Biologia 67/4: 731—738, 2012Section ZoologyDOI: 10.2478/s11756-012-0069-y

Coexistence of Placobdella costata (Fr. Muller, 1846)(Hirudinida: Glossiphoniidae) and mud turtle Emys orbicularis

Aleksander Bielecki1, Joanna M. Cichocka1, Andrzej Jab�lonski2, Iwona Jelen1,Ewa Ropelewska3, Anna Biedunkiewicz4, Janusz Terlecki5, Jacek J. Nowakowski6,Joanna Pakulnicka6 & Jolanta Szlachciak1

1Department of Zoology, University of Warmia and Mazury in Olsztyn, Oczapowskiego st. 5, 10-718 Olsztyn, Poland; e-mail:alekb@uwm.edu.pl2Museum of Natural History, Wroc�law University, Sienkiewicza st. 21, 50–335 Wroc�law, Poland3Department of Chemistry, University of Warmia and Mazury in Olsztyn, �Lódzki Square 4, 10–957 Olsztyn, Poland; e-mail:ewa.ropelewska@uwm.edu.pl4Department of Mycology, University of Warmia and Mazury in Olsztyn,Oczapowskiego st. 1A, 10–719 Olsztyn, Poland;e-mail: alibi@uwm.edu.pl5Department of Applied Ecology, University of Warmia and Mazury in Olsztyn, Oczapowskiego st. 5, 10–718 Olsztyn,Poland; e-mail: terlecki@uwm.edu.pl6Department of Ecology and Environmental Preservation, University of Warmia and Mazury in Olsztyn, �Lódzki Square 3,10–727 Olsztyn, Poland; e-mail: jacek.nowakowski@uwm.edu.pl

Abstract: Emys orbicularis is receding from Europe, mainly due to anthropogenic habitat changes. Its parasite, Placobdellacostata, is widely distributed within both the former and the present distribution range of the host. Though closely associatedwith the mud turtle, it may have other hosts (birds, amphibians, reptiles). Its reproductive period coincides with that ofits host’s migration to the breeding grounds, thus facilitating dispersal of the parasite. Based on literature data we haveanalyzed the geographic spread of P. costata and mud turtle to observe the possible overlap of their habitats. Observationson the population of mud turtle and the associated leech species (P. costata) were carried out in eastern Poland – PodlasieLowland. The studies were conducted in spring and summer in 1986–1993. The leeches were collected from the turtles caughtin the water and on land. Observations showed that most leeches were found on turtles inhabiting the lake or moving toa breeding area. The greatest intensity of invasion was observed in June and July and that most leeches were observedin female E. orbicularis characterized by greater length of the carapace and weight, compared with males and juvenileindividuals.

Key words: Hirudinida; Glossiphoniidae; mud turtle; Emydinae; parasite; distribution

Introduction

The mud turtle Emys orbicularis (L., 1758) is the onlyPalaeartic species of the American subfamily Emydi-nae; the remaining Eurasian freshwater turtles repre-sent the Asian Batagurinae. Its original distributionrange included whole Europe and western Asia, theeasternmost fringe being the Caspian Sea coast (Fig. 1).During the glaciations the species receded to south-ern Europe and northern Africa. With the subsequentwarming of the climate its distribution range shiftednorthwards, though it never reached northern Europe.At present its northernmost localities are situated inLatvia and the southernmost ones in North Africa,along the Mediterranean coast. In the west the speciesreaches the Iberian Peninsula, in the east – the CaspianSea (Jab�lonski 1992a, b; Fritz 1998, 2000; Lenk et al.1999).

Anthropogenic habitat changes (drainage of mar-shes, intensified agriculture), especially in the last cen-tury, have resulted in a rapid disappearance of the mudturtle. It has become extinct in the Benelux countries,West Germany and northern France. In Central Europe(eastern Germany, Poland, former Czechoslovakia) itsrange is disjunct and limited to insular localities whoserate of disappearance has been increasing within thelast 50 years (Jab�lonski 1992a, b; Fritz 1998, 2000; Lenket al. 1999). In Poland, the mud turtle was a commonspecies with change in its distribution during historicaltimes (Fig. 2); it inhabited practically the whole low-land part of the country.

