Skip to main content
NCBI home page
UKPMC Funders Author Manuscripts logoLink to UKPMC Funders Author Manuscripts
. Author manuscript; available in PMC: 2016 Mar 10.
Published in final edited form as: Zootaxa. 2015 May 13;3957(1):85–97. doi: 10.11646/zootaxa.3957.1.7

Larval description of Drusus bosnicus Klapálek 1899 (Trichoptera: Limnephilidae), with distributional, molecular and ecological features

MLADEN KUČINIĆ 1,7, ANA PREVIŠIĆ 1, WOLFRAM GRAF 2, IVA MIHOCI 3, MARIN ŠOUFEK 3, SVJETLANA STANIĆ-KOŠTROMAN 4, SUVAD LELO 5, SIMON VITECEK 6, JOHANN WARINGER 6
PMCID: PMC4785675  EMSID: EMS67466  PMID: 26249056

Abstract

In this study we present morphological, molecular and ecological features of the last instar larvae of Drusus bosnicus with data about distribution of this species in Bosnia and Herzegovina. We also included are the most important diagnostic features enabling separation of larvae of D. bosnicus from larvae of the other European Drusinae and Trichoptera species.

Keywords: Drusinae, 5th instar larva, identification, morphology, Bosnia and Herzegovina

Introduction

The Balkan Peninsula is one of the most interesting centres of diversity for different animal groups in Europe (e.g., Gottstein-Matočec et al. 2002; Džukić & Kalezić 2004; Kryštufek 2004; Bedek et al. 2006; Bilandžija et al. 2013) including Trichoptera (e.g., Kumanski & Malicky 1999; Malicky 2005; Oláh 2010, 2011). In this region (Albania, Bosnia and Herzegovina, Bulgaria, Croatia, Kosovo, Macedonia, Montenegro, Serbia, Greece) 40 species from the Eurasian genus Drusus (family Limnephilidae) have been recorded (Schmid 1956; Radovanović 1942; Krušnik 1987; Kumanski 1988; Malicky 2004, 2005; Oláh 2010, 2011; Oláh & Kovács 2013). Except Drusus botosaneanui Kumanski 1968, Drusus discolor (Rambur 1842), Drusus biguttatus (Pictet 1834) and Drusus tenellus (Klapálek 1898), all other Drusus species are endemic to this region. Drusus tenellus and D. botosaneanui also occur in Romania, D. biguttatus and especially D. discolor are widespread throughout Europe. Drusus larvae usually inhabit springs and the crenal section of mountain streams and rivers with low water temperature.

Within family Limnephilidae, one of the most interesting groups is the Drusus bosnicus Group (Schmid 1956) with numerous endemic species described from the Balkan Peninsula (e.g., Radovanović 1942; Marinković-Gospodnetić 1976). All species of the Drusus bosnicus Group share some morphological and behavioural features like the shape of male genitalia, the dark coloration of adults and daylight activity. The first species described from this group at the end of the 19th century was Drusus bosnicus Klapálek 1899 (Fig. 1), with locus typicus at the spring of the River Bosna situated in Sarajevo, central Bosnia and Herzegovina (Fig. 2). Recently, eight the newly described species from Albania and Greece (Oláh 2010, 2011) were found to belong to the Drusus bosnicus Group. The main distribution area of the Drusus bosnicus Group is the Balkan Peninsula with more than 20 described species (e.g., Radovanović 1942; Marinković–Gospodnetić 1976; Kumanski 1988). So far, larvae of 5 species of the Drusus bosnicus Group from the Balkan Peninsula have been described: Drusus klapaleki Marinković-Gospodnetić 1971a, Drusus medianus Marinković-Gospodnetić 1976, Drusus radovanovici Marinković-Gospodnetić 1971a, Drusus ramae Marinković-Gospodnetić 1971a, and Drusus septentrionis Marinković-Gospodnetić 1976 (Kučinić et al. 2008, 2010, 2011a, 2011b).

FIGURES 1-3.

FIGURES 1-3

Open in a new tab

1, Drusus bosnicus Klapálek 1898, adults in copula; 2, Bosnia and Herzegovina with distribution of D. bosnicus; 3, spring of the Paljanska Miljacka River, site where larvae and adults of D. klapaleki Marinković-Gospodnetić 1971a were collected.

In this study we present morphological features of the last instar larvae of Drusus bosnicus, combined with molecular and ecological notes and distribution data on this species. We also present the most important diagnostic features enabling separation of larvae of D. bosnicus from larvae of the other European Drusinae species.

Material and Methods

Fieldwork and sampling

The studied material of D. bosnicus comprises 10 larvae and one adult, collected on 17 May 2008, all of them from the spring of the Paljanska Miljacka River (Fig. 3), situated 15 kilometres southeast of Sarajevo, and two adults of D. bosnicus collected at the spring of the Bosna River situated in Sarajevo. Larvae were collected by handpicking and adults with an entomological net. Collected specimens were stored in containers with 80 and 96% EtOH, for morphological and molecular analysis, respectively. All collected specimens are deposited in the Faculty of Science in Zagreb, Croatian Natural History Museum in Zagreb and the Institute of Hydrobiology and Aquatic Ecology Management in Vienna (Austria). Larval morphological features were analysed according to Wiggins (1996) and Kučinić et al. (2010, 2011a, 2011b). Systematic presentation follows Morse (2015). We use Drusus adustus McLachan 1867 as a valid name (syn. Drusus destitutus Kolenati 1848). In this paper, we include species Leptodrusus budtzi (Ulmer 1913), but it is possible that this speceis does not belong to Drusinae (J. Waringer, personal communication, 2015).

DNA extraction and PCR amplification

One adult male and two larvae of D. bosnicus from the spring of the Paljanska Miljacka River were genetically analysed in order to support the association of the larvae with the adults. Additionally we included two adult males from the spring of the Bosna River. Association was based on 541-bp-long fragment of the mitochondrial cytochrome oxidase I (mtCOI) gene and sequences were taken from Kučinić et al. (2010), Previšić et al. (2009) and Previšić et al. (2014b). Intraspecific p-distances were calculated in Mega 4.0.1 (Tamura et al. 2007).

