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Midges of the genus Pseudodiamesa Goetghebuer (Diptera, Chironomidae): current knowledge and palaeoecological perspective

Abstract

Larvae of the genus Pseudodiamesa Goetghebuer, which includes 12 described valid species and is divided by Makarchenko and Makarchenko (1999) into two species groups, Pseudodiamesa branickii group and Pseudodiamesa nivosa group, are widespread in lakes and running waters of cold, high-latitude and high-altitude areas of the Northern Hemisphere. Larval remains of the genus are often found in subfossil assemblages from these cold regions, but intra-genus morphotypes usually are not distinguished by palaeoecologists. Current knowledge of the ecology of the species indicates that the Pseudodiamesa nivosa group is more cold-adapted than the Pseudodiamesa branickii group and, therefore, these two intra-genus morphotypes cannot be amalgamated into a larger taxonomic unit without losing substantial information. Here we present the morphological characters of head capsules of Pseudodiamesa larvae attributed to the different species-group morphotypes, which are clearly visible in subfossil specimens. The information summarized in this paper will help provide more reliable chironomid-based palaeoclimatic inferences from lake sediment records covering colder phases through the late Quaternary in the Northern Hemisphere.

Introduction

Species of the genus Pseudodiamesa Goetghebuer, 1939 are relatively large chironomids (non-biting midges), which are recorded from all continents of the Northern Hemisphere (Pagast 1947). The taxonomy of this genus from the subfamily Diamesinae is based mainly on morphological characters of the adult males (Makarchenko 1985; Oliver 1989), but the larvae of the different Pseudodiamesa species are morphologically similar and can be difficult to separate (Oliver 1983; Makarchenko and Makarchenko 1999; Makarchenko 2006). This genus was divided into two subgenera, Pachydiamesa Oliver, 1959 and Pseudodiamesa s. str. by Oliver (1959). The first subgenus is represented by only one Nearctic species, Pseudodiamesa arctica (Malloch), and the second subgenus includes all other known species of this genus, following the nomenclature of Oliver (1959, 1983). Makarchenko and Makarchenko (1999) suggested applying a species-group nomenclature to the Pseudodiamesa larvae and dividing the genus into two species groups, the Pseudodiamesa branickii group and the Pseudodiamesa nivosa group. According to the nomenclature of Makarchenko and Makarchenko (1999), the first species group is represented by two species, namely Pseudodiamesa branickii (Nowicki) and Pseudodiamesa pertinax (Garret), and the Pseudodiamesa nivosa group includes all other known species (Table 1). Hereafter, we use the species-group nomenclature to differentiate Pseudodiamesa larvae within the genus, as this nomenclature is based on different morphological characters of the larval head capsules and can be applied to chironomid subfossil material represented by larval remains.

Table 1 Distribution of Pseudodiamesa species in the zoogeographic regions: (+) presence and (−) absence

The genus Pseudodiamesa is known as one of the cold-adapted chironomid taxa (Serra-Tosio 1976; Barley et al. 2006; Heiri and Lotter 2008). Larvae of both species groups are widespread in lakes and running waters of cold areas of the Holarctic and Oriental regions (Pagast 1947; Manca et al. 1998; Oliver et al. 1990; Makarchenko and Makarchenko 1999). Studies of fossil chironomid assemblages indicate that Pseudodiamesa was common in lakes during past cold climate phases of the late Quaternary (Ilyashuk et al. 2008; Kurek et al. 2009).

High-latitude and high-altitude regions are especially sensitive to the effects of recent climate warming (Ørbæk et al. 2004). In recent years, palaeoclimate studies in these remote regions have received increasing attention by the scientific community. Interest in chironomid-based palaeoclimate inferences has grown, especially over the past decade, driven largely by the potential for using chironomids to infer palaeotemperatures accurately and independently of other methods (Walker and Cwynar 2006). Larval remains of the genus Pseudodiamesa are quite often found in subfossil chironomid assemblages from these cold regions, but intra-genus morphotypes are usually not distinguished by palaeoecologists (Larocque et al. 2001; Barley et al. 2006; Heiri and Lotter 2008). Previous studies in the European Alps (Pagast 1947; Serra-Tosio 1973, 1976; Rossaro et al. 2006) and the Nepalese Himalayas (Manca et al. 1998), however, have shown that the Pseudodiamesa species, which can be attributed to different species groups, but live together in these mountain areas, prefer different altitudes and/or temperature conditions within lakes and streams. As demonstrated by Brooks et al. (2007), many morphotypes within other genera show different distributions along environmental gradients than the genus as a whole, and therefore have the potential to be useful palaeoecological indicators. Thus, identification of Pseudodiamesa subfossil remains to a more precise taxonomic level would provide more reliable palaeoclimate inferences.

