Jenyns, 1832) PA, Henslowiana henslowana (Sheppard, 1823) ES, H. lilljeborgii (Clessin, 1886) ES, Hiberneuglesa normalis (Stelfox, 1929) ES, H. bodamica (Starobogatov & Korniushin, 1989) PA, H. portentosa (Stelfox in Ellis, 1940) ES, and Tetragonocyclas baudoniana (de Cessac, 1855) ES, and the family Sphaeriidae (pea clams): Sphaerium westerlundi Clessin in Westerlund, 1873 PA (identified by A.A. Frolov). Representatives of the family Unionidae (genera Anodonta and Unio) occurred solitary in sites with a high trophy level in medium and large water courses. Margaritifera margaritifera (Linnaeus, 1758) ES (family Margaritiferidae) was recorded in salmon rivers. The distribution is presented according to [14, 25]. Malacostraca are rare inhabitants of rapids. Solitary specimens of Mysis relicta Loven, 1862 (order Mysida) HA were recorded. Amphipoda Gammarus duebeni, Liljeborg 1852 HA and G. zaddachi, Sexton 1912 HA were found near marine estuaries of the rivers. G. lacustris Sars, 1863 and Asellus aquaticus (Linnaeus, 1758) ГА (Isopoda), which are widespread in fresh waters, avoid rapids; only solitary specimens of the latter were found. The distribution is presented according to [5, 36]. According to the feeding mode, the representatives of this group are shredders [34]. Hydracarina. Larval stages are parasites and adults are predators. They are widespread in the rivers of the region (occurrence 40%); they do not reach high abundance. Ephemeroptera. They are widespread in macrozoobenthos in rapid parts; the frequency of their occurrence averages 94%; the proportion in biomass is 15%. These parameters increase as the water course increases. Twenty-four species have been detected; this constitutes slightly more than half of all mayfly fauna in the region [23, 34]. The species composition and distribution according to size classes of water courses are presented in Table 1. The family Baetidae is widely represented, nine species; four species belong to the family Ephemerellidae. Of 21 identified species, INLAND WATER BIOLOGY
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Table 1. Ecologo-faunistic characteristic and occurrence of mayflies Taxon
Range
Mode of feeding
Size classes of watercourses, m3/s 30
– –
– +
+ –
– –
Siphlonuridae Siphlonurus sp. Parameletus sp.
– –
Ametropodidae Metretopus borealis (Eaton, 1871) Baetidae Baetis (Acentrella) lapponicus (Bengtsson, 1912) B. rhodani (Pictet, 1843) B. vernus Curtis, 1834 B. fuscatus* (Linnaeus, 1761) B. tracheatus Keff. & Mach., 1967 B.(Nigrobaetis) digitatus Bengtsson, 1912 B. (N.) niger (Linnaeus, 1761) B. (N.) muticus (Linnaeus, 1758) Cloeon (Centroptilum) luteolum (Müller, 1776) Heptageniidae Ecdyonurus (Afghanurus) joernensis Bengtsson, 1909 Heptagenia dalecarlica Bengtsson, 1912 H. sulphurea (Müller, 1776) Ephemerellidae Ephemerella mucronata (Bengtsson, 1909) E. notata Eaton, 1887 E. aroni Eaton, 1908 =aurivillii Bengtsson, 1908 E. ignita Poda, 1761 Ephemeridae Ephemera sp. Potamanthidae Potamanthus luteus (Linnaeus, 1767) Leptophlebidae Habrophlebia lauta Eaton, 1884 H. fusca (Curtis, 1834) Paraleptophlebia submarginata (Stephens, 1835)
– –
HA**
CG
–
–
+
–
ES ES PA PA ES ES ES ES PA
CG CG CG CG CG CG CG CG CG
1 20 21 13 – 7 4 – –
+ 28 25 7 – 8 7 + –
– 40 25 14 + 3 9 2 1
– 24 9 19 – 19 1 1 –
PA PA PA
S S S
– 5 18
3 20 14
4 17 29
12 16 16
PA ES HA PA
CG CG S CG