In the 19th century it still occurred in all the largerriver valleys and lake-pond complexes. In the 20th cen-tury, with increasing devastation of natural habitats,and especially disappearance of large marshy areas, thespecies started to recede rapidly. Climate seems to con-

c©2012 Institute of Zoology, Slovak Academy of Sciences

732 A. Bielecki et al.

Fig. 1. Former (hatched area) and present (black areas) distribution of the mud turtle (Jab�lonski 1992a, b; Fritz 1998, 2000; Lenk etal. 1999) and records of P. costata (circles) (Augener 1925; Autrum 1932, 1936; Paw�lowski 1936; Arndt 1943; Sapkarev 1964, 1975;Paw�lowski 1968; Sket 1968; Soós 1969; Zinevici 1971; Lukin 1976; Russev & Janeva 1976; Sawyer 1986; Bielecki & Tarnawski 1980).

Fig. 2. Former and present distribution of themud turtle (M�lynarski 1971; Gos�lawski & Rybacki pers. com.,Jab�lonski 1992b; Zemanek 1992; Najbar 2008) and localities of

P. costata (Paw�lowski 1968; Dastych 1967; Kufel 1969;Kasprzak 1972; Radkiewicz 1972; Sandner & Wilkialis 1972;Wilkialis 1964, 1970a, b, 1971, 1973; Agapow 1975, 1976, 1977a,b; Hajduk et al. 1978; Hajduk & Hajduk 1979a, b; Hajduk 1980;Hajduk et al. 1980; Najbar 2008) in Poland.

tribute additionally to this situation; on the northerndistribution border it is one of the factors that seri-

ously limit the population density (M�lynarski 1971).At present in Poland there are only three areas (north,east and west Poland) (Fig. 2) where the mud tur-tle reproduces successfully, sporadically or regularly(Gos�lawski & Rybacki pers. com., Jab�lonski 1992b; Ze-manek 1992; Zemanek & Mitrus 1997; So�ltys 2002;Mitrus & Zemanek 2004; Najbar & Szuszkiewicz 2006;Najbar 2008). In the remaining areas mostly few adultindividuals are seen, whose number decreases from yearto year.Placobdella costata [= Haementeria costata (Fr.

Muller, 1846)] is a species of the family Glossiphoniidae.Recent studies have induced Sawyer (1986) to transferit from the genus Haementeria Autrum, 1939 to Pla-cobdella Blanchard, 1893. The latter genus is typicallyNearctic and includes 9 species. Placobdella costata (Fr.Muller, 1846) is a widely distributed species (Fig. 1).It occurs along the European Mediterranean coast(from the Pyrennean Peninsula to the Balkan Penin-sula) and the Black Sea coast (Paw�lowski 1968). It wasalso recorded from the former Czechoslovakia (Lukin1976) and Yugoslavia (Sket 1968; Soós 1969; Augener1925; Sapkarev 1964, 1975), Germany (Paw�lowski 1936,1968), Hungary (Sawyer 1986), Romania (Sket 1968;Zinevici 1971), Bulgaria (Augener 1925; Arndt 1943;Autrum 1936; Russev & Janeva 1976; Bielecki & Tar-nawski 1980), Greece and Albania (Sawyer 1986). It iscommon also in Ukraine, Lithuania, Latvia and Estonia(Sawyer 1986). In France, Spain, the Netherlands and

Coexistence of Placobdella costata and mud turtle 733

England it was found only in the south (Sawyer 1986).In the Scandinavian Peninsula it was found only in Fin-land (Lukin 1976). In the south it is known from Mo-rocco, Algeria, Palestina, Syria, Iran, and also northernCaucasus and Transcaucasia (Paw�lowski 1936, 1968).There are no records of the leech from Switzerland,Luxemburg, Belgium, Denmark, Scotland and Ireland(Paw�lowski 1936, 1968; Sawyer 1968). Lukin (1976) in-cluded P. costata in a group of Palaeartic endemics oflimited distribution, subgroup of southern species.

The distribution of P. costata in Poland until 1965was summarized by Paw�lowski (1968), further recordsbeing listed by Dastych (1967), Kufel (1969), Kasprzak(1972), Radkiewicz (1972), Sandner & Wilkialis (1972),Wilkialis (1964, 1970a, b, 1971, 1973), Agapow (1975,1976, 1977a, b), Hajduk et al. (1978, 1980), Hajduk &Hajduk (1979a, b), Hajduk (1980), and Krodkiewska(2003). The distribution is uneven (Fig. 2), most local-ities being concentrated in the regions of Podlasie Low-land, Baltic Coast and Muzarian Lakeland District.

Until recently it was assumed that P. costata wasan exclusive ectoparasite of E. orbicularis. However,since it was recorded from outside the distribution areaof the mud turtle, it has probably also other hosts. Itshould be noted that P. costata was previously collecteddirectly from the turtles only in rare instances (in the

former USSR, Kowalewski, after Lukin 1976, in Poland,Kasprzak 1972; Najbar 2008, in Bulgaria, Bielecki &Tarnawski 1980).

