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A key to the freshwater triclads (Platyhelminthes, Tricladida) of Herzegovina watercourses

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The aim of this paper is to describe morphological characteristics of freshwater triclads in Herzegovina and to provide a key for their identification based mainly on their external morphology. Our research is based on the freshwater triclads
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  srcinal research article PERIODICUM BIOLOGORUM UDC 57:61 VOL. 117, No 3, 1–??, 2015 CODEN PDBIAD DOI: 10.18054/pb.2015.117.3.2951 ISSN 0031-5362  A key to the freshwater triclads (Platyhelminthes, Tricladida) of Herzegovina watercourses  Abstract  e aim of this paper is to describe morphological characteristics of fresh-water triclads in Herzegovina and to provide a key for their identification based mainly on their external morphology. Our research is based on the  freshwater triclads collected at 26 sites in Herzegovina, including 10 rivers, 6 springs and 1 lake.Triclads were collected by hand and with the bait jar with a lid bearing many small perforations. Specimens were identified immediately after being collected or we transported them to the laboratory in termal containers with ice. e morphological features used for species identification in this key are: body coloration (color of the dorsal and ventral side), the size of the pharynx, the presence of tentacles and their location, number and position of the eyes in respect to each other and the body margin, and the shape of the head. Specimens were fixed using Steinmann’s fluid and conserved in 70 % alco-hol. Inner morphological feature, shape of a penis, was used in determination of Polycelis tenuis and Polycelis nigra.We collected a total of 11 species, belonging to 8 genera (Polycelis Ehren-berg, 1831, Crenobia Kenk, 1930, Phagocata Leidy, 1847, Planaria Mül-ler, 1776, Dendrocoelum Örsted, 1844, Schmidtea Ball, 1974, Dugesia Girard, 1850, Girardia Ball, 1974) and 3 families.e present study forms a baseline for future studies on the diversity and biogeography of Herzegovinian freshwater triclads.  INTRODUCTION T he order Tricladida comprises the free-living flatworms. Within Tricladida, three infraorders have been recognized: Maricola (ma-rine triclads), Paludicola (freshwater triclads), and Terricola (land tri-clads) (1), to which a new one, the Cavernicola was further added (2). Study based on molecular properties (3) indicates that the Terricola and Paludicola should be replaced with a clade Continenticola. is new clade comprises the families Planariidae Stimpson, 1857, Dendrocoeli-dae Hallez, 1892, Kenkiidae Hyman, 1937, Dugesiidae Ball, 1974 and Geoplanidae Stimpson, 1857 (4). We based our research on freshwater triclads belonging to the families Planariidae, Dendrocoelidae and Du-gesiidae. Despite some intensive studies (5–9), phylogeny, taxonomy and dis-tribution of this group of organisms are still quite unknown and unex-plained. e fauna of freshwater triclads in Bosnia and Herzegovina is not sufficiently explored. e latest surveys were conducted in the 1920s LEJLA KNEZOVIĆ 1 MARKO MILIŠA 2 MIRJANA KALAFATIĆ 2 NIVES RAJEVIĆ 2 ADRIANA PLANINIĆ 1 1 Faculty of Science and EducationUniversity of Mostar, Matice hrvatske bb BiH-88000 Mostar 2 Faculty of Science, University of ZagrebRooseveltov trg 6, RH-10000 Zagreb Correspondence: Lejla Knezovi} Faculty of Science and Education University of Mostar, Matice hrvatske bb BiH-88000 Mostar e-mail: lejla.knezovic @ fpmoz.ba Key words:  planarians, free-living triclads, morphology, Balkans, Planariidae, Dendrocoelidae, Dugesiidae Received January 21, 2015. Revised April 3, 2015. Accepted October 23, 2015.  