Zootaxa 2026: 47–52 (2009)
www.mapress.com / zootaxa/
ISSN 1175-5326 (print edition)
Article
Copyright © 2009 · Magnolia Press
ZOOTAXA
ISSN 1175-5334 (online edition)
The pupal exuviae of Chironomus crassimanus Strenzke (Diptera:
Chironomidae), an acid-resistant species from Germany
GILBERTO GONÇALVES RODRIGUES1,4, PETER H. LANGTON2 & BURKHARD W. SCHARF3
1
UFZ-Helmholtz Centre for Environmental Research Leipzig-Halle, Dept. of Inland Water Research Magdeburg, Brückstr. 3A, 39114
Magdeburg, Germany
2
University Museum of Zoology Cambridge, Downing Street, Cambridge, UK
3
Ellhornstr. 21, D-28195 Bremen, Germany. Earlier: UFZ-Helmholtz Centre for Environmental Research Leipzig-Halle, Dept. of
Inland Water Research Magdeburg
4
Corresponding author: Universidade Federal da Bahia-UFBa, Instituto de Biologia, Depto. de Botânica. Rua Barão de Jeremoabo,
s/n-Campus Universitário de Ondina, CEP: 40170–115 Salvador-Bahia, Brasil. E-mail: biol.gilbertorodrigues@gmail.com
Abstract
The first descriptions of the pupal exuviae of Chironomus crassimanus Strenzke, 1959 were based on mixed populations
of Chironomus which did not allow a proper recognition of their features in the available taxonomical keys. This paper
describes the morphological characteristics of Ch. crassimanus based on laboratory-reared specimens. A more
comprehensive description is ensued and ecological information on the species is also provided.
Key words: Chironomidae, Chironomus, systematics, pupa, acid water
Introduction
Species of the genus Chironomus Meigen, 1803 are distributed in all zoogeographical regions except
Antarctica (Ashe 1983) and have been reported in extremely acidic ecosystems (Rodrigues 2001, Rodrigues
& Scharf 2001). Chironomus comprise several hundred species, some of which are discernible only on
cytological characters (Correia & Trivinho-Strixino 2007). More than 50 valid European species of
Chironomus have been described so far (Fittkau & Reiss 1978, Lindeberg & Wiederholm 1979, Vallenduuk &
Moller Pillot 1999), but the taxonomic descriptions have been mostly based on features of the imaginal and
larval stages alone, so that few studies have aimed at an in-depth description of their pupae/exuviae (but see
Langton 1991).
A key species found in extremely acidic mining lakes, pH 2–3, in Eastern Germany, Chironomus
crassimanus Strenzke, 1959 had described his exuviae based on a few specimens mounted on slides in the late
1950’s. The relevance of this species as an acid-resistant bioindicator propels further studies on its
reexamination, in order to offer a more accurate description of their immature stages.
Here, we describe the pupal exuviae of Ch. crassimanus based on laboratory-reared specimens, and
provide information on their morphology that facilitates the identification of the species. Further discussion
on the ecology and distribution of the species is also incorporated.
Methods and morphology
Egg masses of Ch. crassimanus were collected from littoral macrophytes acidic in Lusatian mining lakes,
eastern Germany lakes in July–September 1998. Eggs were reared in the laboratory in batches in 150 ml water
Accepted by W. Gilka: 1 Dec. 2008; published: 4 Mar. 2009
47
from the lake. The water was aerated continuously and leaves of Urtica dioica L. (Urticaceae) were added as
food source. Emerged adults were collected daily and 4 t h instar larvae were taken for karyological
examination. The larvae were prepared by the first author and identified by Prof. Dr. W. Wülker. Pupal
exuviae were taken after emergence of the adults in the laboratory. Morphological nomenclature follows that
of Langton (1991, 1994 and 1995) and Langton & Armitage (1995). Pupal exuviae were deposited in the
Zoologische Staatssammlung (ZSM), in Munich, Germany and in the authors’ collection.
Description
Pupa
Colour: Cephalothorax pale brown, darker brown anteriorly before and behind the oblique hinge line
(Langton 1995) and posteriorly above the base of the wing sheath. Wing sheaths broadly streaked with pale
brown and margined with darker brown. Abdomen colourless with lateral adhesion marks (Langton 1994)
golden brown diminishing in length from segment II to VI and a golden brown streak along the parasternites
from segment V to VIII intensifying and becoming broader posteriad. Anal lobes golden brown, transparent at
base and with a narrow pale streak along the insertion of the fringe.
Exuvial length 8.2–10.0 mm (n = 9).
Cephalothorax: Cephalic tubercle (Fig. 1A) elongate conical, 70–120 µm high (n = 8); frontal seta 48–62
µm long (n = 3). Thorax with distinct small granulation anteriorly, becoming weaker posteriad, mid thorax
reticulate or smooth (Fig. 1B). Basal ring of thoracic horn (L x W) 140 x 60 µm – 180 x 90 µm (n = 10);
tracheole diameter 2.7–3.3 µm (n = 3).
