Biologia 65/5: 884—891, 2010 Section Zoology DOI: 10.2478/s11756-010-0102-y
Benthic macroinvertebrate fauna of two alpine lakes over the last century: The value of historical data for interpreting environmental changes Peter Bitušík1, Ferdinand Šporka2, & Iľja Krno3 1
Faculty of Science, Matthias Belius University, SK-97401 Banská Bystrica, Slovakia; e-mail:
[email protected] Institute of Zoology, Slovak Academy of Sciences, Dúbravská cesta 9, SK-845 06 Bratislava, Slovakia 3 Faculty of Sciences, Comenius University, Mlynská dolina B-2, SK-84215 Bratislava, Slovakia 2
Abstract: Data on benthic macroinvertebrate assemblages of two alpine lakes in the Tatra Mts (Slovakia) collected in 1914, 1933, 1979–1982, 1993–1997, and 2000 were collated and analysed in an attempt to define their relationship to major environmental events affecting these alpine lakes over the last century. The oldest data were considered an important background before the onset of acidification in one of the lakes in the 1950s, while the most current contain possible information on biological recovery. Results show that data from the 1910s are insufficient to characterize the macroinvertebrate fauna. Deep zone assemblages of both studied lakes have remained stable since the 1930s. Changes in the density of dominant species over time were found in the acidified lake, suggesting a connection between an increase in phosphorus and chlorophyll-a concentration. The composition of the littoral assemblages in the acidified lake in the 1930s indicates that the lake was not strongly acidified at that time. A stable composition since the 1980s reflects the ongoing acid stress. Incomplete species data on the non-acidified lake did not allow us to detect possible changes in the littoral fauna related to acidification. Single findings of species indicating a recovery process need longer-term data to confirm such a trend. Results from this study suggest that historical datasets consist of valuable information that can supplement palaeolimnological analyses in the reconstruction of lake ontogeny. Key words: aquatic insects; oligochaetes; acidification; biological recovery; High Tatra Mts; Slovakia
Introduction Lakes of glacial origin represent more than 90% of all natural lakes in Slovakia. Due to their natural beauty and extreme conditions, they have been the focus of interest for limnologists since the time of the first pioneers in 1804. The first studies of macroinvertebrate benthic fauna performed by Vejdovský (1884) and Daday (1896, 1897) were followed by the works of Kowalewski (1914) and Minkiewicz (1914). More extensive investigations were carried out in the 1930s, especially thanks to Hrabě (1939a, b). About twenty years later, benthic macroinvertebrate assemblages started to be intensely studied, initially in connection with eutrophication, and later with acidification processes (see Krno et al. 2006 for references to earlier studies). Recently, surveys have focused on changes in the littoral macroinvertebrate fauna induced by climatic change (Hamerlík & Bitušík 2009; Čiamporová-Zaťovičová et al. 2010). Starolesnianske pleso and Nižné Terianske pleso are among the most intensively investigated lakes in Slovakia, and for the past few decades have been monitoring sites as part of multi-disciplinary and multi-national projects founded by Commissions of European Communities (AL:PE 2, MOLAR, EMERGE; Štefková & Šporka 2001) c 2010 Institute of Zoology, Slovak Academy of Sciences
Acidification became one of the most serious global anthropogenic stresses in the latter half of the past century. Remote lakes situated above timber-line and on acid sensitive geology were extremely sensitive to acid atmospheric deposition. Compared with other European mountain ranges, the Tatra Mts have been exposed to the strongest effects of acidification pollutants for more than a half of the century (Kopáček et al. 2004). Acidification caused significant changes in water chemistry that induced water toxicity, influenced lakes’ trophic status, and led to serious changes in the structure of planktonic and benthic communities in many Tatra Mts lakes (Stuchlík et al. 1985; Krno 1991). The first signs of lake water recovery from acidification were seen at the beginning of the 1990s (Kopáček et al. 2004) as a consequence of a large drop in the emission of sulphur and nitrogen compounds throughout Europe. The recovery process in the Tatra Mts has been considered to be the most extensive of European mountain ranges (Wright et al. 2005). The biological recovery of communities following the reversal in water chemistry is now one of the main topics of limnological research in the Tatra lake district. Even though this process is delayed by hysteresis in the chemical reversal from acidification (Kopáček et al. 2002), the first indications of recovery for planktonic communities have