L. Knezović et al. A key to the freshwater triclads (Platyhelminthes, Tricladida) of Herzegovina watercourses 44 Period biol, Vol 117, No 3, 2015. and 1930s (10–12). Lanfranchi and Papi (13), Italian zo-ologists, wrote about fauna of freshwater turbelarians in Limnofauna europea  . However, they have not studied tri-clads, but they highlighted the fact that one could prob-ably found a large number of new species in unexplored areas (Iberian and Balkan Peninsula). Dahm and Gur-bault (14) reported 122 species of triclads in Europe and 42 of them were reported in the Balkans. It is significant that, as they said, the richest region is Southeast Europe, in particular the Balkan Peninsula, and southwestern re-gions of Europe. De Beauchamp (10) reported triclads in rivers Buna ( Neodendrocoelum nausicae  , Schmidt, Polyce-lis felina  , Dalyell i Crenobia montenigrina  , Mrezak),  Jasenica ( C. montenigrina  , Mrezak) and Radobolja ( C. montenigrina  , Mrezak). Fauna of the karst regions such as western Balkan Peninsula represents one of the most interesting in Europe (15). So far no keys for freshwater triclads were published in this region and the aim of this paper is to remedy this. SAMPLING SITES AND METHODS  Altogether, 26 sites in Herzegovina were sampled, en-compassing sites along the courses of rivers Neretva, Buna, Bunica, Bijela, Trebižat, Lištica, Jasenica, Radobol- ja, Studenčica and Crnašnica but also various habitats (springs and streams) in many of their tributaries (e.g. Crnašnica Vrilo, Crno Oko, Jasle, Arapi Vrilo, Rebrac etc.). Sampling sites, apart from spring Jasle in Masna Luka, belong to the so-called „lower Herzegovina“ with an average temperature of 15 °C and an average rainfall of about 1500 mm (16). Details on geographic position of sampling sites and their photos are presented in Fig. 1 and Table 1.Freshwater triclads were collected by hand between  April and December 2011. It is the most convenient, most common and also the easiest way for their collecting. Only at two sites, source of river Buna and Crno Oko spring, where the water depth was greater and it was im-possible to collect the specimens by hand, specimens were collected as described in Kenk (17). e bait jar with a lid bearing many small round perforations is submerged, to-gether with some anchoring ballast, and attached by a line to a float. After 24 hours, triclads will be found inside the  jar. Where possible, during the fieldwork we processed more stations of the same river – e.g. source, middle and lower reach, to include all available habitats and their re-spective characteristic species that occur at different parts of the river. Altogether, samples were collected at 26 sites, including 10 rivers, 6 springs and 1 lake. Fixation, identication and handling tips Many triclads are very sensitive to temperature fluc-tuation and if the water warms up too much, triclads disintegrate easily. Following species collected in studied area belong in this group, Polycelis felina  , Crenobia alpina   and species belonging to genus Phagocata  . ose species must be identified immediately after being collected or they should be transported to the laboratory in termal containers with ice. e specimens of freshwater triclads are often changed after fixation and conservation. So, when it is possible the best practice is to observe, analyse and record external morphological features on living specimens. Although there are several methods for triclads fixation described in Reynoldson & Young (18), Steinmann’s fluid (mixture of 300 ml concentrated nitric acid (65–70%), 300 ml satu-rated solution of mercuric chloride in 5% sodium chloride and 300 ml distilled water) proved to be the best medium Figure 1. Sampling region of Herzegovina.   A  k  e  y t  o t  h  e f   r  e s  h  w a t  e r  t  r  i   c  l   a d  s  (   P  l   a t   y h  e l   m i   n t  h  e s  , T  r  i   c  l   a d  i   d  a )   o f   H e r  z  e  g o v i   n a w a t  e r  c  o u r  s  e s  L  . K n e z  o v i   ć   e t  a l   .  P  e r  i   o d  b  i   o l   , V  o l   1  1  7  , N o 3  , 2  0  1  5  . 