Abdomen: Tergite I bare; point patches of tergites II–VI moderately developed for the genus (Figs. 2A,
2B), the points dense, overlapping those of the previous row; the patch on VI reduced in lateral extent in the
posterior half of the tergite, to form a wine glass shaped pattern. Tergite VII with an anterior pair of patches of
small points anterior to setae D1, narrowly separated medially or joined by shagreen. Tergite VIII with a large
patch of strong points on each side, some points often arranged in groups of two or three. Hook row of
segment II about half segment width, of 68–108 hooks (n = 9). Conjunctives IV/V, V/VI, VI/VII dorsally
armed with small spinulate points. Paratergites V and VI with a longitudinal narrow band of spinulate points.
Pedes spurii B on pleuron II well developed. Pleuron IV armed with dense narrow spinules up to 14µm long
(Fig. 2A). Sternites (Fig. 1C): II nearly covered with small isolated points; III with lateral longitudinal bands
of small points anteriorly spreading inwards, but not meeting medially; IV without lateral longitudinal point
bands, though the anterior inward extensions may be developed; V as IV; VI and VII with antero-lateral
patches of small points. Parasternite II shagreened; IV with well developed vortex, not extended anteriad; V
and VI armed with small points posteriorly. Spur of segment VIII with 1–4 robust long–acuminate teeth. Anal
fringe with 86–116 (n = 10) taeniae Chaetotaxy (D = dorsal, V = ventral, L = lateral setae; DT = dorsal
taeniae; LT = lateral taeniae).
D
I
II
III
IV
V
VI
VII
VIII
2
3
5
5
5
5
5
2
DT
L
1
0
3
3
4
LT
V
IX
2
3
3
3
4
4
(3)4
3–5
3
4
4
2
Diagnosis. The description of Chironomus crassimanus in Langton (1991) was based on a slide from the
ZSM containing three exuviae from Strenzke’s original rearing. However, because the rearing was done from
48
· Zootaxa 2026 © 2009 Magnolia Press
RODRIGUES ET AL.
egg masses collected in the wild, undetected by Strenzke, two species emerged; re-examination of the slide
reveals one exuviae of Ch. crassimanus and two of an undescribed Chironomus. Neither species will run to
Ch. crassimanus in Langton’s (1991) key, because the character set used in placing the taxon is a mosaic
derived from both species.
FIGURE 1. Chironomus crassimanus pupal exuviae. A: frontal apotome. B: thorax, lateral. C: sternites II–IV. (scale
lines = 0.1 mm)
The pupal exuviae of Ch. crassimanus may be distinguished from other species of moderate size (8–12
mm length) by the following combination of characters: thorax distinctly, but not densely, small granulate
anteriorly only, reticulate elsewhere; sternite II nearly covered with small points, sternite III with lateral
longitudinal bands of small points spreading inwards anteriorly to form a transverse band, broken medially,
and sternite IV bare or with some small points forming a medially broken anterior band.
Ecology and distribution. Ch. crassimanus was described by Strenzke (1959) from a clay pool, named
Tonteich near Reinbek, in Northern Germany with a pH of 3.05. Rodrigues (2001) found Ch. crassimanus to
be a pioneer and dominant acid-resistant species in mining lakes of pH 2–3 in eastern Germany. The most
striking physical characteristic of these mining lakes are their extremely low pH and range of colour:
CHIRONOMUS CRASSIMANUS, AN ACID-RESISTANT SPECIES
Zootaxa 2026 © 2009 Magnolia Press ·
49
red–brown. These red hues are probably caused by contamination of dissolved iron compounds (FeS 2)
stemming from pyrite and marcasite associated to the coal. Ch. crassimanus can tolerate a wide range of
dissolved iron (0.36–9.84 mmol L-1), sulphate (4.47–27.92 mmol L-1) and aluminium (0.071–1.91 mmol L-1)
(Rodrigues 2001).
FIGURE 2. Chironomus crassimanus pupal exuviae. A: tergites II–IV. B: tergites VI–VII. C: spur of segment VIII.
(scales line = 0.1 mm)
50
· Zootaxa 2026 © 2009 Magnolia Press
RODRIGUES ET AL.
Adaptation to highly acid waters is known to have occurred in the genus Chironomus a number of times.
Three species have been reported from volcanic regions of Japan: Ch. acerbiphilus Tokunaga, 1939 from
Lake Katanuma (Fujimatsu 1938) with pH 1.4 (Yoshimura 1933), Ch. fusciceps Yamamoto, 1990 and Ch.
sulfurosus Yamamoto, 1990 from hot sulphurous springs with pH 2.9–4.3 (Uéno 1932, 1933, Itô 1937;
reported by Yamamoto 1986). According to Yamamoto (1986), these form a distinct species group, the male
hypopygium having appendage 1 broad apically, and the gonostylus short and broad. Ch. harpi Sublette, 1991
from acidic lakes (pH about 3, Zullo & Stahl 1988) in strip-mined areas of Illinois, USA, has appendage 1
long and narrow (Wülker et al. 1991), whereas in Ch. crassimanus it is short and somewhat swollen medially
(Strenzke 1959). Bates & Stahl (1985) demonstrated for Ch. harpi (as Chironomus nr. maturus) that growth
rates were slower at pH 6.6, implying that the more acid environments are optimal. There appears to be
primitive facility in the Chironomus genome for adaptation to extreme acidic conditions not shared by other
genera of the Chironomini.