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been observed (Nedbalová et al. 2006; Hořická et al. 2006; Sacherová et al. 2006). Changes in the benthic macroinvertebrate assemblages of the impacted lakes have mostly not been so clear, and need to be interpreted carefully in terms of recovery. As invertebrates have been used as “early-warning” organisms to detect the extent of acidification stress in the past (e.g., Raddum & Fjellheim 1984), recently they have been employed to assess the biological recovery of aquatic ecosystems (Raddum et al. 2001). To reveal and assess recovery, however, knowledge of the pre-acidification faunal composition is needed. Earlier published and unpublished data can be considered an important „background“ of the Tatra Mts lake fauna before the onset of acidification in the 1950s (Kopáček et al. 2004). Respectively, data from the late 1990s and 2000s could be expected to reveal some signs of biological recovery. Palaeolimnological analyses of the sediment records from some Tatra Mountain lakes situated on an acidification gradient have revealed the structure of their chironomid fauna prior to the acidification period (Kubovčík & Bitušík 2006; Bitušík et al. 2009). However, if the historical data span a sufficiently long interval, they can also be used for the detection of such changes. In addition, the analyses can also include groups that are either not preserved in the sediments (e.g., Oligochaeta), leave remains that are scarcely found, or are usually impossible to identify (e.g., larvae of Ephemeroptera, Plecoptera, Trichoptera, etc.). The results of several studies examining planktonic crustaceans over a time scale of ∼100 years have specified the timing in community changes related to acidification in the Tatra region (Vranovský 1991; Fott et al. 1994; Sacherová et al. 2006). Here, we studied several published and unpublished records, with hopes that historical data can help us complete a similar analysis for lake benthic fauna during the substantial changes in water chemistry. This paper addresses the following questions (i) does the composition of benthic macroinvertebrate assemblages have any definable relationship to the major events (acidification, recovery) affecting the alpine lakes in the last century; and (ii) are the historical data consistent with palaeolimnological interpretations?
The bedrock of the lakes is mostly composed of granodiorite. Bare rocks and moraines cover more than 60% of the catchment of Nižné Terianske pleso, while alpine meadows predominate (60%) in the catchment of Starolesnianske pleso. Alpine soils are undeveloped (lithosol, ranker), with a negligible carbonate content. The lakes have ice cover more than 200 days per year and a maximum daily mean of surface water temperature of ca. 12–13 ◦C (Šporka et al. 2006). Both lakes are fishless. In the 1980s, the studied lakes represented two different types of sensitivity to the acidification processes affecting the region (Fott et al. 1994). While Nižné Terianske pleso was (and remains) relatively non-sensitive to acidification, with pH > 6.0, and acid neutralising capacity (ANC) > 25 µeq L−1 , Starolesnianske pleso was extremely sensitive to acidification, characterised by pH < 5.0, and ANC < 0 µeq L−1 (Kopáček et al. 2004). Despite clear signs of a reversal from acidification since the 1990s (Stuchlík et al. 2002), this lake remains acidified to the present.
Study sites
‘1980’ dataset The dataset combines samples collected in August 1979, August and October 1981 (Nižné Terianske pleso), and August and October 1982 (Starolesnianske pleso), as part of an integrated limnological investigation of the Tatra Mountain lakes (Vranovský et al. 1994). Starting with this period, at least one of the authors of this paper has participated in the sampling, laboratory processing, and identification of the material. Macroinverebrates were collected with an EkmanBirge grab at the deepest part of the lakes, and quantitative littoral samples were taken with a 0.1 m2 modified Hess sampler with mesh-size 500 µm (Helan et al. 1973; use in standing water followed Krno 1988). The datasets also include species data identified from microscopic slides by E. Ertlová that have not yet been published.
The studied sites are lakes of Quaternary glacial origin in the High Tatra Mts in northern Slovakia. Nižné Terianske pleso (49◦ 10 11.3 N, 20◦ 00 51.5 E) is situated in the Nefcerka Valley at altitude 1941 m a.s.l., with a lake area of 5.6 ha, catchment area 114 ha, maximum depth 47.3 m, and mean depth 15.7 m (Gregor & Pacl 2005). The lake has an inflow and an outflow. Starolesnianske pleso is located in the Veľká Studená Valley (49◦ 10 48.0 N, 20◦ 10 04.1 E) at an elevation of 1988 m a.s.l., with a lake area of 0.72 ha, catchment area 2.64 ha, maximum depth 4.2 m and mean depth 1.47 m (Gregor & Pacl 2005). It has a temporary outlet (at higher water levels) at the south-western side of the lake, while the inlet is not developed.