The aim of this work was to assess whether intra-genus morphotypes of Pseudodiamesa larvae can be differentiated reliably in subfossil material from surface and down-core samples. To achieve this objective, it is necessary to determine the morphological characters of head capsules of Pseudodiamesa larvae that are clearly visible in subfossil remains. Here we used subfossil specimens represented by both Pseudodiamesa species groups, which were collected in the European Alps and Northern Russia to examine several key morphological features described in the available literature for identification of contemporary Pseudodiamesa larvae. In addition, we provide a short summary of the zoogeography and ecology of Pseudodiamesa species, which will contribute to palaeoecological interpretation of subfossil records.

Zoogeography

At the end of the twentieth century, there were 11 valid Pseudodiamesa species known to science from the Holarctic and Oriental regions (Makarchenko and Makarchenko 1999). More recently, a twelfth species, Pseudodiamesa sunabacedea Tanaka and Sasa, was described from Japan (Tanaka and Sasa 2001) (Table 1).

At present, three Pseudodiamesa species are known from the Nearctic, where they are recorded only from western and northern areas (Oliver et al. 1990; Epler 2001). The P. nivosa group is represented there by P. arctica, and the P. branickii group is represented by two species, P. branickii and P. pertinax.

In the Palaearctic and Oriental regions, the P. branickii group is represented only by widespread P. branickii. The P. nivosa group is represented by one species, Pseudodiamesa nepalensis Reiss, in the Oriental region (Nepalese Himalayas; Manca et al. 1998) and by eight other species in the Palaearctic region. Among the Palaearctic Pseudodiamesa species belonging to the P. nivosa group, Pseudodiamesa nivosa (Goetghebuer) is the most widely distributed species known from both eastern and western areas of the Palaearctic (Table 1). Schnell and Willassen (1991) suggested that the Nearctic P. arctica and the Palaearctic P. nivosa are the same species and should be named P. arctica, as this is the older name (Sæther and Spies 2004). Makarchenko (2009), however, compared adult morphological characteristics of both species and showed that they are two valid sister species.

Another of the widely distributed Palaearctic species from the P. nivosa group is Pseudodiamesa stackelbergi (Goetghebuer) known from both eastern and western areas. The other species are restricted to smaller areas of the Palaearctic. Furthermore, the immature stages of the four Palaearctic species are unknown (Table 1).

Ecology

Larvae of the genus Pseudodiamesa are detritus feeders that gather fine particulate organic matter, but can prey on smaller chironomids and other small aquatic invertebrates as well (Pagast 1947). The species are well adapted to harsh physical environments and can complete their life cycle where water temperatures never exceed 2°C (Milner et al. 2001). On the other hand, the larvae can enter diapause during relatively long periods of low temperatures, when conditions are not suitable for activity. Usually, all instars develop during summer, enter diapause at the 4th instar, and emerge synchronously the next year during the springtime thaw period (Oliver 1959; Tátosová and Stuchlík 2006). Adults of Pseudodiamesa emerge through cracks in the ice cover at the onset of thawing, and can copulate on the snow cover at sub-zero temperatures (−1 to −2°C; Oliver 1964; Danks and Oliver 1972; Hågvar and Østbye 1973). Diapausal eggs of Pseudodiamesa, frozen and covered by snow, were also found in early spring near an Alpine glacial stream (Lencioni 2004). In contrast to the high degree of synchrony observed in mountain and Arctic lakes, stream studies suggest that emergence is not synchronized by diapause (Hayes and Murray 1987). Studies from North America and Europe indicated that the Pseudodiamesa species are usually univoltine (Oliver 1959; Tátosová and Stuchlík 2006). However, there is evidence that P. branickii exhibits bi- and trivoltinism under warmer conditions at lower altitudes and latitudes (Nolte and Hoffmann 1992).