– – – 9
+ 3 – 18
6 + + 28
– 6 – 12
–
2
1
1
–
–
PA
CG
–
–
3
3
PA PA PA
CG CG CG
4 1 8
2 3 10
3 – 4
– – 9
Here and in Tables 2–4: “+” means solitary findings (3 m3/s and 19% in rivers with higher discharge. The species is widespread in the European–Siberian subregion [11]. In watercourses of the region it is abundant in the southern part (rivers of the basins of lakes Ladoga and Onega) in sites with a high trophy level. The species occurs rarely in rivers of the White Sea basin, only in the southern part of the catchment area (Nyukhcha and Kem rivers). Coleoptera. They are represented both by larvae and imagoes. Their occurrence is 66% regardless the size of watercourses (Table 3). The contribution to
biomass is 7000 ind./m2 and 10 g/m2) were recorded rarely (in 1% of samples) and in sites with high abundance of seston in outflow sites from lakes. Biting midges Ceratopogonidae occurred rather rarely (12% of samples) and did not form accumulations. Athericidae were represented by a predatory Atherix ibis (Fabricus, 1798). The occurrence in samples was 8%. Solitary representatives of the groups Spongia, Spongilla lacustris (Linnaeus, 1758), Hydrae, Plathelminthes, Planaria torva (Müller, 1774), Nematoda, Nematomorpha, Ostracoda, Collembola, Neuroptera, Sisyra sp., and Megaloptera, Sialis fuliginosa Pictet, 1836 were found. DISCUSSION A specific community of bottom invertebrates which includes species with different modes of feeding and ranges of distribution is formed in rapid parts of rivers in the Republic of Karelia and Murmansk oblast. The identified composition seems to be not very large in respect to benthic fauna of all water objects in the region, >600 taxa [33], which may indicate a specific character both of a habitat and its dwellers. The list of species can be broadened considerably after a detailed identification of Diptera, which may constitute about half of the fauna [33]. Thus, 1290 species of chironomids from 178 genera are indicated for the Palearctic region; preimaginal stages are known only for a third of them [19]. Undoubtedly, the species diversity of this group is high in the rivers of the studied region as well. Thus, V.A. Yakovlev [34] indicates 140 species and forms of chironomids from 81 genera for waters of northern Fennoscandia. NevINLAND WATER BIOLOGY
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ertheless, a significant part of chironomids belongs to the subfamily Orthocladiinae, which has been studied insufficiently, and the species identification using larvae is difficult [19]. A detailed identification of the other group of Diptera, Simuliidae, presented by ≥35 species according to the data of Z.V. Usova, also present difficulties. The ratio of species with different distribution and modes of feeding according to taxonomic groups is given in Table 5. Secondary aquatic animals (insects) have European–Siberian (46.8%) and Palearctic (42.0%) distribution. Most primary aquatic organisms have Holarctic (38.6%) and European–Siberian (46.8%) ranges. The detected faunogenetic structure of zoobenthos in rapids is similar to that of all freshwater benthos in Murmansk oblast (mainly, of lacustrine benthos) [33]. Thus, the rheophilic zoobenthos in the region do not have pronounced differences from the limnophilic one in respect to genesis. One important characteristic of the structure