Methods In this study, several datasets were included to represent different periods of history for the two studied lakes, Starolesnianske pleso and Nižné Terianske pleso. ‘1914’ dataset The first data on benthic macroinvertebrates were collected by Minkievicz (1914). He took the samples qualitatively, but did not give details on sampling devices or laboratory procedures. Kowalewski (1914), who identified his material, wrote that he received the specimens fixed in formalin or alive. ‘1930’ dataset The data were gathered by S. Hrabě during his investigations of the Tatra Mts lakes in the 1930s. He collected the material using an Ekman-Birge grab from the deepest part of the lakes in July 1933 (Nižné Terianske pleso) and in August 1933 (Starolesnianske pleso). The samples were sieved through 1000 µm mesh size and organisms were hand-sorted in the field without any magnification (Hrabě 1942). Information on the sampling method in the lake littorals is unavailable.
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Table 1. Historical occurrence and abundance (individuals m−2 ) of benthic macroinvertebrates in the deepest part of Starolesnianske pleso. 19331 Oligochaeta Tubifex tubifex (M¨ uller, 1774) Stylodrilus heringianus (Claparéde, 1862) Enchytraeidae indet. Coleoptera Agabus sp. (L) Chironomidae Procladius (Holotanypus) sp. (L) Cricotopus sylvestris group (L) Heterotrissocladius marcidus (Walker, 1856) (L) Zalutschia tatrica (Pagast, 1935) (L) Tanytarsus gregarius Kieffer, 1909 (L, P) Tanytarsus cf. bathophilus Kieffer, 1911 (L) Explanation:
1
1982
1993
1994
1996
1997
+ + –
27 – –
143 – –
304 – 24
31774 – –
19866 – –
–
–
–
–
+ – + – – –
2 9 87 3 2 1
22 – 14 2 – –
24 – 32 16 119 –
20 1533 – 59 236 13931 –
– 1631 – 373 39 629 –
Hrabě (1939a, b, 1942), + presence, – absence, L – larvae, P – pupae.
‘1990’ dataset The data comes from studies performed within the projects AL:PE 2 and MOLAR. Sampling of the deep lake zones was carried out in October 1993, September 1994, in August and September 1995 (Nižné Terianske pleso), in June, August and September 1995 (Starolesnianske pleso), and in July, August and October 1997, using a Kajak type sampler. Littoral zoobenthos was collected with a hand net (frame 25 × 25 cm, mesh size 300 µm) disturbing the substrate for 5 min. The sampling consisted of short kick series from different substrate types to obtain comparable data (Frost et al. 1971). ‘2000’ dataset The last dataset consists of samples from September 2000 obtained only from the littorals using the kicking method. Since the 1980s, the sampled material was sieved through 500 µm sized mesh. In the laboratory, all animals were sorted and counted under a low-power stereomicroscope (× 7–40). Oligochaetes and chironomid larvae were mounted on slides and identified under high magnification (× 400). Invertebrates were identified to the lowest possible taxonomic level. With the exception of the 1930 period, when the oligochaetes were identified by S. Hrabě and some specialists (see below), and the 1980s when chironomids were determined partly by E. Ertlová, identifications have been made by the same persons throughout the collection period: oligochaetes by F. Šporka, chironomids by P. Bitušík and other macroinnvertebrate groups by I. Krno. For the purposes of this paper, lists of taxa provided by Minkievicz (1914) and Hrabě (1939a, b, 1942) were revised, and the identification and nomenclature were harmonised with contemporary knowledge (Fauna Europaea Web Service 2007) with the aim to minimise differences due to different taxonomic identification levels.
Results Starolesnianske pleso Twenty-four taxa of benthic macroinvertebrates belonging to five taxonomic groups have been found in Starolesnianske pleso over the studied period (Tables 1, 2).