Our knowledge of the ecology of the Pseudodiamesa species is still fragmentary. The most comprehensive studies of the ecology and distribution of the Pseudodiamesa species are from Western Europe, where the genus is represented by P. branickii and P. nivosa, i.e. every species group is represented by a single species. Both species are common and widespread taxa in the European Alps (Boggero et al. 2006; Rossaro et al. 2006), the Tatra Mountains (Bitušík et al. 2006; Krno et al. 2006), the Pyrenees (Rieradevall and Prat 1999), Arctic and sub-arctic regions of Fennoscandia (Paasivirta 2009) and Iceland (Langdon et al. 2008). In the European Alps, P. branickii prefers altitudes between 200 and 2,300 m asl, whereas P. nivosa dwells mainly at altitudes of 2,000–3,000 m asl (Pagast 1947; Serra-Tosio 1973; Janecek 1998). Nevertheless P. nivosa can also colonize cold habitats of the periglacial zones at lower altitudes, 345–230 m asl (Siciński 1988).

Though both Pseudodiamesa species are known from lakes and running waters of Western Europe, P. nivosa prefers the cold profundal of Arctic and alpine lakes, where in some cases it displays very abundant populations (Nauwerck 1981; Lindegaard 1992; Tátosová and Stuchlík 2006). P. branickii is more common in running waters and the littoral zone of lakes (Bretschko 1974; Boggero et al. 2006; Rossaro et al. 2006). Previous studies of chironomids from European glacier-fed streams have shown that P. nivosa survives in the first 100 m from a glacier, where water temperature does not exceed 2°C. It colonises downstream habitats with maximum temperature <9°C, whereas P. branickii is associated with “non-glacial” conditions and can be very abundant further downstream in biotopes where the water temperature does not exceed 18°C (Janecek et al. 2002; Lods-Crozet et al. 2001; Lencioni and Rossaro 2005). According to Rossaro et al. (2006), who calculated water temperature optima for the chironomid taxa living in running waters in the Southern European Alps above 800–1,000 m asl, P. branickii is characterised by a higher temperature optimum than P. nivosa (4.90 and 4.45°C, respectively). In addition, the larvae of both species tolerate low pH and occur in acidified lakes and streams (Braukmann and Biss 2004; Bitušík et al. 2006).

The Pseudodiamesa species from Nearctic and Oriental regions demonstrate a similar difference in ecological preferences of the two species-group morphotypes. The Nearctic P. arctica and the Oriental P. nepalensis, both belonging to the P. nivosa group, prefer the cold profundal of lakes and, like their sister species P. nivosa in the Palaearctic region, often produce very abundant populations in large arctic lakes of North America (Oliver 1964, 1976) and in deep, high alpine lakes and glacial pools of the Nepalese Himalayas (Roback and Coffman 1987; Manca et al. 1998), respectively. Both species belonging to the P. branickii group from North America, P. pertinax and P. branickii, occupy similar warmer biotopes, namely the littoral zone of lakes and “non-glacial” habitats of springs and streams (Mackay 1969; Elgmork and Sæther 1970; Sæther 1970). Mackay (1969) found that the Nearctic P. pertinax is able to survive in the stream biotopes where the water temperature reaches 17.2°C. In high alpine lakes of the Oriental region, P. branickii is also restricted to habitats within the warmer littoral (Manca et al. 1998).

The information presented above suggests that the P. nivosa group is more cold-adapted than the P. branickii group, which occurs under more moderate conditions. Unfortunately, our knowledge of the ecology of some Eastern Palaearctic species belonging to the P. nivosa group is poor. The distribution and ecology of the four species is restricted and comes only from the occurrence of the adult forms. It would be helpful to study the adults and immatures together, but this is not always practical. Current knowledge of the ecology of both species groups suggests that all the sister species forming the P. nivosa group have similar environmental preferences within different zoogeographic regions.