According to Lukin (1976) P. costata is the onlyPalaearctic leech that feeds on reptilian blood, andmainly on E. orbicularis; in some parts of its distribu-tion area (Asia) it attacks Mauremys caspica Gmelin,1774. Facultatively, it may feed on bird and mammalianblood. This suggestion of Lukin (1976), and also ofother authors, is probably correct, since the mud tur-tle population is undergoing a constant decrease, thusforcing the leech to find other hosts (cf. distribution ofboth species in Figs 1, 2). The only direct observationconfirming the possibility that P. costata under naturalconditions feeds on blood of other vertebrates is findingit by Sapkarev (1964) on a frog and on an aquatic bird(the author did not specify the names of host species).

Life cycle of P. costata has not been studied com-pletely, some information were given in papers byWilkialis (1970b, 1973) and Sawyer (1986). In temper-ate climate it reproduces in the summer. According toliterature data (Wilkialis 1970b, 1973) individuals withdeveloping embryos or young were found only outsidethe hosts. There may be up to 114 embryos, on an av-erage 33. The species, like all other members of Glossi-phoniidae, displays parental care. In laboratory it lives

Table 1. Collection data on the mud turtle and P. costata, east Poland, Podlasie Lowland.

Emys orbicularisNumber of P. costata Date Habitat

No ID Sex Weight (g) Length of carapace (mm)

1 28 F 1200 213 1 (+42*) 5.06.1986 P2 – F 1230 220 7 12.06.1987 P3 – F 1250 224 8 12.06.1987 P4 – F 1270 225 7 12.06.1987 L5 – F 1300 220 1 (+27*) 10.06.1987 L6 73 F 1000 215 3 1.06.1988 L7 – F 1050 218 4 1.06.1988 M8 98 M 460 170 1 1.06.1988 P9 72 M 500 186 2 1.06.1988 P

10 0 J 100 89 1 26.08.1989 C11 52 J 100 89 1 26.08.1989 L12 92 F 870 200 6 13.07.1989 C13 90 F 820 185 1 13.07.1989 C14 97 F 1200 215 6 14.07.1989 L15 93 F 860 200 2 14.07.1989 P16 31 F 1220 225 12 3.06.1991 L17 25 F 1250 215 4 4.06.1991 M18 82 F 800 190 2 6.06.1991 M19 111 F 800 180 1 13.08.1991 P20 112 M 450 157 2 14.08.1991 P21 113 F 850 190 3 15.08.1991 P22 30 F 1050 220 7 4.06.1992 L23 123 F 870 186 2 16.06.1992 C24 94 F 830 182 1 17.08.1992 P25 95 F 450 155 1 24.08.1992 C26 54 F 1100 216 10 7.06.1993 M27 31 F 1180 227 1 (+88*) 7.06.1993 M28 39 F 1250 221 3 9.06.1993 P29 179 M 850 190 2 10.06.1993 C30 29 F 950 185 3 29.05.1993 L

Explanations: ID – individual marking numbers of the turtles, F – female, M – male, J – juvenile, P – ponds or other small stagnantwater bodies, L – lakes, C – water courses, M – migrating to the breeding ground, ( – ) – no data ID, ( * ) – young leeches.

734 A. Bielecki et al.

24–25 months, in the wild most probably the life spanis longer. During lifetime it reproduces several times.Placobdella costata is a vector of Haemogregarina

stepanovi Danilewsky, 1885, a pathogenic parasite ofthe mud turtle (Reichenow 1910; Mishra & Gonzalez1978; Sawyer 1986).

The aim of the study was to analyze the relation-ship between the parasitic leech P. costata and one ofits hosts – the mud turtle E. orbicularis. The authorsput forward a hypothesis: there is a high probability,that intensity of invasion by the leech is related withsize and weight of the body of E. orbicularis.

Study area, material and methods

Observations on the population of mud turtle and the as-sociated leech species P. costata were carried out in easternPoland – Podlasie Lowland. The study area (ca. 25,000 ha)included all the characteristic habitats: water courses, per-manent and ephemeral water bodies, marshes and swamps.The studies were carried out in spring and summer in 1986–1993 (Table 1). The leeches were collected from the turtlescaught in the water and on land. Most turtles were individ-ually marked for other purposes, thus ensuring that eachturtle was caught and examined once only. Plants, suchas Phragmites communis Trin., Schoenoplectus lacustris L.,Sparganium ramosum Huds., Acorus calamus L., Typha lat-ifolia L., Typha angustifolia L., Glyceria aquatica L. Wahlb.in the littoral of the streams and reservoirs, and also in thecommunities of Stratiotes aloides L. and Nymphaea candidaPresl. were also checked for the leeches.