The assemblage of the deep lake zone consists of 10 taxa. The oligochaete Tubifex tubifex, and the chironomids Procladius sp. and Heterotrissocladius marcidus appeared consistently throughout the study period, while rare taxa were inconsistent. One species, Stylodrilus heringianus was found in the oldest sampling period only, and was absent after. Four common species:Tubifex tubifex, Procladius sp., Heterotrissocladius marcidus, and Tanytarsus gregarius became increasingly abundant over time, beginning in the second half of 1990s. Twenty-one taxa constitute the littoral assemblage of the lake (Table 2). Three taxa were consistent over the study periods: the caddisfly Limnephilus coenosus and the beetles Agabus spp., Hydroporus spp. Regularly occurring representatives since the 1980s include the oligochaetes Cognettia sphagnetorum, Cernosvitoviella tatrensis, the stonefly Nemurella pictetii, and the chironomid Zalutschia tatrica. Species exclusively found in the 1930s study period include the caddisflies Limnephilus griseus, and Drusus trifidus. Nižné Terianske pleso A total of 30 taxa belonging to 6 taxonomic groups have been reported from the lake over the study period. Profundal benthic fauna consisted of 7 oligochaete and chironomid taxa (Table 3). The oligochaetes, Stylodrilus heringianus, Trichodrilus tatrensis, and Haplotaxis gordioides were regularly seen in the 1980s (Stylodrilus heringianus also in the 1930s), but nearly disappeared after, with the exception of 1994, when Cernosvitoviella tatrensis were recorded as well. The chironomids record is more consistent, although the absence of Heterotrissocladius marcidus and Micropsectra radialis in some datasets is notable. Nevertheless, the chironomid species composition can be considered to have been stable. None of the species showed discernable trends in density over time: A total of 29 taxa were documented in the lake littoral (Table 4). Three species, Crenobia alpina, Stylodrilus heringianus and Heterotrissocladius marcidus
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Table 2. Historical occurrence and abundance (individuals m−2 , and individuals 5 min−1 in 2004) of benthic macroinvertebrates in the littoral zone of Starolesnianske pleso. 19331,2
1982
1993
1994
1996
1997
20004
– – – – –
– 1 1172 244 –
– – 141 56 –
– – 40 11 –
– – 74 2 –
1 – 406 69 2
– – 100 6 –
–
20
24
39
9
23
28
+ – – – – + –
10 4 22 1 +3 10 –
– 3 16 – – – 11
3 4 20 – – – 2
4 1 19 3 1 – 13
5 2 6 3 1 – 1
7 – – – – – 5
+ + – + +
88 – +3 – –
43 – – – –
33 – – – –
54 – – – –
26 – – – –
15 – – – –
– – – – – –
– – 10 5 – –
– 13 221 – – 1
1 47 299 – – 1
26 3 87 2 – 14
17 177 98 – – 14
– 228 48 – 6 12
Oligochaeta Nais variabilis Piguet, 1906 Stylodrilus heringianus (Claparéde, 1862) Cognettia sphagnetorum (Vejdovský, 1887) Cernosvitoviella tatrensis (Kowalewski, 1916) Enchytraeidae g. sp. Plecoptera Nemurella pictetii Klapálek, 1900 (L) Coleoptera Agabus bipustulatus (L., 1768) (I) Agabus solieri Aubé, 1836 (I) Agabus sp. (L) Hydroporus ferrugineus Stephens, 1827 (I) Hydroporus incognitos Sharp, 1869 (I) Hydroporus palustris (L., 1761) (I) Hydroporus sp. (L) Trichoptera Limnephilus coenosus Curtis, 1834 (L, I) Limnephilus griseus (L., 1758) (L) Limnephilus sericeus (Say, 1824) (L) Drusus trifidus McLachlan, 1868 (L, I) Limnophilidae gen. sp. Chironomidae Procladius (Holotanypus) sp. (L, P) Heterotrissocladius marcidus (Walker, 1856) (L) Zalutschia tatrica (Pagast, 1935) (L) Chironomus sp. (L) Paratanytarsus austriacus (Kieffer, 1924) (L) Tanytarsus gregarius Kieffer, 1909 (L, P) Explanation: 1 Hrabě (1939a, b, 1942), pupae, I – adults.
2
Mayer, (1939),
3
Krno (1991),
4
Krno et al. (2006), + presence, – absence, L – larvae, P –
Table 3. Historical occurrence and abundance (individuals m−2 ) of benthic macroinvertebrates in the profundal of Nižné Terianske pleso. 19331 Oligochaeta Stylodrilus heringianus (Claparéde, 1862) Trichodrilus tatrensis (Hrabě, 1937) Cernosvitoviella tatrensis (Kowalewski, 1916) Haplotaxis gordioides (Hartmann, 1821) Chironomidae Procladius (Holotanypus) sp. (L) Heterotrissocladius marcidus (Walker, 1856) (L) Micropsectra radialis Goetghebuer, 1939 (L) Explanation:
1
Hrabě (1939a,b; 1942),
2
1979
1981
1993
1994
29 – – –
26 9 – 1
342 1022 – 52
– – – –
1 5 3 –
1200 38 10
36 44 –
3 65 8
20 – 20
13 3 –
1996
– – – – 2653 – 59
1997
– – – – 943 413 1709
Šporka (1984), + presence, – absence, L – larvae.
occurred nearly in all the datasets since the ’1930’, another two species (Ameletus inopinatus Allogamus starmachi) were recorded regularly since the 1980s, and Nais variabilis appeared consistently throughout all periods. The chironomids Macropelopia nebulosa, Zavrelimyia sp., and Corynoneura scutellata group were found exclusively during the most recent period and were absent from the historical samples. The caddisfly Philopotamus ludificatus collected in the 1930s disappeared later, while the chironomids Macropelopia nebulosa, Zavrelimyia sp., and Corynoneura scutellata group appeared during the most recent period.