Acknowledgements
The authors thank Prof. W. F. Wülker for karyosystematic analysis of Ch. crassimanus, Dr. Martin Spies and
Dr. Simão Dias Vasconcelos for review of the manuscript, and DAAD (Germany) and CAPES (Brazil) for the
scholarship.
References
Ashe, P. (1983) A catalogue of chironomid genera and subgenera of the world including synonyms (Diptera:
Chironomidae). Entomologica scandinavica Supplement, 17, 1–68.
Bates, N.M. & Stahl, J.B. (1985) Effect of pH and total ion concentration on growth of Chironomus nr. maturus larvae
(Diptera: Chironomidae) from an acid strip-mine lake. Transactions of the Illinois Academy of Science, 78, 127–132.
Correia, L.C.S. & Trivinho-Strixino, S. (2007) New species of Chironomus Meigen (Diptera: Chironomidae:
Chironominae) from Brazil. Zootaxa, 1504, 53–68.
Fitkau, E.J. and Reiss, F. (1978): Chironomidae, Limnofauna Europaea. - Illies, J. Gustav Fischer Verlag, Stuttgart, 404440 pp.
Fujimatsu, K. (1938) A study on animals and plants in a highly acidic lake, Katanuma. Seitaigaku Kenkyu, 4, 131–140.
[In Japanese.]
Langton, P.H. (1991) A key to pupal exuviae of West Palaearctic Chironomidae. Privately published, Huntingdon,
Cambridgeshire, 386 pp.
Langton, P.H. (1994) Adhesion marks on the abdomen of pupal Chironomidae (Diptera). British Journal of Entomology
and Natural History, 7, 89–91.
Langton, P.H. (1995) The pupa and events leading to eclosion. In: Armitage, P.D., Cranston, P.S. & Pinder, L.C.V.P.
(Eds.), The Chironomidae: Biology and ecology of non-biting midges. Chapter 8. Chapman & Hall, London, pp.
169–193.
Langton, P.H. & Armitage, P.D. (1995) Rheotanytarsus rioensis (Diptera: Chironomidae), a new species of the
pentapoda group from the Canary Islands. British Journal of Entomology and Natural History, 8, 11–17.
Lindeberg, B. & T. Wiederholm, 1979. Notes on the taxonomy of European species of Chironomus (Diptera:
Chironomidae). Ent. stand. Suppl. 10 : 99-116.
Rodrigues, G.G. (2001) Benthic fauna of extremely acidic lakes. UFZ-Bericht, 23/2001, Leipzig, 131 pp.
Rodrigues, G.G. & Scharf, B.W. (2001) Review of benthic invertebrate fauna in acidic environments (pH ≤ 3). Mine
Water and the Environment, 20, 114–121.
Strenzke, K. (1959) Revision der Gattung Chironomus Meig. I. Die imagines von 15 norddeutschen Arten und
Unterarten. Archiv für Hydrobiologie, 56, 1–42.
Tokunaga, M. (1939) Chironomidae from Japan (Diptera) X. New or little-known midges, with descriptions of the
metamorphosis of several species. The Philippine Journal of Science, 65, 313–383.
Vallenduuk, H.J. & Moller Pillot, H.K.M. (1999) Key to the larvae of Chironomus in Western Europe. Privately
published, 18 pp.
Webb, C.J. & Scholl, A. (1990) The larval morphology of European Chironomus species C. acidophilus Keyl and C.
CHIRONOMUS CRASSIMANUS, AN ACID-RESISTANT SPECIES
Zootaxa 2026 © 2009 Magnolia Press ·
51
crassimanus Strenzke (Dipt.: Chir.). Revue suisse de Zoologie, 97, 31–48.
Wülker, W., Sublette, J.E. & Martin, J. (1991) Chironomus utahensis Malloch and Chironomus harpi new species and
their karyosystematic relationships to other species in the decorus-group of Chironomus (Chironomidae: Diptera).
Spixiana, 14, 71–94.
Yamamoto, M. (1986) Study of the Japanese Chironomus inhabiting high acidic water (Diptera, Chironomidae) I.
Kontyu, 54, 324–332.
Yamamoto, M. (1990) Study of the Japanese Chironomus inhabiting high acidic water (Diptera: Chironomidae) II.
Japanese Journal of Entomology, 58, 167–181.
Yoshimura, S. (1933) Katanuma, a very strong acid-water lake on Volcano Katanuma, Miyagi Prefecture, Japan. Archiv
für Hydrobiologie, 26, 197–202.
Zullo, S.J. & Stahl, J.B. (1988) Abundance, distribution and life cycles of midges (Chironomidae: Diptera) in an acid
strip-mine lake in southern Illinois. American Midland Naturalist, 119, 353–365.
52
· Zootaxa 2026 © 2009 Magnolia Press
RODRIGUES ET AL.