Electronic microscopy, macrophotography and measuring

Morphological observations of samples were accomplished using a Tescan TS 5136 variable pressure scanning electron microscope (SEM). Samples were mounted with graphitic adhesive tape on the SEM stub and coated with carbon. The samples were examined by SEM operating in secondary electron (SE), or back-scattered (BSE) mode at an accelerating voltage of 20 kV, running current of 110 pA and variable pressure of 30 Pa to 5×10−1 Pa, sometimes pressure was increased to 10 Pa to eliminate sample charging.

Macrophotographing and measurements of larvae and larval cases were accomplished using a Leica Wild MZ8 stereomicroscope and Olympus SP-500 UZ digital camera, processed with computer programme Olympus Quick Photo Camera 2.2. In larvae of D. bosnicus the following features were measured: head width, total body length, length of the anterior-median metadorsal sclerites, their width in the widest median part and distance between them, and also the length of the posterior metadorsal sclerites (N=10). The following characters of cases were measured: total length, width of the anterior part, and width of the posterior part.

Description of fifth instar larva of Drusus bosnicus

Case and Larva

Case constructed completely of mineral particles (Fig. 4), slightly curving, total length 9.50–13.60 mm, width of anterior part 2.92–3.76 mm, width of posterior part 1.66–2.62 mm (N=10). Overall body shape eruciform (Fig. 5), total length without case 8.50–13.34 mm (N=10).

FIGURES 4–10.

FIGURES 4–10

Open in a new tab

Drusus bosnicus Klapálek 1898. 4, case, right lateral; 5, larva, left lateral; 6 head, pronotum and mesonotum, right lateral; 7, head and pronotum, right lateral; 8 head, right lateral; 9, head, frontal; 10, left mandible, ventral.

Head

Head capsule hypognathous, with width 1.57–1.77 mm (N=10) (Figs 5–8). In lateral view, posterior part of head capsule (vertex) flat with slight median concavity (Figs 5–8). Head brown, dorsally darker and laterally lighter, with granular surface sculpturing (Fig. 9). Genae of parietals reddish-brown to yellowish with lighter ring around each eye (Fig. 5). Dorsum of head capsule with dark muscle attachment spots (Fig. 9). Distinct area with small number of spinules (small spines) positioned laterally on each side of head capsule in areas between setae 13 and 16, but some specimens without visible spinules. Frontoclypeal apotome bell-shaped with narrow central region (Fig. 9). Antennae short, brown to dark brown, each positioned on small, noticeable prominences. Labrum symmetrical, brown posteriorly to yellowish anteriorly (Fig. 9), with setal brush at anterolateral margins (Fig. 9) and thin primary setae on dorsal surface. Mandibles black, distally reddish (Fig. 9); typical for grazers, mesal margin of each mandible with setal brush (Fig. 10); two setae present laterobasally on each mandible (Fig. 10). Labium and maxillae light-brown (yellowish). Maxillary palps 5-segmented.

Thorax

Pronotum dark brown to black (Fig. 5) with granular sculptured surface. Posterior margin rounded, both posterior and lateral margins thick and darkly sclerotized. Anterior part (50–60%) of pronotum slightly concave and rising, posterior part with prominent median hump (Figs. 5, 7–8). Pronotum bearing dark setae, especially laterally and on anterior margin, some of them long and conspicuous (Figs. 5–8). Dorsal (posterior part) and lateral regions of pronotum with white recumbent setae (Fig. 8); in some specimens, pronotum with small number of white recumbent setae. Prosternal horn present.

Mesonotal sclerites brown, lighter than pronotum, with dark setae and uneven rugous surface (Figs. 5–6, 11). Posterior and lateral margins thick and darkly sclerotized (Fig. 11).

FIGURES 11–18.

FIGURES 11–18

Open in a new tab

Drusus bosnicus Klapálek 1898. 11, thorax (pronotum, mesonotum and metanotum), dorsal; 12, left foreleg, posterior 13, left midleg, posterior; 14, left hind leg, posterior; 15, abdominal gill diagram: position of filaments on left side of abdominal segments I-VIII, with ● = gill present; ; 16, abdomen with gills, right lateral; 17, abdominal segment IX, dorsal; 18, left anal proleg, left lateral.

Metanotum with 3 pairs of dorsal sclerites (Fig. 11). Anteromedian (sa1) sclerites elongated, triangular with rounded apices, inter-sclerite distance less than width of either sclerite (Fig. 11), covered by setae, mainly anteriorly, color similar to mesonotum. Length of anteriomedian sclerites 0.51–0.65 mm (mean 0.59 mm); width of anteriomedian sclerites 0.26–0.34 mm (mean 0.30 mm); distance between anteromedian sclerites 0.07–014 mm (mean 0.10 mm). Posteromedian (sa2) sclerites smaller and lighter than sa1 sclerites (Fig. 11), triangularly or irregularly ellipsoid and with many setae. Length of posteromedian sclerites 0.32–0.51 mm (mean 0.45 mm). Group of setae present on membranes between sa2 sclerites and between sa2 and sa3 sclerites. Lateral (sa3) sclerites longitudinally prolonged, sickle-shaped, lighter brown with dark median region, and group of setae anteriorly.

Legs yellow-brown to dark brown or black, with dark ventral and dorsal margins (Figs. 5, 12–14). Coxae and femora of all legs with dark setae on both dorsal and ventral edges (Figs. 12–14). Trochanters of all legs without setae on dorsal margins (Figs. 12–14). Ventral margin on distal part of each foreleg trochanter with row of fine, yellowish setae (trochanteral brush). Midleg trochanters with few, fine, yellowish setae apicoventrally. Foreleg coxae and femora wide compared to those of mid- and hind legs (Figs. 12–14). Additional setae present on anterior and posterior faces of all femora. Mid- and hind legs similar in shape and size (Figs. 13–14), with slender coxae, trochanters, and femora. Setae on dorsal edges of tibiae present only distally in all legs (Figs. 13–14). Tarsi each with claw and basal seta, and tibial spurs light brown, almost yellowish (Figs. 12–14).

Abdomen

Abdominal segment I with well-developed dorsal (Fig. 11) and lateral humps (protuberances). Numerous setae present anterior and lateral to dorsal hump. Distinction between dorsal setal areas sa1 and sa2 not possible (Fig. 11). Ventrally with numerous setae, some of them with small sclerites at bases.