Table 1 shows the number of collected individuals ofP. costata, place, date and selected parameters describingE. orbicularis, prepared charts showing the relationship be-tween the turtle body weight, length, habitat, collectiondate and the number of leech species. The null hypothesisthat the Spearman’s rank correlation coefficient is equal tozero (H0: R = 0), to determine statistical significance of therelationship between body length and weight of the turtlesand the number of leeches, was verified. All analyses wereperformed using STATISTICA-PL 8.

Results

The leeches found on the turtles were usually attachedin the region of groin and neck, where the skin is thinand unarmoured. In one case the leech was attachedto the mid part of plastron. Twelve leech specimenswere collected from plants, in deeper reservoirs mostlyfrom Stratiotes aloides, in shallower ones from old, deadleaves of Typha latifolia.

In shallow, swampy reservoirs overgrown with veg-etation, practically all the turtles collected had fromone to several dozen leeches of various sizes (Fig. 3,Table 1). In less vegetated, deeper reservoirs, irrespec-tive from their size, most of the turtles had no leeches.It is noteworthy that adult leeches with several dozenyoung were found attached to several females migratingto their breeding grounds (Table 1).

The relations between the turtle body weight,length, habitat, collection date and the number ofleeches are presented in Figs 4 and 5.

Fig. 3. A – dorsal view of P. costata, B – ventral view of P. costatawith eggs (Photo: J. Cichocka), C – P. costata on an adult mudturtle. �Leczynsko-W�lodawskie lakeland, east Poland (Photo: A.Bielecki).

Fig. 4. The relation between the habitat, collection date and thenumber of leeches. P – ponds and other small stagnant reservoirs,L – lakes, M – during migration to breeding grounds, C – watercourses.

The relation shown in Fig. 4 demonstrates thatmost leeches were found on turtles inhabiting the lake[from 1 adult with 27 young to 12 adult specimens]or moving to a breeding area [from 1 adult with 88young to 10 adult leeches]. The greatest intensity of

Coexistence of Placobdella costata and mud turtle 735

Fig. 5. The relation between the turtle body weight, length ofcarapace and the number of leeches.

invasion was observed in June and July, when 75 and15 individuals of P. costata, respectively, were collected.

The relation shown in Fig. 5 and Table 1 indicatesthat most leeches were observed in female E. orbicularis(96 individuals of P. costata). Females were character-ized by greater length of the carapace (155–225 mm)and weight (450–1300 g), compared with males and ju-venile individuals, which were not numerous.

The Spearman’s rank correlation coefficients (R)of the relationships between body length and weight ofthe turtles and the number of leeches were 0.8919 and0.8531, respectively and were statistically significant(n = 27; P < 0.05).

Discussion

According to Siddall et al. (2005) the genus Placobdellais a wholly North American clade with the exceptionof the European Placobdella costata nested well withinthe group. Although the position for P. costata may atfirst appear to be odd, it is completely consistent withpatterns of host association. Fossil and molecular datasuggest that the dispersal of E. orbicularis from NorthAmerica to Europe occurred in the early Miocene (Lenket al. 1999; Fritz 1998). It appears they arrived withleeches attached (Fig. 6).

Leeches, which parasitize on reptiles (mostly tur-tles) and originate from North America like P. costataare P. parasitica (Say, 1824) and P. ornata (Ver-rill, 1872). Placobdella parasitica is not closely relatedto one host, but parasitizes on many species of tur-tles: Chrysemys picta Schneider, 1783, Clemmys gut-tata (Schneider, 1792), Graptemys pseudogeographica(Gray, 1831), Pseudemys scripta (Schoepff, 1792) Ster-nothaerus odoratus (Latreille, 1802) and Chelydra ser-pentine (L., 1758). The leech parasitizes on them sea-sonally from early spring to midsummer. Placobdellaornata parasitizes the same species of turtles, but alsoattacks alligators. Both P. parasitica and P. oranatajust as P. costata are able to attack other animals thanreptiles, P. parasitica reportedly on amphibians andP. ornata on amphibians, birds in northern Canada andon humans facultatively (Sawyer 1986; Siddall & Bow-erman 2006). The leech P. ornata was observed feedingfrom the blood sinuses of the plastron and carapacebones of turtles (Siddall & Gaffney 2004).