4  5  Table 1. Details of sampling sites. Sampling siteBačevićiBlagajBunaBunaBunaČapljinaDonji BrigJasenicaJasenica Freshwater body with locality code Jasenica (15)Buna (16)Neretva (19)Buna (18)Bunica (17)Neretva (22) Arapi Vrilo (21)Jasenica (14)Rebrac (13) Freshwater body type riverriverriverriverriverriverspringriverspring Geographic coordinatesE 17° 49’ 24’’ N 43° 15’ 18’’43° 15’ 24’’43° 14’ 16’’43° 14’ 45’’43° 14’ 28’’43° 06’ 31’’43° 12’ 58’’43° 16’ 31’’43° 16’ 36’’ 17° 54’ 14’’17° 49’ 59’’17° 51’ 21’’ 17° 51’ 14’’ 17° 42’ 23’’17° 48’ 44’’17° 48’ 12’’17° 48’ 06’’  Altitude (m)371262736306275859Sampling siteKnešpoljeKnešpoljeKnešpoljeMaloševići - BrigMaloševići - BrigMasna LukaMostar - BareMostar - DumMostarFreshwater body with locality codeCrnašnica (10)Crnašnica (11)Crnašnica Vrilo (9)Crno Oko (20)Neretva (7)Spring Jasle (1)Radobolja (4)Radobolja (5)Radobolja (6)Freshwater body typeriverriverspringspringriverspringriverriverriverGeographic coordinatesN 43° 21’ 54’’43° 21’ 52’’43° 11’ 51’’43° 13’ 23’’43° 13’ 12’’43° 37’ 49’’43° 20’ 33’’43° 20’ 21’’43° 20’ 12’’ E 17° 38’ 12’’17° 38’ 21’’17° 38’ 12’’17° 49’ 28’’17° 49’ 29’’17° 32’ 46’’ 17° 47’ 17’’17° 48’ 18’’17° 48’ 52’’  Altitude (m)24024424035331210736543Sampling siteMostarsko BlatoPrenj, BijelaPrenjStrugeStudenciStudenciŠiroki Brijeg - Borak Ustava Freshwater body with locality codeLištica (12)Bijela (3)Bijela (2)Trebižat (25)Studenčica (23)Trebižat (24)Lištica (8)Svitava (26)Freshwater body typeriverriverriverriverspringriverriverlakeGeographic coordinatesN 43° 20’ 35’’43° 29’ 28’’ 43° 33’ 04’’ 43° 05’ 32’’43° 10’ 09’’ 43° 09’ 27’’ 43° 23’ 50’’43° 02’ 36’’ E 17° 41’ 36’’17° 48’ 27’’ 17° 47’ 49’’ 17° 41’ 38’’ 17° 37’ 1’’ 17° 36’ 31’’ 17° 35’ 52’’17° 44’ 32’’  Altitude (m)2311454921440482901  L. Knezović et al. A key to the freshwater triclads (Platyhelminthes, Tricladida) of Herzegovina watercourses 46 Period biol, Vol 117, No 3, 2015. for fixation of aquatic triclads. After the fixation, speci-mens were conserved in 70 % alcohol. e morphological features used in identification in this key are: body coloration (color of the dorsal and ven-tral side), the size of the pharynx, the presence of tentacles and their location, number and position of the eyes in respect to each other and the body margin, and the shape of the head. e size of the body and pharynx, as well as the distance between the eyes and the distance between the eyes and body margins are the features best main-tained on fixed specimens. Inner morphological feature, shape of a penis, was used in determination of Polycelis tenuis   and Polycelis nigra  .Some specimens of Dendrocoelum sp., Dugesia sp. and Schmidtea polychroa   have more than two eyes (Fig. 2). In specimens of genus Dugesia   feature when animals have more than two eyes can be related with the age of an ani-mal, while in the specimens of genus Dendrocoelum  this feature can be important for species determination (19). Identification was based on the available literature (e.g. 10, 11, 15, 18, 20 – 24). Notes on the species  We collected freshwater triclads of the following gen-era: Polycelis   Ehrenberg, 1831, Crenobia   Kenk, 1930, Phagocata   Leidy, 1847, Planaria   Müller, 1776, Dendrocoe-lum Örsted, 1844, Schmidtea   Ball, 1974, Dugesia   Girard, 1850, Girardia   Ball, 1974. According to Stanković (12) triclads fauna of western Balkan is divided into three groups, i) widespread Palearctic species, ii) species that occur only in Europe and iii) endemic Balkan species. From the first group in Herzegovina we have reported three species, Crenobia alpina  , Dugesia sp. and Polycelis nigra  . Polycelis felina  , Schmidtea lugubris  , Schmidtea poly- Figure 2. Heads of Dendrocoelum sp. (a,b,c), Schmidtea polychroa (d,e,f) and Dugesia sp. (g,h) showing specimens with different num-ber of eyes. TABLE 2. A list of species at each locality. SpeciesLocality code number1234567891011121314151617181920212223242526 Crenobia alpina  x  Dendrocoelum sp.xxxxxxxxxxxx  Dugesia sp.x  Girardia tigrina  xx  Phagocata bosniaca  x  Phagocata dalmatica  x  Planaria torva  xxxx  Polycelis felina  xxxxxx  Polycelis nigra  xx  Polycelis tenuis  xxxxx  Schmidtea polychroa  xxxxxx Number of species10000231112222202015124232   A key to the freshwater triclads (Platyhelminthes, Tricladida) of Herzegovina watercourses L. Knezović et al. Period biol, Vol 117, No 3, 2015. 