Single filamentous gills present on segments II–VII (Figs. 15–16). Dorsal pre-segmental gills present on segments II–VII; dorsal post-segmental gills present on segments II–VI, ventral pre- and post-segmental gills present on segments II–VII (Fig. 15). Lateral pre- and post-segmental gills present on segments II–IV (Fig. 16). On abdominal segment VIII, four dorsal setae present. Lateral fringe extending from last third of segment II to segment VIII (Fig. 16); in some specimens, only few setae forming lateral fringe on segment II or setae not visible.

Segment IX bearing irregular, semicircular, light brown dorsal sclerite, generally with 8 long, dark setae on posterior margin and several shorter, lighter setae on posterior half of sclerite (Fig. 17). Anal prolegs typical of limnephilids (Fig. 18), each with longitudinally prolonged lateral sclerite, sickle-shaped, yellowish, with setae mainly in posterior part and 2 large, dark setae at posterior end (Fig. 18). Anal claws and accessory hook brown to dark brown (Fig. 18).

Discussion

Association of Drusus bosnicus larvae and adults

COI haplotypes of adult male and larvae from the spring of the Paljanska Miljacka River were either completely identical or differed in one nucleotide position (Table 1). Overall, intraspecific variability recorded in D. bosnicus (Table 1) is in line with the observed variability of the same COI fragment in populations of some other Drusus species (e.g., Pauls et al. 2009; Previšić et al. 2009), including the D. bosnicus Group (e.g., Kučinić et al. 2008). However, the association of larvae and adults are not completely reliable based solely on comparisons of sequences of a single gene from one specimen each (e.g., Zhou et al. 2007). In addition to the molecular genetic data, association of adults and larvae of D. bosnicus are further supported by:

  1. Species distribution data on the Drusus bosnicus Group in Bosnia and Herzegovina, in which all species have restricted ranges and generally show allopatric distribution (Marinković-Gospodnetić 1979, Kučinić et al. 2008, 2011a, 2011b; Previšić et al. 2009),

  2. Presence of D. bosnicus as exclusive Drusus species in the Paljanska Miljacka River spring (Marinković-Gospodnetić 1979).

Table 1.

Intraspecific uncorrected pairwise distances (p) shown as percents and number of nucleotide differences (in brackets) of the mitochondrial cytochrome oxidase I (mtCOI) gene recorded in D. bosnicus. Abbreviations are used to denote life stages; IM(M) = adult male, L = larva.

Sampling site Specimen code Stage DbsIM1 DbsIBIM2 DbsVMIM1 DbsVML1 DbsVML2 GenBank accession nos
Bosna spring DbsIM1 IM(M) FJ002689
Bosna spring DbsIBIM2 IM(M) 0.2% (1) KC881518
Paljanska Miljacka spring DbsVMIM1 IM(M) 0.0% (0) 0.2% (1) GQ470609
Paljanska Miljacka spring DbsVML1 L 0.0% (0) 0.2% (1) 0.0% (0) GQ470610
Paljanska Miljacka spring DbsVML2 L 0.2% (1) 0.4% (2) 0.2% (1) 0.2% (1) GQ470611
Open in a new tab

Morphological separation of Drusus bosnicus larvae from other European Trichoptera larvae

In Europe, larvae of numerous different species of Trichoptera have been described (e.g., Urbanič et al. 2003a, 2003b; Graf et al. 2011; Sáinz-Bariáin & Zamora-Muñoz 2012; Waringer et al. 2012a, 2012b) including larvae of species in the genus Drusus (e.g., Lepneva 1966; Decamps & Pujol 1975; Szczesny 1978; Waringer 1987; Wallace et al. 1990; Waringer & Graf 1997; Waringer et al. 2000, 2007a, 2007b, 2011; Graf et al. 2005, 2009; Kučinić et al. 2008). The larvae of the subfamily Drusinae share common morphological features such as:

  • -

    a fully sclerotised pronotum and mesonotum;

  • -

    metanotum with six sclerites;

  • -

    additional setae present on anterior and posterior faces of mid- and hind leg femora;

  • -

    gills with one filament;

  • -

    slightly curved case, etc.

Distinctive features of D. bosnicus larvae are the specific shape of the head, pronotum, and anteromedian sclerites, enabling separation from other known larvae of European Trichoptera. Also, larvae of D. bosnicus differ from other larvae of the Drusus bosnicus Group in the shape of the head, except for D. ramae larvae. Drusus bosnicus and D. ramae exibit similar head shapes in lateral view, but differ in pronotal shape (Figs. 19–21). Larvae of D. ramae have two very prominent and widely separated humps posteriorly on the pronotum (Figs. 20–21), whereas the pronotum in D. bosnicus larvae has a ridge in this position (Figs. 6–7, 19).

FIGURES 19–21.

FIGURES 19–21

Open in a new tab

Pronotum. 19, Drusus bosnicus Klapálek 1898, right lateral; 20–21, Drusus ramae Marinković-Gospodnetić 1971a: 20, right lateral; 21, right dorsolateral.

The following features clearly distinguish larvae of D. bosnicus from other described Drusinae larave (Lepneva 1966; Hickin 1967; Decamps & Pujol 1975; Szczesny 1978; Sedlák 1980; Waringer 1987; Wallace et al. 1990; Pitsch 1993; Urbanič et al. 2003c; Graf et al. 2005, 2009; Waringer & Graf 1997; Waringer et al. 2000, 2007a, 2007b, 2008a, 2008b, 2010, 2013a, 2013b, 2015; Vieira-Lanero et al. 2005; Kučinić et al. 2008, 2010, 2011a, 2011b; Previšić et al. 2014a):

Anomalopterygella chauviniana (Stein 1874), D. bolivari (McLachlan 1880) and D. brunneus Klapálek 1898, have a different shape of the posterior part of the pronotum than the larva of D. bosnicus. These species have a very pronounced mid-dorsal concavity in the dorsal hump which is lacking in D. bosnicus.