of bottom communities is the ratio of trophic groups (Table 6). The prevalence of collectors–gatherers and collectors–filterers is typical for zoobenthos in river rapids [15, 27]. According to the ratio of trophic groups, the rheophilic benthos in the Republic of Karelia and Murmansk oblast differs considerably from the limnophilic benthos, in which predators and collectors–gatherers predominate [34]. A considerable difference in the composition is due to the fact that current makes passive filtration possible, i.e., collection of seston by water filtering. Net-weaving caddisflies of the families Hydropsychidae and Polycentropodidae and black flies Simuliidae are typical representatives of passive filterers. Features of a watercourse affect the trophic structure of zoobenthos. Thus, the proportion of scrapers
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Table 4. Ecologo-faunistic characteristic and occurrence of caddisflies Taxon Rhyacophilidae Rhyacophila fasciata Hagen, 1859 R. nubila Zetterstedt, 1840 R. obliterata McLachlan, 1863 Glossosomatidae Agapetus ochripes Curtis, 1834 Glossosoma sp. Hydroptilidae Agraylea multipunctata Curtis, 1834 Hydroptila sp. Ithytrichia lamellaris Eaton, 1873 Oxyethira frici Klapalek, 1891 O. sp. Arctopsychidae Arctopsyche ladogensis (Kolenati, 1859) Hydropsychidae Cheumatopsyche lepida (Pictet, 1834) Hydropsyche contubernalis McLachlan, 1865 H. newae Kolenati, 1858 H. pellucidula (Curtis, 1834) H. saxonica McLachlan, 1884 H. silfvenii Ulmer, 1906 H. siltalai Doehler, 1963 Polycentropodidae Cyrnus sp. Neureclipsis bimaculata (Linnaeus, 1758) Plectrocnemia sp. Polycentropus flavomaculatus (Pictet, 1834) P. irroratus Curtis, 1835 Psychomyiidae Psychomyia pusilla (Fabricius, 1781) Philopotamidae Chimarra marginata (Linnaeus, 1767) Philopotamus montanus (Donovan, 1813) Wormaldia subnigra McLachlan, 1865 Brachycentridae Brachycentrus subnubilus Curtis, 1834 Micrasema setiferum (Pictet, 1834) Limnephilidae Halesus sp. Micropterna lateralis (Stephens, 1837) M. sequax McLachlan, 1875 M. sp. Potamophylax latipennis (Curtis, 1834)
Size classes of watercourses, m3/s
Mode of feeding
30
ES* ES ES
P P P
1 32 3
2 34 2
– 36 –
– 21 –
ES –
S –
– –
3 +
3 +
1 1
HA – ES ES –
CG – CG CG –
– 3 4 – 5
+ 3 6 + 8
2 4 10 – 6
1 6 9 – 1
HA
CF
7
4
11
7
ES PA PA PA ES ES ES
CF CF CF CF CF CF CF
1 – – 25 – 1 –
4 – + 31 + 12 3
27 3 5 41 – 4 22
19 6 6 25 – – 9
– HA – PA ES
– CF – CF CF
– 9 3 9 –
+ 12 + 20 +
– 19 + 9 –
– 3 – 4 –
ES
CF
3
3
8
9
ES ES ES
CF CF CF
– 4 –
– 2 3
2 – +
13 – –
PA ES
CF CF
3 4
8 5
16 5
– –
– PA PA – PA
– Sh Sh – Sh
1 – – 1 1
+ + – – 2
+ – + 3 +
1 – – – –
Range
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Table 4. (Contd.) Taxon Goeridae Silo pallipes (Fabricius, 1781) Lepidostomatidae Lepidostoma hirtum (Fabricius, 1775) Leptoceridae Athripsodes aterrimus (Stephens, 1836) A. cinereus (Curtis, 1834) Ceraclea annulicornis (Stephens, 1836) C. fulva (Rambur, 1842) C. nigronervosa (Retzius, 1783) C. sp. Oecetis notata (Rambur, 1842) Sericostomatidae Sericostoma personatum (Kirby & Spence, 1826) Beraeidae Beraea pullata (Curtis, 1834)
Size classes of watercourses, m3/s
Mode of feeding
30
ES
Sh
1
–
–
–
PA
Sh
8
6
10
12
PA PA HA PA HA – PA
S S S S S – S
– – – – 4 – –
– – – – – 5 +
2 6 + + 4 2 –
– – – – – – –
ES
S
1
2
+
–
ES
S
–
–
+
–
Range
* Presented according to the works [17, 39].