Najbar (2008), examining the parasites and dis-eases of E. orbicularis in Poland, found that the turtlewas attacked by three leech species: P. costata and twonew records in Poland – P. ornata and P. papillifera.We had checked this material and we found that young

Fig. 6. Approximate pattern for continents during Tertiary and probable dispersal events for species of Placobdella (modified afterSiddall et al. 2005).

736 A. Bielecki et al.

specimens of P. costata were mistakenly determined asP. ornata or P. papillifera which are distributed onlyin the Nearctic Region.

During the studies the leeches were found most fre-quently on turtles inhabiting the lake (Fig. 4). Thisplace is a shallow gulf of the lake with dense vegeta-tion, drain watercourse and little available for people.A mud turtle prefers such kind of stands. The obser-vation that in strongly marshy, shallow reservoirs thatovergrow with vegetation practically all the turtles boreleeches is in accordance with Sapkarev’s (1963, 1964)results. He studied the occurrence of the leeches de-pending on the depth of the reservoir and demonstratedthat P. costata occurred always in the shallowest partof the littoral zone. Such an occurrence in water bodiesis probably associated on one hand with its tempera-ture requirements, and on the other with the fact thatthere it waits for its potential hosts – the turtle or otherhosts, e.g., grass snake or wading birds.

The study showed that most leeches were observedon female E. orbicularis (Fig. 5, Table 1). Females werecharacterized by a greater carapace length and bodyweight compared with males and juvenile individuals.At the same time, a strong correlation was shown be-tween body length and the number of leeches parasiticon a turtles, (the larger specimen the greater chancefor find the leeches on it). A similar relationship re-cently described in detail, but for leeches parasitic onfish has been demonstrated between the length of thebody of grayling and Atlantic sturgeon and the numberof leeches (Bielecki et al. 2011a, b).

In view of the lack of literature data on leecheswith young being attached to the hosts, it is interest-ing that during the research we found several instancesfrom 1 adult with 88 young to 10 adult leeches being at-tached to five female turtles migrating to their breedinggrounds (Fig. 4). The coincidence of the leech reproduc-tive period and the migration to the breeding groundsof the mud turtle females seems to favour spreadingof the leech to new water bodies crossed by the turtlefemale on the way to lay her eggs.

During the research in late summer leeches withblood-filled crop were found only in those reservoirswhere the turtles winter over (27 specimens in 5 reser-voirs). In four reservoirs left by the turtles in the latesummer we found only leeches with empty crop (12specimens) (Fig. 4). The fact that leeches with blood-filled crops in the summer were limited to the reservoirswhere the turtles winter over indicates a strong associ-ation between the leech species and its host, and is anindicator of the reservoirs which are used by the turtleas winter quarters. If these observations are confirmed,they can be used for an indirect finding of the turtle.It is easier to find the leeches outside their hosts andcheck their alimentary tracts, than to catch the turtles.

Considering the purportedly stenozoic character ofthe host-parasite association between E. orbicularis andP. costata, it is interesting to consider their geographicdistribution. Except a large area in south west Poland(Fig. 2), the records of P. costata coincide to a large

extent with either former or present distribution of themud turtle. The distribution area of the mud turtle inEurope (M�lynarski 1971) (Fig. 1) overlaps to a large ex-tent with the data on the occurrence of P. costata con-tained in the papers of Paw�lowski (1936) and Sawyer(1986), but the localities of the leech in England, theNetherlands and perhaps in Finland do not confirm thestenozoic association between the mud turtle and theparasite. They are located outside the present, but stillwithin the historical distribution range of the host, sug-gesting that the parasite has retained its former distri-bution though the host receded. In such areas, remnantsof the former distribution of the mud turtle, it has mostprobably found new hosts. In laboratory conditions theleech was fed with blood of grass snake Natrix natrixL. or duck (Paw�lowski 1968). In turn, in nature theleech often attach legs of researchers who are walkingin water reservoirs (Pawlowski, oral information, 1980).

The new and probably correct systematic place-ment of P. costata in the Nearctic genus Placobdella bySawyer (1986) is in agreement with the geographic ori-gin of its host. Since E. orbicularis is the only Palaearc-tic member of the American subfamily Emydinae andP. costata is the only Palaearctic species of the genusPlacobdella, its Nearctic origin is almost certain.

In conclusion, the hypothesis in this study has beencorroborated: there is a high probability, that intensityof invasion by the leech is related with size and weightof the body of E. orbicularis.

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Received October 18, 2011Accepted February 25, 2012