- Cryptothrix nebulicola McLachlan 1867, D. alpinus (Meyer-Dür 1875), D. chrysotus (Rambur 1842), D. discolor, D. franzi Schmid 1956, D. muelleri McLachlan 1868, and D. romanicus Murgoci & Botosaneanu 1954 have teeth along the mesal margin of each mandible which are lacking in D. bosnicus.

- In Drusus adustus, D. alpinus, Drusus annulatus (Stephens 1837), D. biguttatus, D. camerinus Moretti 1981, D. balcanicus Kumanski 1973, D. croaticus Marinković-Gospodnetić 1971b, D. franzressli Malicky 1974 (in Malicky & Kumanski 1974), Drusus franzi, D. improvisus McLachlan 1884, D. klapaleki, D. medianus, D. mixtus (Pictet 1834), Drusus monticola McLachlan 1876, D. nigrescens Meyer-Dür 1875, D. rectus McLachlan 1868, D. septentrionis, D. trifidus McLachlan 1868, D. vinconi Sipahiler 1992, and Ecclisopteryx malickyi Moretti 1991 the head vertex is evenly rounded. In D. bosnicus this part of the head is flat with a slight median concavity.

- Drusus alpinus, D. aprutiensis Moretti 1981, D. camerinus Moretti 1981, D. croaticus, D. franzi Schmid 1956, and D. mixtus lack prominent, long median setae dorsally on the anterior border of the pronotum; D. bosnicus larvae have long, median setae in this part of the pronotum.

- Drusus biguttatus, D. croaticus, D. ingridae Sipahiler 1993, D. vinconi Sipahiler 1992, and Hadimina torosensis Sipahiler 2002 have an evenly rounded pronotum in lateral view. The pronotum of D. bosnicus, in lateral view, has a prominent median hump.

- Drusus botosaneanui, Drusus tenellus, Drusus schmidi Botosaneanu 1960, Ecclisopteryx dalecarlica Kolenati 1848, E. guttulata (Pictet 1834), E. ivkae Previšić, Vitecek & Graf 2014, E. keroveci Previšić, Vitecek & Graf 2014, and E. madida (McLachlan 1867) have prominent spines on the head and/or pronotum; D. bosnicus lacks these prominent spines on the head and pronotum.

- Drusus discolor and D. romanicus have hair-like structures on the head and pronotum; these structures are absent in D. bosnicus.

- Drusus carpathicus Dziedzielewicz 1911 lacks dorsal gills on the abdomen; D. bosnicus has such gills.

- In Drusus adustus and D. melanchaetes McLachlan 1876, setae along the whole length on the dorsal side of mid- and hind-leg tibiae are present; in D. bosnicus such setae are present only distally.

- Drusus franzressli, D. spelaeus (Ulmer 1920), Metanoea rhaetica Schmid 1956 and M. flavipennis (Pictet 1834) have a large median sclerotized patch on abdominal sternum I which is lacking in D. bosnicus.

- Drusus radovanovici has numerous thin, long, yellow (yellowish) setae on the dorsal and lateral parts of the pronotum. Such long setae are lacking in D. bosnicus.

- In Drusus serbicus Marinković-Gospodneti 1971b, the dorsal profile of the pronotum in lateral view has an annular crest that is highest at its dorsal centre and gradually declining laterally. This crest is lacking in D. bosnicus.

- Drusus trifidus has numerous light spines on the pronotum which are lacking in D. bosnicus.

- Ecclisopteryx asterix Malicky 1979 has ovoidal metanotal anteromedian sclerites (metanotal sa1 sclerites) which are more triangular in D. bosnicus.

- Leptodrusus budtzi has a rounded pronotum in lateral view with a clear ridge in its anterior part. The pronotum of D. bosnicus does not have this shape and lacks a ridge.

Distribution, protection status, and feeding ecology of Drusus bosnicus

According to literature data (Marinković-Gospodnetić 1979) Drusus bosnicus was found in central Bosnia and Herzegovina at three localities: the Bosna River spring, the Paljanska River spring, and the Mokračka Miljacka River spring. The distance between springs of the Paljanska and Mokračka Miljancka Rivers is 21 kilometres, and the distance between these springs and the spring of the Bosna River is about 34 kilometres. This species thus occupies the smallest area known in the Drusus bosnicus Group, except for D. ramae (Kučinić et al. 2010).

In our investigation of caddisflies in Bosnia and Herzegovina, we found D. bosnicus in all three localities listed in literature (Marinković-Gospodnetić 1979), but not elsewhere (Stanić-Koštroman 2009). Considering the locations of these springs, i.e. the spring of the River Bosna is situated in Sarajevo and two other springs are located near villages, it is very important to protect them. A spring of the Paljanska Miljacka River is used as a source for drinking water, but the habitat was not considerably disturbed, so aquatic fauna is preserved, including the population of D. bosnicus (Kučinić et al. 2010). The other two springs are natural, at the moment without visible negative anthropogenic influence.

According to morphological features of mandibles, D. bosnicus belongs to the group of grazers, like larvae of the other species that form the Drusus bosnicus Group from the Balkan Peninsula (Kučinić et al. 2008, 2010, 2011a, 2011b). Larvae of these species are feeding mainly on epilithic algae in the periphyton of mosses, cobbles, pebbles and gravel. This consistent feeding ecology of all species from the Drusus bosnicus Group in Bosnia and Herzegovina is possibly a result of the monophyletic origin of the species (Marinković-Gospodnetić 1976; Kučinić et al. 2011a). The taxa of the Drusus bosnicus Group were separated in different periods during the Pleistocene, probably from one ancestral species (Marinković-Gospodnetić 1976; Previšić et al. 2009; Kučinić et al. 2011a, 2014). Recent molecular study showed that two different species from the Drusus bosnicus Group inhabit the spring of the Bosna River (Kučinić et al. 2014; Previšić et al., 2014b). This is possibly an indication of a more complex distribution pattern and evolutionary history of the Drusus bosnicus Group than previously recognised (e.g., Kučinić et al. 2011a, 2014). So far, we have not found adults or last instar larvae of this possibly new species in this spring.