Table 5. The ratio of species with different distributions and modes of feeding in macrozoobenthos in rapid parts, % Distribution Taxon Spongia Plathelminthes Oligochaeta Hirudinea Gastropoda Bivalvia Malacostraca Ephemeroptera Odonata Plecoptera Hemiptera Coleoptera Trichoptera Total
Mode of feeding
Number of species PA
HA
ES
WW
P
Sh
S
CF
CG
1 1 3 3 8 11 4 21 4 13 1 7 37
0 0 0 67 13 27 0 57 100 38 0 14 35
100 0 67 33 50 0 100 10 0 15 0 0 14
0 0 0 0 38 73 0 33 0 46 100 86 51
0 100 33 0 0 0 0 0 0 0 0 0 0
0 100 0 100 0 0 0 0 100 46 100 14 8
0 0 0 0 0 0 100 0 0 54 0 0 14
0 0 0 0 0 0 0 19 0 0 0 0 24
100 0 0 0 0 100 0 0 0 0 0 0 46
0 0 100 0 100 0 0 81 0 0 0 86 8
114
36
18
44
2
17
14
11
25
32
Only organisms identified to the species were taken into account.
and filterers increases due to shredders as the watercourse increases, which corresponds to the provisions of the river continuum concept [41]. Open lakes also make a great contribution to the formation of the zoobenthos structure; as the distance from a waterbody increases, the share of filtrating forms decreases due to INLAND WATER BIOLOGY
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the increase in the number of collectors and scrapers; the share of predators tends to decrease. The question of the validity of distinguishing the northern territories as separate zoogeographical provinces has not yet been solved. Thus, according to the
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Table 6. A relative biomass of trophic groups of macrozoobenthos depending on the size of a watercourse and distance from a running-water lake, % Water discharge, m3/s
Mode of feeding P Sh S CF CG
Distance from the lake, km
30
20
13 20 1 32 33
26 10 3 37 24
16 14 4 43 23
9 8 7 46 30
20 8 1 53 18
23 10 3 43 22
19 12 4 40 25
13 23 5 22 38
Table 7. Taxonomic composition of the rheophilic benthos in the territory of the Republic of Karelia and Murmansk oblast Taxon
Republic of Karelia
Murmansk oblast
Number of common species
Plathelminthes Oligochaeta Hirudinea Mollusca Hemiptera Ephemeroptera Plecoptera Megaloptera Neuroptera Trichoptera Odonata Coleoptera
0 2 1 2 0 19 13 0 0 25 0 6
1 6 3 6 1 25 15 1 1 40 4 9
0 2 1 2 0 17 12 0 0 24 0 6
Total
68
112
64
system of V.Ya. Starobogatova [24], the boundary between the Lapland and Baltic provinces lies in the surveyed territory. A similar boundary was proposed by L.S. Berg based on the study of fish ranges [3]. Nevertheless, distinguishing the northern territories as separate zoogeographical provinces is based, sometimes, not on the faunogenetic principle but on a zonal one [16, 30]. The severe climate in Murmansk oblast (average annual temperatures are close to zero, the frost-free period lasts 60–120 days, and isotherms of July constitute 8–13°C) when compared to a mild climate in Karelia (average annual temperatures are 1– 1.5°C, frost-free period lasts 70–130 days, isotherms of are July are 14–16°C) determines the location of the northern boundary of distribution of many species between these regions [1, 2]. The composition of macrozoobenthos in river rapids in the Republic of Karelia and Murmansk oblast are given in Table 7 (the data on Diptera are fragmentary and are not presented). The analysis of the zoobenthos fauna shows that the main distinctive feature of the fauna in the norther territories is its poor species composition. There are only four species which were recorded in rivers in Murmansk oblast and were not found southward: Baetis
lapponicus, Ephemerella aurivillii, Arcynopteryx compacta, and Philopotamus montanus, or