Discussion What is conspicuous in Tables 1–4 is the low number of macroinvertebrate taxa recorded from earlier investigations (Minkiewicz 1914; Hrabě 1939a, b, 1942) compared to the later studies. These data are insufficient to characterize the historical macroinvertebrate assemblages in the 1910s and partly in the 1930s. It should be mentioned that Minkiewicz was interested above all in zooplankton. Some data on benthic macroinvertebrates in his paper were taken from Wierzejski (1882, 1883), and other groups of benthic macroinvertebrates were left in the hands of the other specialists.
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Table 4. Historical occurrence and abundance (individuals m−2 , and individuals 5 min−1 in 2004) of benthic macroinvertebrates in the littoral zone of Nižné Terianske pleso.
Turbellaria Crenobia alpina Dana, 1766 Oligochaeta Nais variabilis Piguet, 1906 Tubifex tubifex (M¨ uller, 1774) Stylodrilus heringianus (Claparéde, 1862) Cognettia sphagnetorum (Vejdovský, 1887) Cognettia sp. Cernosvitoviella tatrensis (Kowalewski, 1916) Enchytraeidae indet. . Haplotaxis gordioides (Hartmann, 1821) Ephemeroptera Ameletus inopinatus Eaton, 1887 (L) Plecoptera Arcynopteryx compacta (Klapálek, 1904) (L) Diura bicaudata (L. 1758) (L) Capnia vidua Klapálek, 1904 (L) Leuctra rosinae Kempny, 1900 (L) Trichoptera Drusus trifidus McLachlan, 1868 Philopotamus ludificatus McLachlan, 1868 (I) Acrophylax vernalis Dziedzielewicz, 1912 (L, I) Allogamus starmachi Szcesny, 1967 Chaetopteryx sahlbergi McLachlan 1876 (L, I) Limnophilidae gen. sp. Chironomidae Procladius (Holotanypus) sp. (L, P) Macropelopia nebulosa (Meigen, 1804) (L, P) Zavrelimyia sp. (L) Diamesa sp. (L) Pseudodiamesa branickii (Nowicki, 1837) (L) Corynoneura scutellata group (L) Heterotrissocladius marcidus (Walker, 1856) (L) Zalutschia tatrica (Pagast, 1935) (L) Micropsectra junci (Meigen, 1818) (L, P) Micropsectra radialis Goetghebuer, 1939 (L, P)
19141
19332,3
–
20006
1981
1993
1994
1996
1997
+
+
24
39
13
19
55
+ – – – – – – –
– – 24 – – – – 95
85 – 45 – – – 5 –
68 – 40 1 – 3 – –
18 – 14 – – 1 – –
66 – 24 – 4 5 – –
126 – 34 – 38 30 5 –
141 3 23 16 – – – 1
–
–
3
2
1
24
27
1
– – – –
– + – –
1 4 13 –
2 – – 2
– – – –
2 5 15 –
– 6 181 –
– 1 – –
– – – – – –
+ + – – – +
5 – 8 32 +5 –
– – – 10 – –
7 – – 4 – –
– – 1 31 – –
9 – 58 26 – –
13 – – 4 – –
– – – – – – – – – –
595 – – – 95 – 381 – – –
+4 – – +4 +4 – 290,+4 – – –
– – – – 1 – 19 3 5 –
– – – – 4 – – – – –
– – – – – – 7 – – –
– – – – 4 – 16 – 34 30
– 166 11 – – 2 96 – 44 –
Explanation: 1 Minkiewicz (1914), 2 Hrabě (1939a, b, 1942), + presence, – absence, L – larvae, P – pupae, I – adults.