Acknowledgements

We are very grateful to Milivoj Franjević, University of Zagreb, Faculty of Forestry, for his help with macrophotography; Ivana Maguire, University of Zagreb, Faculty of Science and Ana Mrnjavčić Vojvoda, Croatian Centre for Agriculture, Food and Rural Affairs, for technical help. This research was supported by the Austrian Science Fund (FWF) as a part of the Project P 23687-B17, and Croatian Ministry of Science, Education and Sports as a part of the Projects No. 119–1193080–1206 and No 119-1193080-3076.

References

  1. Bedek J, Gottstein-Matočec S, Jalžić B, Ozimec R, Štamol V. Katalog tipskih lokaliteta faune Hrvatske, Catalogue of cave type localities of Croatian fauna. Natura Croatica. 2006;18(Suppl. 1):1–154. [Google Scholar]
  2. Bilandžija H, Brian M, Podnar M, Ćetković H. Evolutionary history of relict Congeria (Bivalvia: Dreissenidae): Unearthing the subterranean biodiversity of the Dinaric Karst. Frontiers in Zoology. 2013;10:5. doi: 10.1186/1742-9994-10-5. http://dx.doi.org/10.1186/1742-9994-10-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Botosaneanu L. Trichoptères de Yougoslavie recueillis en 1955 par le Dr. F. Schmid. Deutsche Entomologische Zeitschrift. 1960;7(3):261–293. N. Ser. [Google Scholar]
  4. Decamps H, Pujol JY. Les larves de Drusinae des Pyrenees (Trichopteres, Limnephilidae) Annales de Limnologie. 1975;11:157–167. [Google Scholar]
  5. Dziedielewicz Nova species ex ordine trichopterorum in Karpathibus orientalibus anno 1909 collectae. Kosmos Lwów [Lemberg] 1911;36:206–209. [Google Scholar]
  6. Džukić G, Kalezić M. The biodiversity of amphibians and reptiles in the Balkan Peninsula. In: Griffiths HI, Kryštufek B, Reed JM, editors. Balkan Biodiversity, Pattern and Process in the European Hotspot. Kluwer Academic Publisher; Dordrecht, The Netherlands: 2004. pp. 167–192. [Google Scholar]
  7. Gottstein-Matočec S, Bakran-Petricoli T, Bedek J, Bukovec D, Buzjak S, Franičević M, Jalžić B, Kerovec M, Kletečki E, Kovačić M, Kralj J, Kružić P, Kučinić M, Kuhta M, Matočec N, Ozimec R, Rađa T, Štamol V, Ternjej I, Trvtković N. An overview of the cave and interstitial biota of Croatia. Natura Croatica. 2002;11(Suppl. 1):1–112. [Google Scholar]
  8. Graf W, Lubini V, Pauls SU. Larval description of Drusus muelleri McLachlan, 1868 (Trichoptera: Limnephilidae) with some notes on its ecology and systematic position within the genus Drusus. Annales de Limnologie. 2005;41:93–98. [Google Scholar]
  9. Graf W, Waringer J, Pauls SU. A new feeding group within larval Drusinae (Trichoptera: Limnephilidae): The Drusus alpinus Group sensu Schmid, 1956, including larval description of Drusus franzi Schmid, 1965, and D. alpinus (Meyer-Dür, 1875) Zootaxa. 2009;2031:53–62. [PMC free article] [PubMed] [Google Scholar]
  10. Graf W, Kučinić M, Previšić A, Pauls SU, Waringer J. The larva of Ecclisopteryx malickyi Moretti, 1991 (Trichoptera: Limnephilidae: Drusinae), with comments on the genus. Zoosymposia. 2011;5:36–142. doi: 10.11646/zoosymposia.5.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hickin NE. Caddis Larvae, Larvae of British Trichoptera. Hutchinson & Co.; London, United Kingdom: 1967. p. 476. [Google Scholar]
  12. Klapálek F. Fünf neue Trichopteren-Arten aus Ungarn. Természetrajzi Füzetek. 1898;21:488–490. [Google Scholar]
  13. Klapálek F. Preelozu k Poznovanu Faune Trichoptera ee Neuroptera Bosne ee Hercegovine. Glasnik Zemaljskog Muzeja u Bosne ee Hercegovine. 1899;11:323–338. 1 pl. [Google Scholar]
  14. Kolenati FA. Genera et Species Trichopterorum. Pars prior Heteropalpoidea. Kronberger, Prague, Czech Republic. 1848;6:1–108. 3 pls. [Google Scholar]; Also ; Abhandlungen der Königlichen Böhmischen Gesellschaft der Wissenschaften. 6:1–108. [Google Scholar]
  15. Krušnik C. Trichoptera. Fauna Durmitora. 1987;2:201–224. [Google Scholar]
  16. Kryštufek B. A quantitative assessment of Balkan mammal diversity. In: Griffiths HI, Kryštufek B, Reed JM, editors. Balkan Biodiversity, Pattern and Process in the European Hotspot. Kluwer Academic Publisher; Dordrecht, The Netherlands: 2004. pp. 78–108. [Google Scholar]
  17. Kučinić M, Previšić A, Gottstein-Matočec S, Hrašovec B, Stanić-Koštroman S, Pernek M, Delić A. Description of the larvae of Drusus radovanovici septentrionis Marinković-Gospodnetić, 1976 and Drusus croaticus Marinković-Gospodnetić, 1971 (Trichoptera: Limnephilidae) from Bosnia and Herzegovina, and Croatia. Zootaxa. 2008;1783:1–17. [Google Scholar]
  18. Kučinić M, Previšić A, Stanić-Koštroman S, Franjević M, Šerić Jelaska L, Delić A, Posilović H. Description of the larvae of Drusus ramae Marinković-Gospodnetić, 1971 and Drusus medianus Marinković-Gospodnetić, 1976 (Trichoptera: Limnephilidae) with some genetic data, distribution, ecological, faunal and conservation notes. Zootaxa. 2010;2484:1–24. [Google Scholar]
  19. Kučinić M, Previšić A, Graf W, Šerić Jelaska L, Stanić-Koštroman S, Waringer J. Larval description, genetic and ecological features of Drusus radovanovici radovanovici Marinković-Gospodnetić, 1971 (Trichoptera: Limnephilidae: Drusinae) with some phylogenetic and taxonomic data on the bosnicus group in the Balkan Peninsula. Deutsche Entomologische Zeitschrift. 2011a;58:135–153. [Google Scholar]