Materials and methods

Subfossil material from surface and down-core samples gathered in the European Alps and Northern Russia was used in this study. Material including Pseudodiamesa nivosa species-group subfossils was taken from sediment sequences (core tops and lower parts) retrieved from three sites: (1) Nikolay Lake, a large Arctic lake situated in northeast Russia (73°20′N, 124°12′E; ~1 m asl); (2) Schwarzsee ob Sölden, a high alpine lake located at 2,796 m asl in the Ötztaler Alps, Austria (46°58′N, 10°57′E); and a palaeo-lake near the Maloja Pass, Central Alps, Switzerland (46°24′N, 9°41′E; 1,865 m asl). Cores were collected at all three sites to produce late Quaternary palaeoclimate reconstructions (Andreev et al. 2004; Ilyashuk et al. 2008, 2009). Material including Pseudodiamesa branickii species-group subfossils was taken from surface and down-core sediment samples that were collected from Lake Golcovoe, a subarctic lake situated on the Kola Peninsula, northwest Russia (67°50′N 33°40′E; 208 m asl), and from surface sediment samples collected at Weißenbach, a first-order tributary of the Inn River, Austria (47°17′N, 11°31′E; 605 m asl). In addition, material including subfossils of both the Pseudodiamesa species groups was taken from surface sediment samples collected at Matscherjochsee, a high alpine lake located 3,188 m asl in the Italian Alps (46°47′N, 10°41′E). At least 40 Pseudodiamesa head capsules from every site were examined.

The Pseudodiamesa head capsules were picked from the fresh sediment in a Bogorov counting tray at 40–50× magnification under a stereomicroscope. After dehydration they were mounted on glass slides in Euparal® mounting medium for microscopic identification. Taxonomic identification of the Pseudodiamesa intra-genus morphotypes was accomplished using different key morphological characters of the larval head capsules described in Oliver (1959, 1983), Makarchenko (1985, 2006), Schmid (1993), Janecek (1998), Makarchenko and Makarchenko (1999), and Epler (2001). Morphological terminology is consistent with that of Sæther (1980).

Results

Key morphological characters: contemporary versus subfossil material

The Pseudodiamesa larvae belonging to the different species groups are separable by several morphological characters, namely by antennal ratio, pecten epipharyngis, mandibular seta interna, and mentum, following Makarchenko and Makarchenko (1999). Morphological features of the larval head capsules described in the identification keys to the contemporary Pseudodiamesa larvae, and summarised in Table 2, were used to identify subfossil specimens.

Table 2 Morphological characters of the Pseudodiamesa larval head capsules for identification of the species-group morphotypes within contemporary and subfossil material

Labral lamellae and labral setae SI

The larvae of P. arctica can be separated from all other Pseudodiamesa species by having labral lamellae (Oliver 1959, 1983). The larvae of P. arctica and P. pertinax belonging to the P. nivosa group and the P. branickii group, respectively, are separable from all other Pseudodiamesa species by the shape of labral setae SI. P. arctica has simple seta-like SI and P. pertinax has apically bifid SI, whereas all known larvae of other Pseudodiamesa species are characterized by lamelliform SI (Oliver 1983). Unfortunately, labral lamellae and labral setae SI are rarely preserved in subfossil specimens and these characters thus cannot be used to distinguish chironomid taxa in subfossil material.

Mandibular seta interna

Mandibular setae interna of the P. nivosa group consist of 14–24 branches according to Makarchenko (1985, 2006) and Makarchenko and Makarchenko (1999), and 18–23 branches according to Schmid (1993), whereas mandibular setae interna of the P. branickii group consist of 9–15 branches (10–15 branches according to Schmid (1993) and 9–13 according to Makarchenko (1985, 2006) and Makarchenko and Makarchenko (1999)). Unfortunately, the mandibular setae interna are rarely preserved and usually absent in subfossil specimens (Table 2).