3
Mayer (1939),
(e.g., oligochaetes from his collection were identified by Kowalewski), but there is no information on the fate of other benthic macroinvertebrate groups. He wrote, for example, that “larvae of Diptera collected by me from many Tatra lakes are not determined, yet”. Hrabě and his team spent five seasons in the Tatra Mts (from 1932 to 1938), and sampled 88 lakes and pools. He was the first investigator to use a quantitative method to study the benthic fauna dwelling in the Tatra Mts lakes. Hrabě was also a pioneer regarding ecological factors, and in his papers he distinguished two types of lakes based on their characteristic species composition. There is no doubt about the correctness of the macroinvertebrate identifications. He was engaged as an oligochaete specialist, and other groups were identified by respected specialists of that time (J. Zavřel, F. Pagast, K. Mayer, D.E. Kimmins, J. Mařan). Some of them published their results separately (Zavřel 1935, 1937a, b; Zavřel & Pagast 1935; Mayer 1939). However, there is some uncertainty related to the sample processing procedures. Firstly, uncounted smaller specimens (e.g., Naididae, small chironomid larvae) could have passed unobserved through the 1-mm mesh screen;
4
Ertlová (1987),
5
Krno (1991),
6
Krno et al. (2006),
secondly, many specimens could have been overlooked when animals were picked out from bottom material with the naked eye in the field, and as Hrabe reported, “. . . often in bad weather”. This could be one reason for the absence of some species in his dataset. On the other hand, we know about Hrabe’s aversion to the Enchytraeidae, which he knowingly left out mainly because of difficult determination. Another problem connected with the incomplete species data is the frequency and intensity of sampling. In fact, some species might be difficult to detect using conventional benthic sampling due to low density and/or patchy distribution (e.g., Fjellheim et al. 2001), especially during a once-a-year sampling effort. Our experience shows that some species may not be found even in ongoing yearly macroinvertebrate sampling in the same lakes (Bitušík, unpubl. data). In the case of historical data, it is difficult to decide if a particular species is really absent from a lake or if it is merely scarce or patchy. In addition, it should also be mentioned that using data from historical papers is problematic in many cases because of the lake names used by authors. For
Benthic macroinvertebrate fauna of two alpine lakes example, Minkiewicz (1914) mistook Zbojnícke plesá for Sesterské plesá and Starolesnianske pleso. This mistake was already recognized by Hrabě (1939b), who noticed that Minkiewicz’s “Starolesnianski Wyzni Staw” (in Polish) was likely Zbojnícke horné pleso. In our opinion, Starolesnianske pleso is identical with “Zbojnicki Wyžni Staw” in Minkiewicz’s paper. It is interesting that Hrabě and Mayer, who published their papers simultaneously in 1939, named Starolesnianske pleso differently. Mayer (1939) called it Líščie pleso (= Fox Lake) based on an incorrect literal translation of the name Fuchsee (= Fuchsovo pleso), which Starolesnianske pleso was called for a short period (Bohuš 1996) in honor of Fridrich Fuchs, whose family name means “fox” in German. Starolesnianske pleso Taxonomic composition of the deeper zone assemblages has remained stable through more than 60 years of sampling. Chironomids and oligochaetes dominated the assemblages in terms of both taxa richness and abundance. Observed changes in the density of dominant species over time may be connected with an increase in chlorophylla concentration during the acidification phase and chemical reversal from acidification (Fott et al. 1994). Gathering collectors, like the oligochaeteTubifex tubifex and chironomids Heterotrissocladius marcidus, and Tanytarsus gregarius may have benefited from the increased amount of food resources under conditions of temporarily high lake productivity. Procladius larvae in later instars feed mainly on small Crustacea, chironomids and oligochaetes (Vallenduuk & Moller Pillot 2007). The increase in predator density may have been followed by changes in the density of their prey. This could partly explain the fluctuations of Procladius subfossil remains in sediment records where information on oligochaetes is lacking. In considering the history of this lake, the insufficient data from earlier periods of investigations is a weakness. Although Minkiewicz mentioned benthic macroinvertebrates of four lakes named “Starolesnianski Staw” (Minkiewicz 1914), because of the confusion in lake names there are no information on benthic macroinvertebrate fauna from his studies. Unfortunately, Hrabě did not collect quantitative samples with an Ekman-Birge grab in this lake, so it is not possible to compare his results with the data obtained later. Starolesnianske pleso is a typical representative of the extremely acid-sensitive lakes in the Tatra region, with sensitivity resulting mostly from low weathering rates and soil base saturation. We had hoped that the earlier data would help explain the dramatic changes in faunal composition indicated by subfossil records. Analyses of the chironomid remains from the lake sediments revealed the most important change in the chironomid fauna in layers corresponding to the 1930s, which was characterized mainly by shifts in the relative abundance of the two dominant taxa: Tanytarsus lugens gr. and Tanytarsus gregarius. The chironomids Tanytarsus lugens gr., Micropsectra cf. insignilobus and Paratanytar-