  20. Kučinić M, Previšić A, Stanić-Koštroman S, Graf W, Franjević M, Posilović H, Waringer J. Morphological and ecological features of Drusus larvae from the bosnicus group on the Balkan Peninsula with description of the larva of Drusus klapaleki Marinković-Gospodnetić, 1976. Zoosymposia. 2011b;5:244–254. [Google Scholar]
  21. Kučinić M, Delić A, Ćuk R, Previšić A, Mihoci I, Žganec K, Cerjanec D, Vučković I. The first finding of Drusus bosnicus Group (Insecta, Trichoptera, Limnepohilidae) in Croatia with some notes on diversity, distribution and ecology of genus Drusus ina Croatia and in Dinaric karst of the Balkan Peninsula. Natura Croatia. 2014;23:265–377. [Google Scholar]
  22. Kumanski KP. Zwei neue Köcherfliegen aus Bulgarien (Trichoptera, Limnephilidae) Entomologische Berichten, Amsterdam. 1968;28:214–218. [Google Scholar]
  23. Kumanski KP. Die Unterfamilie Drusinae (Trichoptera) in Bulgarien. Tijdschrift voor Entomologie. 1973;116(6):107–121. [Google Scholar]
  24. Kumanski KP. Trichoptera, Integripalpia. In: Josifov M, editor. Fauna Bulgarica. Vol. 19. Bulgarska Akademi na Naukite; Sofia, Bulgaria: 1988. p. 354. [Google Scholar]
  25. Kumanski KP, Malicky H. A survey of the genus Potamophylax Wallengren 1891 in the Balkan Peninsula, with description of two new species (Trichoptera: Limnephilidae) Braueria. 1999;26:27–30. [Google Scholar]
  26. Lepneva SG. Ličinki i kukolki podotryada tsel’noshchupikovykh (Integripalpia) In: Strelkov AA, editor. Fauna SSSR. Trichoptera, Rucheiniki, Vol. II, No 2 (In Russian) Zoologičeski Institut Akademii Nauk SSSR; Moskva, Russia: 1966. p. 560. [Google Scholar]
  27. Malicky H, Kumanski K. Neun neue Köcherfliegen aus Südeuropa (Trichoptera) Entomologische Zeitschrift mit Insektenbörse. 1974;84:9–20. [Google Scholar]
  28. Malicky H. Notes on some caddisflies (Trichoptera) from Europe and Iran. Aquatic Insects. 1979;1:3–16. [Google Scholar]; Malicky H. Atlas of European Trichoptera. Springer; Dordrecht, Germany: 2004. p. 359. [Google Scholar]
  29. Malicky H. Die Köcherfliegen Griechenlands. Denisia. 2005;17:1–240. [Google Scholar]
  30. Marinković-Gospodnetić M. New species of Trichoptera from Bosnia and Hercegovina. Bulletin Scientifique, Conseil Academies des Sciences et des Arts de la RSF de Yougoslavie, Section A: Sciences Naturelles, Techniques et Medicales. 1971a;16:144–145. [Google Scholar]
  31. Marinković-Gospodnetić M. The species of the genus Drusus in Yugoslavia. Godisnjak Bioloskog Instituta Univerziteta u Sarajevu. 1971b;24:105–109. [Google Scholar]; Marinković-Gospodnetić M. The differentiation of Drusus species of the group bosnicus. In: Malicky H, editor. Proceedings of the First International Symposium on Trichoptera; The Hague, The Netherlands: Dr. W. Junk Publishers; 1976. pp. 77–85. [Google Scholar]
  32. Marinković-Gospodnetić M. Trichoptera (Insecta) velikih karstnih izvora u Dinaridima. In: Rauš Đ, editor. Drugi kongres Ekologa Jugoslavije (Second Congress of Ecologists of Yugoslavia) Savez društava ekologa Jugoslavije; Zagreb, Croatia: 1979. pp. 1837–1849. [Google Scholar]
  33. McLachlan R. Bemerkungen über Europäische Phryganiden, nebst beschreibungen einiger neuer genera und species. Stettiner Entomologische Zeitung. 1867;28:50–63. [Google Scholar]
  34. McLachlan R. Contributions to a knowledge of European Trichoptera. Transactions of the Royal Entomological Society of London. 1868;1868:289–308. plate 14. [Google Scholar]
  35. McLachlan R. A Monographic Revision and Synopsis of the Trichoptera of the European Fauna, Part 4. John van Voorst; London: 1876. pp. 145–220. plates XVI–XXIII. [Google Scholar]
  36. McLachlan R. A Monographic Revision and Synopsis of the Trichoptera of the European Fauna, Supplement Part 2. John van Voorst; London: 1880. pp. xiii–lxxxiv. pls. LII–LIX. [Google Scholar]
  37. McLachlan R. A Monographic Revision and Synopsis of the Trichoptera of the European Fauna, First Additional Supplement. John van Voorst; London: 1884. pp. i–iv.pp. 1–76. pls. I–VII. [Google Scholar]
  38. Meyer-Dür Die Neuropteren-fauna der Schweiz. Mitteilungen der Schweizerischen Entomologischen Gesellschaft. 1875;7:353–436. [Google Scholar]
  39. Moretti GP. New Trichoptera species and subspecies found in Italy. In: Moretti GP, editor. Proceedings of the 3rd International Symposium on Trichoptera; The Hague, The Netherlands: Dr. W. Junk; 1981. pp. 165–192. [Google Scholar]
  40. Moretti GP. Nouvelles espèces et sous-espèces de Trichoptères Italiens et examples de variabilitè des populations des Alpes Méridionales et des Apennins. In: Tomaszewski C, editor. Proceedings of the 6th International Symposium on Trichoptera; Poznan, Poland: Adam Mickiewicz University Press; 1991. pp. 385–402. [Google Scholar]
  41. Morse JC, editor. [accessed 19 March 2015];Trichoptera World Checklist. 2015 Available from http://entweb.clemson.edu/database/trichopt/index.htm.
  42. Murgoci A, Botosaneanu L. Contribuţii la studiul genului Drusus Steph. (Trichoptera) R.P.R. Buletin Ştiinţific Secţiunea de Ştiinţe Biologice, Agronomice, Geologice şi Geografice. 1954;6(3):967–979. [Google Scholar]