47 chroa  , Planaria torva  , Polycelis tenuis  , Dendrocoelum lac-teum , D. album , Phagocata albissima   and  Atrioplanaria racovitzai   belong to the second group, only European spe-cies. From those nine species, we have reported four of them, P. felina  , S. polychroa  , P. torva   and P. tenuis  . From the third group, two endemic species are present in stud-ied area, P. dalmatica   and P. bosniaca  . A list of collected species at each locality is given in Table 2. Family Planariidae Polycelis felina   Dalyell, 1814 (Fig. 3a) is widespread throughout Europe (14), and is one of the most widespread species of freshwater triclads in Herzegovina. P. felina   tol-erates higher temperatures better than C. alpina   and usu-ally inhabits the lower parts of the rivers and streams where the water is warmer and where the water current is slower (25, 26). P. felina   has numerous eyes placed along the an-terior part of the head and along the lateral margins of the body. Two long and narrowed tentacles are situated later-ally on the head. Between head and the posterior part of the body there is a slight constriction. Color of the body, ranges widely from red (individuals recorded at the source of the river Lištica), light and dark brown, to black (indi-viduals recorded in rivers Bunica and Neretva). e aver-age size of the body is 14 mm. Size of the pharynx is a little bit more than half of the total body length. Crenobia alpina   Dana, 1766 (Fig. 3b) is generally as-sociated with high altitude and low temperature, although it also occurs at sea-level in streams that are shaded and cool (27). We collected the species only at one site, in stream Jasle at 1210 m altitude. Specimens of C. alpina   have two eyes situated in non pigmented cup. e distance between the eyes is shorter than the distance between the eyes and body margin. e eyes are situated far back on the head. Tentacles are pointed and located laterally on the head. Although in literature (e.g, 22) individuals of different colors (gray, brown or black) were reported, all of our sampled individuals were black. Ventral side is paler than the dorsal. Average size of the body is 11 mm. Size of the pharynx is half of the total body length. Polycelis nigra   Müller, 1774 (Fig. 3c) has been reported from various localities in Europe and is considered as one of the most widespread triclad on this continent (28).  Although black and brown specimens of P. nigra   were reported (e.g. 18), all of our specimens were black. Dorsal and ventral sides of the body are equally pigmented. ey have numerous eyes along the anterior and marginal side of the body. Average size of the body is 8 mm and the size of the pharynx is a little bit longer than the one half of the total body length.Specimens of Polycelis tenuis   Ijima, 1884 (Fig. 3d) are very similar to the specimens of P. nigra  . ose animals also have numerous eyes with the same position as in P. nigra  . Color of the body comes in all shades of brown. Pigment is not equally distributed and specimens often have darker brown line along the body. Ventral and dorsal sides of the body are equally colored. Head is not clearly separated from the rest of the body. Average size of the body is 9 mm and the size of the pharynx is a little bit longer than the one half of the total body length. One could find difficult to determine whether speci-mens belong to P. tenuis   or P. nigra   and they are often present together in studied area. ey can be distin-guished on the basis of their reproductive system, more accurately structure of their penis. Specimens of P. tenuis   have elongated penis with or without two adenodactyls, while specimens of P. nigra   have short, barrel-shaped pe-nis (Fig. 4) (22). e penis can be observed by cutting a live specimen with a sharp scalpel immediately distal to the pharynx and mouth opening and placing the speci-men on a glass slide with ventral side facing up. en place Figure 3. Dorsal view of Polycelis felina (a), Crenobia alpina (b), Polycelis nigra (c), Polycelis tenuis (d), Planaria torva (e), Phago-cata bosniaca (f), Phagocata dalmatica (g), Dendrocoelum sp. (h), Dugesia sp. (i), Schmidtea polychroa (j), Girardia tigrina (k). Ab-breviations: a: auricle, e: eye; h: head; i: intestinal caecum; ph:  pharynx; t, tentacle; Scale bar: 1 mm.
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