889 sus austriacus appeared to vanish completely from the layers from ca. the mid-1980s, while the relative abundances of Tanytarsus gregarius followed by Heterotrissoclaius marcidus increased (Kubovčík & Bitušík 2006). The major shift in chironomid fauna composition coincides with the extinction of the original species of planktonic Crustacea (Hořická et al. 2006) and the MAGICreconstructed shift in water chemistry (Stuchlík et al. 2002). Unfortunately, Tanytarsus larvae were absent from Hrabě’s samples, consequently the ‘1930’ dataset cannot be used to support this palaeolimnological scheme. The finding of a single larvae of the Tanytarsus lugens group in the collection of E. Ertlová (it may be Tanytarsus bathophilus, but the incomplete head capsule does not allow a more precise identification) confirms the species survival at low abundance in the 1980s. Macroinvertebrate littoral assemblages were different between 1914 and the 1930s, and compared to more recent study periods. The long-term record has been stable since at least the 1980s because some common and frequent species were absent from samples taken in the 1930s. If we omit the Enchytraeidae that were absent for the reason mentioned above, the absence of Nemourella pictetii and chironomids, and the presence of Limnephilus griseus and Drusus trifidus, seem to be important. Hrabě writes that his investigation of the Tatra lakes was focused first of all on oligochaetes and chironomids, and admits that he did not have enough time to collect Ephemeroptera and Plecoptera (Hrabě 1942). Still, it is unlikely that he would not have found the stonefly Nemourella pictetii if it was present in the lake. The same is true for the chironomid Zalutschia tatrica that was lacking in his samples from Starolesnianske pleso although Hrabě collected the larvae from a few shallow lakes and pools in high abundance. Nemourella pictetii recently is one of the most frequent non-chironomid insects, and is indicative for acidified Tatra Mts lakes (Krno et al. 2006). Since the 1980s, Zalutschia tatrica has been a prominent component of the littoral assemblage. The species is considered a reliable indicator of acid conditions in the Tatra lakes (Kownacki et al. 1999; Bitušík et al. 2006). Despite its occurrence at high abundance, head capsules remains are not preserved in the sediment, so it cannot be used in palaeolimnological studies (Kubovčík & Bitušík 2006). Historical data from benthic samples are the only evidence of its presence and changes in abundance over time. In contrast to Ephemeroptera and Plecoptera, caddisflies were sampled in the 1930s by a specialist (Mayer 1939), thus the list of species is comprehensive. The findings of Limnephilus griseus and Drusus trifidus are remarkable for two reasons: (i) the species have never since been recorded; and (ii) Drusus trifidus is an acidsensitive species indicating non-acid lake water conditions. Consequently, these littoral species provide a useful measure of the acidification process. The assemblage is a mixture of acid tolerant – Limnephilus coenosus, Limnephilus griseus (Graf et al. 2008) and acid sensitive
P. Bitušík et al.
890 species (Drusus trifidus); therefore, it is reasonable to suppose that along with the absence of other acid tolerant species (Nemourella pictetii, Zalutschia tatrica), the lake was not yet strongly acidified at that time. The stable composition of the littoral assemblage since the 1980s indicates continued acid stress. The single finding of Paratanytarsus austriacus in 2000 could signal the beginning of recovery; however, longer-term data is required to confirm such a trend with confidence. Nižné Terianske pleso The lake assemblage was characterized by higher taxa richness reflecting the more extensive littoral that supports more diverse habitats (e.g., Bitušík et al. 2006). The macroinvertebrate fauna of both this lake and Starolesnianske pleso was analysed in detail by Krno (2006) with respect to the functional organization of assemblages, life history, ecology and distribution of species. In constrast to Starolesnianske pleso, rare endemic species for the Tatra Mts (caddisflies Acrophylax sowai Szczc˛esny, 2007, Allogamus starmachi), for the Carpathians (caddisfly Chaetopteryx polonica Dzi˛edzielewicz, 1889) and for Central European mountains (stonefly Leuctra pusilla Krno, 1985) have been representative of Nižné Terianske pleso (Krno 