  43. Oláh J. New species and new records of Palearctic Trichoptera in the material of the Hungarian Natural History Museum. Annales Historico-Naturales Musei Nationalis Hungarici. 2010;102:65–117. [Google Scholar]
  44. Oláh J. New species and records of Balkan Trichoptera. Folia Historico Naturalia Musei Matraensis. 2011;35:111–121. [Google Scholar]
  45. Oláh J, Kovács T. New species and records of Balkan Trichoptera II. Folia Historico Naturalia Musei Matraensis. 2013;37:109–121. [Google Scholar]
  46. Pauls SU, Theissinger K, Ujvarosi L, Balint M, Hasse P. Patterns of population structure in two closely related, partially sympatric caddisflies in Eastern Europe: Historic introgression, limited dispersal, and cryptic diversity. Journal of the North American Benthological Society. 2009;28:517–536. [Google Scholar]
  47. Pictet FJ. Recherches pour Servir à l'Histoire et l'Anatomie des Phryganides. A. Cherbuliez; Geneva, Switzerland: 1834. [Google Scholar]
  48. Pitsch T. Larvaltaxonomie, Faunistik, und Ökologie mitteleuropäischer Fließwasser-Köcherfliegen (Insecta: Trichoptera) Technische Universität; Berlin, Germany: 1993. p. 316. ( Landschaftsentwicklung und Umweltforschung-Schriftenreihe des Fachbereichs Landschaftsentwicklung-Sonderheft S8 ). [Google Scholar]
  49. Previšić A, Walton C, Kučinić M, Mitrikeski PT, Kerovec M. Pleistocene divergence of Dinaric Drusus endemics (Trichoptera, Limnephilidae) in multiple microrefugia within the Balkan Peninsula. Molecular Ecology. 2009;18:634–647. doi: 10.1111/j.1365-294X.2008.04046.x. [DOI] [PubMed] [Google Scholar]
  50. Previšić A, Graf W, Vitecek S, Kučinić M, Bálint M, Keresztes L, Pauls SU, Waringer J. Cryptic diversity of caddisflies in the Balkans: The curious case of Ecclisopteryx species (Trichoptera: Limnephilidae) Arthropod Systematics & Phylogeny. 2014a;72:309–329. [PMC free article] [PubMed] [Google Scholar]
  51. Previšić A, Schnitzler J, Kučinić M, Graf W, Ibrahimi H, Kerovec M, Pauls SU. Microscale vicariance and diversification of western Balkan caddisflies linked to karstification. Freshwater Science. 2014b;33:250–262. doi: 10.1086/674430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Radovanović M. Über zwei neue Trichopteren-Arten aus Mazedonien. Zoologische Anzeiger. 1942;140:183–190. [Google Scholar]
  53. Rambur JP. Histoire Naturelle des Insectes. Névroptères. (Suites à Buffon) Roret; Paris, France: 1842. [Google Scholar]
  54. Sáinz-Bariáin M, Zamora-Muñoz C. The larva and life history of Stenophylax nycterobius (McLachlan, 1875) (Trichoptera: Limnephilidae) in high mountain streams (Sierra Nevada, Spain) and key to the Iberian larvae of the genus. Zootaxa. 2012;3483:71–81. [Google Scholar]
  55. Schmid F. La sous-famille des Drusinae (Trichoptera, Limnephilidae) Memoires Institut Royal des Sciences Naturelles de Belgique, 2eme Series. 1956;55:1–92. [Google Scholar]
  56. Sedlák E. Rád Chrostici—Trichoptera. In: Razkošny R, editor. Klič vodnich larev hmyzu. Československa Akademie Ved; Praha, Czech Republic: 1980. pp. 163–225. [Google Scholar]
  57. Sipahiler F. Four new species of Drusinae from Spain and France. (Insecta, Trichoptera, Limnephilidae) Spixiana. 1992;15(3):285–291. [Google Scholar]
  58. Sipahiler F. A contribution to the knowledge of Trichoptera of France. (Insecta, Trichoptera) Entomofauna. 1993;14:65–80. [Google Scholar]
  59. Sipahiler F. Hadimina torosensis, new genus and new species of Drusinae from southern Turkey (Trichoptera: Limnephilidae) Nova Supplementa Entomologica (Proceedings of the 10th International Symposium on Trichoptera) 2002;15:239–248. [Google Scholar]
  60. Stanić-Koštroman S. Faunističke, ekološke i biogeografske značajke tulara (Insecta: Trichoptera) Bosne i Hercegovine. Sveučilište u Zagrebu; Croatia: 2009. p. 151. Doktorska disertacija (PhD-Thesis) [Google Scholar]
  61. Stein JPEF. Beitrag zur Kenntnis der Phryganiden des Altvaters und einiger Anderer. Stettiner Entomologische Zeitung. 1874;35(7–9):244–253. [Google Scholar]
  62. Stephens JF. Illustrations of British Entomology, or a Synopsis of Indigenous Insects, Containing Their Generic and Specific Descriptions, with an Account of Their Metamorphoses, Times of Appearance, Localities, Food and Economy, as Far as Practicable, with Coloured Figures (from Westwood) of the Rarer and More Interesting Species, Volume 6. London: 1836–1837. [Google Scholar]
  63. Szczesny B. Larvae of the subfamily Drusinae (Insecta: Trichoptera) from the Polish part of the Carpathian Mts. Acta Hydrobiologica. 1978;20:35–53. [Google Scholar]
  64. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution. 2007;24:1596–1599. doi: 10.1093/molbev/msm092. [DOI] [PubMed] [Google Scholar]
  65. Ulmer G. Potamorites budtzi , n. sp. Entomologiske Meddelelser. 1913;10:17–19. [Google Scholar]
  66. Ulmer G. Trichopteren und Ephemeropteren aus Höhlen. Deutsche Entomologische Zeitschrift. 1920;1920:303–309. [Google Scholar]
  67. Urbanič G, Waringer J, Graf W. The larva and distribution of Psychomyia klapaleki Malicky, 1995 (Trichoptera: Psychomyiidae) Lauterbornia. 2003a;46:135–140. [Google Scholar]
