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Diptera, Chironomidae) from the Lukina Jama – Trojama Cave in Croatia

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Diptera, Chironomidae) from the Lukina Jama – Trojama Cave in Croatia RESEARCH ARTICLE Blind Flight? A New Troglobiotic Orthoclad (Diptera, Chironomidae) from the Lukina Jama – Trojama Cave in Croatia Trond Andersen1☯, Viktor Baranov2☯, Linn Katrine Hagenlund1☯*, Marija Ivković3, Gunnar Mikalsen Kvifte1,4, Martina Pavlek5,6 1 Department of Natural History, University Museum of Bergen, University of Bergen, Bergen, Norway, 2 Lebniz Institute for Freshwater Ecology and Inland Fisheries, Berlin, Germany, 3 Department of Zoology, Division of Biology, Faculty of Science, University of Zagreb, Zagreb, Croatia, 4 Department of Zoology, Institute of Biology, University of Kassel, Kassel, Germany, 5 Department of Molecular Biology, Ruđer Bošković Institute, Zagreb, Croatia, 6 Croatian Biospeleological Society, Zagreb, Croatia ☯ These authors contributed equally to this work. * [email protected] a11111 Abstract The genus Troglocladius Andersen, Baranov et Hagenlund, gen. n. is erected based on T. hajdi Andersen, Baranov et Hagenlund, sp. n. collected at 980 m depth in the Lukina jama —Trojama cave system in Croatia. Morphological features such as pale color, strongly OPEN ACCESS reduced eyes and very long legs make it a typical cave animal. Surprisingly, it has also Citation: Andersen T, Baranov V, Hagenlund LK, retained large wings and appears to be capable of flight which would make T. hajdi the first ć Ivkovi M, Kvifte GM, Pavlek M (2016) Blind Flight? A flying troglobiont worldwide, disproving previous beliefs that bats are the only animals capa- New Troglobiotic Orthoclad (Diptera, Chironomidae) from the Lukina Jama – Trojama Cave in Croatia. ble of flying in complete darkness. Morphologically the new species does not readily fit PLoS ONE 11(4): e0152884. doi:10.1371/journal. within any described genus, but shares characteristics with genera both in the tribes pone.0152884 “Metriocnemini” and “Orthocladiini”. Bayesian molecular phylogenetic analysis using the Editor: Donald James Colgan, Australian Museum, markers COI, 18S rDNAs, 28S rDNA, CADI, and CADIV groups it with the genera Tvetenia, AUSTRALIA Cardiocladius and Eukiefferiella in the tribe “Metriocnemini”. Troglocladius hajdi may be par- Received: August 31, 2015 thenogenetic, as only females were collected. The discovery confirms the position of the Accepted: March 20, 2016 Dinaric arch as a highly important hotspot of subterranean biodiversity. Published: April 27, 2016 Copyright: © 2016 Andersen et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are Introduction credited. Terrestrial species adapted to cave life are generally characterized as either troglophiles or tro- Data Availability Statement: All relevant data are globionts. While troglobionts are obligatory cave-dwellers, spending their entire life in the within the paper and its Supporting Information files. caves, troglophiles are essentially epigean species that are subdivided to eutroglophiles (able to Funding: The authors have no support or funding to maintain permanent subterranean populations) and subtroglophiles (dependent on epigean report. habitats for some biological functions). A third category of cave-dwelling organisms, the tro- Competing Interests: The authors have declared gloxenes, are only accidentally found in caves [1]. Out of more than 21,000 terrestrial cave taxa that no competing interests exist. worldwide [2] all troglobionts are ground dwellers. Bats fly in the complete darkness of caves PLOS ONE | DOI:10.1371/journal.pone.0152884 April 27, 2016 1/15 Blind Flight? A New Troglobiotic Othoclad from Croatia using echolocation for navigating, they are however, troglophilic, and there are no known fly- ing troglobionts. The Dinarides or Dinaric Alps stretch along the western part of the Balkan Peninsula in southern Europe and are a part of the Alpine system along the east coast of the Adriatic Sea. According to the most recent census, the Dinaric karst harbors 600 terrestrial and 330 aquatic troglobionts [3]. Comparison of this number to the 1138 obligate cave taxa in United States [4] reveals the Dinarides as the world’s richest area of obligate subterranean fauna when compared to other regions of approximately the same size [4]. The extreme richness of the area can also be portrayed via other fauna, including the world’s sole troglobiotic representatives of Porifera, Cnidaria, Bivalvia and Polychaeta [5]. Although hundreds of different Diptera species have been recorded from caves, it has been stated that Diptera contains few true cave species, most are occasional guests or at most troglo- philes (see e.g. [6, 7]). However, some Diptera have evolved morphological and physiological adaptations for a troglobiotic life [7]. These adaptations are possibly most pronounced in the African Mormotomyia hirsuta Austen, 1936 (Mormotomyiidae), which is associated with bats in caves