2006). The profundal assemblage was species-poor with Procladius sp. the most prominent species. Chironomids showed a more consistent record than oligochaetes. The lake was classified as being “Procladius type” by Hrabě (1939b), in contrast to “Stylodrilus type” with the oligochaete Stylodrilus dominating in the profundal. What is evident in Table 4 are the “gappy” records of most taxa, perhaps with the exception of Crenobia alpina, Nais variabilis, Stylodrilus heringianus, and Heterotrissocladius marcidus. The lake remained nonacidified during the peak of acidification in this area (Kopáček et al. 2004), and palaelimnological analyses have shown a relatively stable taxonomic chironomid assemblage composition throughout a period spanning perhaps 1000 years (Bitušík et al. 2009). Consequently, distinct changes in the assemblage structures over the studied period were not expected. Due to the incompleteness of our data, it is difficult to assess the possible effect of acidification on the littoral fauna. Species occurring in the littoral zone could suffer from episodic acidification during spring snowmelt (Stuchlík et al. 1985), and this effect is stronger in lakes that receive a majority of water from precipitation. Palaeolimnological records have shown that despite high lake alkalinity, acid deposition cannot be excluded as an important driving force in changes to subfossil diatom assemblages (Bitušík et al. 2009). The single finding of acid tolerant Zalutschia tatrica in 1993 may be evidence of such an event in this lake, as well. However, acid sensitive species such as Crenobia alpina, Ameletus inopinatus Diura bicaudata, Arcynopteryx compacta withstood the acidification peak in the 1980s. The appearance of the chironomids Macropelopia nebulosa, Zavrelimyia sp., and Corynoneura scutellata group could be related
to recovery, while the presence of Macropelopia nebulosa may be associated with warming of the littoral. However, caution should be applied to such conclusions because only continuous yearly macroinvertebrate sampling such as is ongoing in the Tatra Mts lakes since 2000 can help verify these hypotheses. Finally, it should be noted that Ertlová (1987) mentioned another chironomids that were collected in 1981–1982 as pupae and adults: Bryophenocladius cf. subvernalis (Edwards, 1929), Tokunagaia cf. rectangularis (Goetghebuer, 1940), Parakiefferiella coronata (Edwards, 1929), Tanypus sp., and Tanytarsus sp. The presence of these last-mentioned species is especially doubtful, as they were never recorded either before or after, and are lacking in the subfossil record of this lake (Bitušík et al. 2009). Moreover, the occurrence of Tanypus, which are generally confined to meso- to eutrophic waters (Vallenduuk & Moller Pillot 2007), is very unlikely in this alpine oligotrophic lake. Since Dr. Ertlová is a chironomid specialist, a mistake in manuscript preparation, rather than a misidentification is most probably the case. Acknowledgements We are grateful to D.W. Hardekopf for the linguistic corrections of the manuscript. The helpful comments of two anonymous referees are appreciated. This research and the manuscript preparation was funded by the European Commission Environment Programme through the EMERGE project (EVK-1-CT-1999-00032), and by the Slovak Scientific Grant Agency (VEGA, project No. 1/4334/07 and No. 1/0464/10). References Bitušík P., Svitok M., Kološta P. & Hubková M. 2006. Classification of the Tatra Mountains lakes (Slovakia) using chironomids (Diptera, Chironomidae). Biologia 61 (Suppl. 18): S191–201. DOI 10.2478/s11756-006-0131-8 Bitušík P., Kubovčík V., Štefková E., Appleby P.G. & Svitok M. 2009. Subfossil diatoms and chironomids along an altitudinal gradient in the High Tatra Mountain lakes: a multi-proxy record of past environmental trends. Hydrobiologia 631: 65– 85. DOI 10.1007/s10750-009-9802-0 Bohuš I. 1996. Od A po Z o názvoch Vysokých Tatier. Zemepisné názvoslovie Tatranského národného parku. I. časť – slovenské Vysoké Tatry. Štátne lesy TANAP-u, Tatranská Lomnica, 457 pp. Čiamporová-Zaťovičová Z., Hamerlík L., Šporka F. & Bitusik P. 2010. Littoral benthic macroinvertebrates of alpine lakes (Tatra Mts) along an altitudinal gradient: a basis for climate change assessment. Hydrobiologia 648: 19–34. DOI 10.1007/s10750-010-0139-5. Daday E. 1896. Adatok a Tátrai tavak mikrofaunájának ismeretéhez. Mathematikai és Természettudományi Értesít˝ o 14: 116–137. Daday E. 1897. Beitr¨ age zur Kenntnis der Microfauna der TatraSeen. Természetrajzi F¨ uzetek 20: 149–196. de Jong H. (ed). 2007. Fauna Europaea: Diptera, Nematocera. Fauna Europaea, version 1.3, http://www.faunaeur.org. Ertlová E. 1987. Chironomids (Chironomidae, Diptera) of the littoral of selected lakes in the High Tatras. Acta Fac. Rerum Nat. Univ. Comenianae, Zool. 29: 53–66. Fjellheim A., Tysse ˚ A. & Bjerknes V. 2001. Reappearance of highly acid-sensitive invertebrates after liming of an alpine
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