  68. Urbanič G, Waringer J, Rotar B. The larva and pupa of Ceraclea riparia (Albarda, 1874) (Trichoptera: Leptoceridae) Aquatic Insects. 2003b;25:259–267. [Google Scholar]
  69. Urbanič G, Waringer J, Graf W. The larva of Ecclisopteryx asterix Malicky, 1979 (Trichoptera: Limnephilidae: Drusinae) Lauterbornia. 2003c;46:125–135. [Google Scholar]
  70. Vieria-Lanero M, González MA, Cobo F. The larva of Drusus bolivari (McLachlan, 1880) (Trichoptera: Limnephilidae: Drusinae) Aquatic Insects. 2005;27:85–93. [Google Scholar]
  71. Wallace ID, Wallace B, Philipson GN. A key to the case-bearing caddis larvae of Britain and Ireland. Freshwater Biological Association; Amblesidae, United Kingdom: 1990. p. 237. [Google Scholar]
  72. Waringer J. The larva of Drusus chrysotus (Rambur, 1942) (Trichoptera: Limnephilidae) from an Austrian brook. Aquatic Insects. 1987;9:21–25. [Google Scholar]
  73. Waringer J, Graf W. Atlas der österreichischen Köcherfliegenlarven. Facultas Universitätsverlag; Wien, Austria: 1997. p. 286. [Google Scholar]
  74. Waringer J, Graf W, Maier K. The larva of Metanoea flavipennis Pictet, 1834 (Trichoptera: Limnephilidae: Drusinae) Aquatic Insects. 2000;22:66–70. [Google Scholar]
  75. Waringer J, Graf W, Pauls SU. Functional feeding ecology in Central European species of subfamily Drusinae (Insecta: Trichoptera) Lauterbornia. 2007a;61:3–8. [PMC free article] [PubMed] [Google Scholar]
  76. Waringer J, Graf W, Pauls S, Lubini V. The larva of Drusus nigrescens Meyer-Dür, 1875 (Trichoptera: Limnephilidae: Drusinae) with notes on its ecology, genetic differentiation and systematic position. Annales de Limnologie. 2007b;43:161–166. doi: 10.1051/limn:2007010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Waringer J, Graf W, Pauls S, Cianficconi F. The larvae of Drusus improvisus McLachlan, 1884, Drusus camerinus Moretti, 1981 and Drusus aprutiensis Moretti, 1981 (Trichoptera: Limnephilidae: Drusinae) Aquatic Insects. 2008a;30:269–279. doi: 10.1080/01650420802334046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Waringer J, Graf W, Pauls SU, Vicentini H, Lubini V. DNA based association and description of the larval stage of Drusus melanchaetes McLachlan, 1876 (Trichoptera: Limnephilidae: Drusinae) with notes on ecology and zoogeography. Limnologica. 2008b;38:34–42. doi: 10.1016/j.limno.2007.09.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Waringer J, Graf W, Pauls St.U., Previšić A, Kučinić M. A larval key to the Drusinae species of Austria, Germany, Switzerland and the dinaric western Balkan. Denisia. 2010;29:323–406. [PMC free article] [PubMed] [Google Scholar]
  80. Waringer J, Graf W, Pitsch T, Pauls SU, Previšić A, Kučinić M. Description of the larval stage of Drusus mixtus (Pictet, 1834) (Trichoptera: Limnephilidae: Drusinae) with notes on ecology and zoogeography. Limnologica. 2011;41:249–255. doi: 10.1016/j.limno.2010.10.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Waringer J, Graf W, Malicky H. The larvae of Allogamus antennatus (McLachlan, 1876), Allogamus mendax (McLachlan, 1876) and Allogamus pertuli Malicky, 1975 (Trichoptera: Limnephilidae) with notes on ecology and zoogeography. Zootaxa. 2012a;3351:27–38. [Google Scholar]
  82. Waringer J, Graf W, Malicky H. Description of the larvae of Anabolia lombarda Ris, 1897 and Limnephilus sericeus (Say, 1824), with additional notes on Limnephilus flavospinosus Stein, 1874 (Trichoptera: Limnephilidae) Aquatic Insects. 2012b;34:93–105. [Google Scholar]
  83. Waringer J, Graf W, Bálint M, Kučinić M, Pauls SU, Previšić A, Keresztes L, Vitecek S. The larva of Drusus vinconi Sipahiler, 1992 (Trichoptera, Limnephilidae, Drusinae) ZooKeys. 2013a;317:69–80. doi: 10.3897/zookeys.317.5749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Waringer J, Graf W, Bálint M, Kučinić M, Pauls SU, Previšić A, Keresztes L, Vitecek S. The larvae of Drusus franzressli Malicky 1974 and Drusus spelaeus (Ulmer 1920) (Trichoptera: Limnephilidae: Drusinae) with notes on ecology and zoogeography. Zootaxa. 2013b;3637:1–16. doi: 10.11646/zootaxa.3637.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Waringer J, Graf W, Bálint M, Kučinić M, Pauls SU, Previšić A, Keresztes L, Ibrahimi H, Živić I, Bjelanović K, Krpač V, Vitecek S. Larval morphology and phylogenetic position of Drusus balcanicus Kumanski, Drusus botosaneanui Kumanski, Drusus serbicus Marinković-Gospodnetić and Drusus tenellus (Klapálek) (Trichoptera: Limnephilidae: Drusinae) European Journal of Entomology. 2015 doi: 10.14411/eje.2015.037. Ahead of Print, 1802–8829. http://dx.doi.org/10.14411/eje.2015.037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Wiggins GB. Larvae of the North American Caddisfly Genera (Trichoptera) University of Toronto Press; Toronto, Canada: 1996. p. 457. Second Edition. [Google Scholar]
  87. Zhou X, Kjer MK, Morse JC. An introduction to the species delimitation, larval-adult association of Chinese Hydropsychidae using independent DNA sequences and adult morphology. In: Bueno-Soria J, Barba-Alvarez A, Armitage BJ, editors. Proceedings of the XIIth International Symposium of Trichoptera; Columbus, Ohio, United States of America: The Caddis Press; 2007. pp. 355–368. [Google Scholar]

RESOURCES