Antennal ratio and pecten epipharyngis

Other key morphological features for the separation of the Pseudodiamesa species-group morphotypes are the antennal ratio and pecten epipharyngis, which are often preserved in subfossil specimens (up to 30% of subfossils; Table 2) (Fig. 1a–f). The antenna of the P. nivosa-group larvae is characterized by an antennal ratio ≥2.5, whereas the antennal ratio of the P. branickii group is <2.5 (Makarchenko 1985, 2006; Schmid 1993; Janecek 1998; Makarchenko and Makarchenko 1999). The pecten epipharyngis of the P. nivosa-group larvae consists of an even number, namely 3–4 pairs, of broad, elongate, apically blunt scales (Fig. 1c, d), but that of the P. branickii-group larvae is characterized by an odd number, namely seven scales (Fig. 1e, f) (Makarchenko 1985, 2006; Makarchenko and Makarchenko 1999; Epler 2001) (Fig. 1e, f). Our inspection of the subfossils showed that the pecten epipharyngis of the species P. branickii consists of seven very weakly sclerotized scales (Fig. 1e, f), whereas that of the species P. nivosa consists of six strongly sclerotized scales (Fig. 1c, d). The pecten epipharyngis consisting of seven scales was assigned mistakenly to the species P. nivosa by Schmid (1993) and Janecek (1998), and to all the Pseudodiamesa species in Oliver (1983), whereas the species P. arctica has a pecten epipharyngis consisting of eight scales (E. Makarchenko, personal observation). In both species groups, two outer pairs of scales often overlap the chaetulae laterales and are difficult to see. Median scales, having paired or unpaired character, can however, be used for the separation of the Pseudodiamesa species-groups (Makarchenko and Makarchenko 1999; Makarchenko 2006) (Table 2).

Fig. 1
figure 1

Pseudodiamesa: antenna (a, b); labro-epipharyngeal region and median scales (MS) of pecten epipharyngis (c, e); pecten epipharyngis and median scales (MS) (d, f); unflattened mentum of 3rd (g), 4th (h, i), and 2nd (k) instars; flattened mentum of 4th instar (j). Pseudodiamesa nivosa (Goetghebuer) (a, c, d, g, h); Pseudodiamesa branickii (Nowicki) (b, e, f, i, j); Pseudodiamesa ind. (k)

Mentum

The mentum is a well-preserved structure in subfossil specimens and can be one of the best morphological characters for differentiating Pseudodiamesa species-group morphotypes in subfossil material. All teeth of the mentum of the P. branickii-group are similar in colour, whereas the P. nivosa group has a mentum with a lighter median tooth than the lateral black teeth (Makarchenko 1985, 2006; Makarchenko and Makarchenko 1999) (Fig. 1g–j). In addition, lateral teeth are more visible in the unflattened mentum of the P. nivosa group than in that of the P. branickii-group (Makarchenko 1985) (Fig. 1h, i). Finally, the 1st and 2nd instars of both subgenera have an identical mentum, with a broad median tooth that is lighter than the lateral blackish teeth (Fig. 1k).

Conclusions

We concluded that the species-group morphotypes of Pseudodiamesa larvae can be differentiated within the subfossil material from surface and down-core samples using a combination of morphological characters, namely the mentum, pecten epipharyngis, and antennal ratio (Table 2). The Pseudodiamesa species groups from different zoogeographic regions demonstrate similar ecological preferences. Thus, more precise taxonomic identification and splitting of the genus into two intra-genus morphotypes could improve existing chironomid-temperature transfer functions and provide better palaeoclimate reconstructions and palaeolimnological interpretation of subfossil chironomid records.

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Acknowledgments

Data presented in this manuscript were produced, in part, during research funded by the European Commission (FP7-PEOPLE-2007-4-2-IIF-ENV, Marie Curie Fellow grant no. 219881 to B. Ilyashuk) and the Austrian Science Fund (FWF grant M964-N10 to E. Ilyashuk). We thank Karin Koinig and Roland Psenner (University of Innsbruck, Austria), and André F. Lotter (Utrecht University) for scientific and logistic support. We are grateful to Mark Brenner and two anonymous reviewers for their useful comments and suggestions on an earlier draft of the manuscript.

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Ilyashuk, B.P., Ilyashuk, E.A., Makarchenko, E.A. et al. Midges of the genus Pseudodiamesa Goetghebuer (Diptera, Chironomidae): current knowledge and palaeoecological perspective. J Paleolimnol 44, 667–676 (2010). https://doi.org/10.1007/s10933-010-9446-0

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Keywords

  • Chironomids
  • Pseudodiamesa
  • Larval subfossils
  • Taxonomy
  • Palaeoclimate