and regarded as troglophilic as it sometimes is found outside of caves. It lacks eyes, wings and pigments and has developed elongate, spindly legs densely covered with sensory setae [8]. In the family Sphaeroceridae, several species and subspecies are found in caves and some of these, such as Crumomyia absoloni (Bezzi, 1914), which is found in caves in northeast- ern Herzegovina, are pale and have reduced eyes, long legs and short wings and halteres [9– 10]. Some of these adaptations are also found in other taxa including Allopnyxia patrizii Free- man, 1952 (Sciaridae) from caves in Italy, the obligate bat parasitic families Nycteribiidae and Strebliidae, and several species in the families Culicidae, Psychodidae, Mycetophilidae, Kero- platidae, Phoridae, and Heleomyzidae [7, 11]. Chironomidae (Diptera) have been recorded from caves in many parts of the world (e.g. [12–17]). Most of these records are from the first few hundred meters from the cave entrance and, if identified beyond family level, the species recorded appear mostly to be trogloxenes. Reeves [18] categorizes Zavrelimyia nr thryptica (Sublette, 1964) from caves in the Great Smoky Mountains, U.S.A., as a troglophile, but until now there seems to be no records of any true troglobionts among the chironomids. During expeditions to the Lukina jama—Trojama cave system in the Velebit Mountain Range in Croatia in 2013, several females of a pale chironomid belonging to the subfamily Orthocladiinae were collected in a chamber at 980 m below the surface. The female is described below and placed in a new genus based on morphological and molecular data. Fur- thermore, its habitat and natural history is outlined based on collection data and in situ observations. The Lukina Jama—Trojama cave system The Lukina jama—Trojama cave system is situated in the Hajdučki and Rožanski kukovi Strict Reserve, Velebit National Park, a 109 km2 park in the northern parts of the Velebit Mountain in Croatia. There are several deep caves in the park with some of the world's largest subterra- nean vertical drops. The Lukina jama—Trojama cave system is 1.431 m deep and thus the deepest cave in southeast Europe and the 14th deepest cave in the world. The cave system has two vertical entrances at 1.438 and 1.475 m above sea-level (Fig 1A) and in winter snow falls into the pits making an icy layer that covers the walls and extends approximately to a depth of 350 m in Lukina jama and 200 m in Trojama; some years, the Lukina jama entrance is completely sealed off by an ice cap. Air temperature gradually sinks and becomes more stable during the first 200 m of the cave system, as influence from the PLOS ONE | DOI:10.1371/journal.pone.0152884 April 27, 2016 2/15 Blind Flight? A New Troglobiotic Othoclad from Croatia Fig 1. A-C.–A. SE-NW profile of the Lukina jama—Trojama cave system in the Velebit Mountain, Croatia. Explored by Speleological Committee of the Croatian Mountaineering Association, Croatian Speleological Federation and Slovak Speleological Society; map prepared by Darko Bakšić. Positions of the 3 campsites (First, second and third camp) inside the pit are marked on the map.–B. The chamber at 980 m depth, where most of the specimens were caught.–C. Newly emerged specimen of Troglocladius hajdi Andersen, Baranov et Hagenlund, gen. n., sp. n., sitting on the cave wall (photo J. Bedek). doi:10.1371/journal.pone.0152884.g001 outside decreases (at -180 m it is around -0.7°C). From there, the temperature is very stable year round and slowly rises again to 2.5°C in the middle reaches (around Second Camp, Fig 1), in the chamber at 980 m depth it reaches 3.5°C, and at the bottom of the pit the temperature is around 4.9°C [19]. PLOS ONE | DOI:10.1371/journal.pone.0152884 April 27, 2016 3/15 Blind Flight? A New Troglobiotic Othoclad from Croatia The first 200 m of the cave system has substantial presence of ice and snow year round. Water and a strong draught of cold air constantly flow down the shaft. These conditions, along with the cold temperatures make this part of the cave system unsuitable for subterranean fauna. The new species has only been observed at depths between 800 and 980 m. Though it cannot completely be ruled out that the species is present in the upper parts of the Lukina jama—Tro- jama cave system, it is highly unlikely given the inhospitable conditions. The chamber at 980 m depth (Fig 1B—third camp) is about 85 x 70 meters in size and contains several habitats includ- ing dry walls, hygropetric environments with water seeping on the walls, small streams with sediment and a small pond with standing water—potential habitats for the immature stages. A total of 54 animal taxa have been recorded from the Lukina jama—Trojama cave system, of which 32 are true cave dwellers [20]. Among these, the cave system houses the endemic snail Zospeum tholussum Weigand, 2013 and one of the largest known colonies of the subterranean leech Croatobranchus mestrovi Kerovec, Kučinić et Jalžić, 1999 [21–22].
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