Distribution and status of medicinal leeches (genus Hirudo ) in the Western Palaearctic: anthropogenic, ecological, or historical effects?

AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

Aquatic Conserv: Mar. Freshw. Ecosyst. (2009)

Published online in Wiley InterScience(www.interscience.wiley.com). DOI: 10.1002/aqc.1071

Distribution and status of medicinal leeches (genus Hirudo) in theWestern Palaearctic: anthropogenic, ecological, or historical effects?

SERGE UTEVSKYa,�, MAJA ZAGMAJSTERb, ANDREI ATEMASOVc, OLEKSANDR ZINENKOd, OLGA UTEVSKAe,

ANDREI UTEVSKYa and PETER TRONTELJb

aDepartment of Zoology and Animal Ecology, V.N. Karazin Kharkiv National University, pl. Svobody 4, Kharkiv 61077, UkrainebDepartment of Biology, Biotechnical Faculty, University of Ljubljana, Vecna pot 111, SI-1000, Ljubljana, SloveniacResearch Institute of Biology, V.N. Karazin Kharkiv National University, pl. Svobody 4, Kharkiv 61077, Ukraine

dMuseum of Nature, V.N. Karazin Kharkiv National University, vul. Trinklera 8, Kharkiv 61022, UkraineeDepartment of Genetics and Cytology, V.N. Karazin Kharkiv National University, pl. Svobody 4, Kharkiv 61077, Ukraine

ABSTRACT

1. Distribution and status of medicinal leeches were re-considered in the light of the new taxonomy recognizingfour Western Palaearctic species: Hirudo medicinalis, Hirudo verbana, Hirudo orientalis and Hirudo troctina.2. Recent records and new data obtained on expeditions to Ukraine, Russia, Azerbaijan, Kazakhstan,

Uzbekistan and the Western Balkans were mapped to obtain an up-to-date overview of the distribution.3. Three hypotheses explaining the current ranges of all Hirudo species were tested. The ecological hypothesis,

suggesting a strong impact of large-scale environmental factors, received the highest support, whileanthropogenic influence was minimal, and no historical patterns of refugia and colonization were detected.4. Mapped localities of all Hirudo species show extensive, belt-shaped ranges extending from east to west.

H. medicinalis is distributed from Britain and southern Norway to the southern Urals and probably as far as theAltai Mountains, occupying the deciduous arboreal zone. H. verbana has been recorded from Switzerland and Italyto Turkey and Uzbekistan, which largely corresponds to the Mediterranean and sub-boreal steppe zone.H. orientalisis associated with mountainous areas in the sub-boreal eremial zone and occurs in Transcaucasian countries, Iranand Central Asia. H. troctina has been found in north-western Africa and Spain in the Mediterranean zone.5. Based on the data gathered, and considering real and potential threats, global IUCN category Near

Threatened is proposed forH. medicinalis,H. verbana, andH. orientalis, whileH. troctina can only be assigned tocategory Data Deficient. Copyright r 2009 John Wiley & Sons, Ltd.

Received 6 February 2009; Revised 22 June 2009; Accepted 1 August 2009

KEY WORDS: Hirudo medicinalis; Hirudo verbana; Hirudo troctina; Hirudo orientalis; ecology; biogeography; conservation

Supporting information may be found in the online version of this article

INTRODUCTION

The medicinal leech (Hirudo spp.) is one of the most famous and

well-studied invertebrates, especially in terms of its medical

applications, biology and physiology (Sawyer, 1986; Zapkuviene

and Petrauskiene, 2000; Baskova and Isakhanyan, 2004;

Petrauskiene, 2008). Furthermore, the medicinal leech has been

considered as an endangered species that was declining

throughout most of its geographical range, mainly because of

the vast harvesting for medicinal purposes in the 19th century,

recent collecting pressure, and a general loss and pollution

of wetland habitats (Sawyer, 1981; Elliott and Tullett, 1984).

Not surprisingly, the species has been subject to international

conservation concern (IUCN, 2008; Wells et al., 1983);

Convention on the Conservation of European Wildlife and

Natural Habitats) and attempts to control commercial trade

(Convention on International Trade in Endangered Species of

Wild Fauna and Flora App. II; Annex V of the EU Council

*Correspondence to: Serge Utevsky, Department of Zoology and Animal Ecology, V.N. Karazin Kharkiv National University, pl. Svobody 4,Kharkiv 61077, Ukraine. E-mail: [email protected]

Copyright r 2009 John Wiley & Sons, Ltd.

directive 92/43/EEC on the conservation of natural habitats and

of wild fauna and flora).

Twenty-five years ago, in their classical paper, Elliott and

Tullett (1984) stated that ‘the presence of the medicinal leech

throughout Europe suggests that it is not an endangered species

y’, but concluded that further information is urgently required

before decisions can be made on its conservation. Since that

time, our understanding of what has been considered as a single

species under the name Hirudo medicinalis Linnaeus, 1758 for

almost two centuries, has changed dramatically. Using different

systematic approaches, two neglected species, Hirudo troctina

Johnson, 1816, and H. verbana Carena, 1820, were reinstated

(Nesemann and Neubert, 1999; Trontelj et al., 2004; Trontelj

and Utevsky, 2005; Siddall et al., 2007). A fourth species,Hirudo

orientalis S. Utevsky and Trontelj, 2005, was described for the

first time. It has been further demonstrated that the species most

often traded and applied as a medical device or model species is

not H. medicinalis at all, but rather its less known congener

H. verbana (Siddall et al., 2007). It is important for the new

taxonomic findings to be taken into account as soon as possible

to avoid confusion and uncertainty. Most of all, conservation

actions based on existing knowledge and regulations might be

misguided. For example, all regulations intended to control the

trade with leeches address H. medicinalis, while the species most

often marketed in main leech-exporting countries, such as

Turkey and Russia, is H. verbana. A prerequisite for status

assessment and correct incorporation into national legislations

is a better understanding of the species’ distribution.

All existing accounts and global distribution maps (Elliott and

Tullett, 1984; Nesemann and Neubert, 1999; Hutchins et al.,

2003) are essentially out of date as they are mostly based on old

data and do not consider the new taxonomy. For the four

Western Palaearctic medicinal leech species, a tentative outline of

their distribution can be inferred indirectly by what has been said

about the distribution of characteristic coloration types or forms.

According to these reports H. medicinalis occurred in Western

and Central Europe (Nesemann and Neubert, 1999), Ukraine

(Lukin, 1976), and Lithuania (Zapkuviene, 1972).H. verbana was

known from the eastern Mediterranean region and the Balkans,

Greece, Turkey and the entire Levant range (Nesemann and

Neubert, 1999), as well as Moldova, Ukraine, the Krasnodar

Territory (Russia), and Armenia (Lukin, 1976; Utevsky et al.,

1998). Hirudo troctina was known from Morocco, Tunisia, and

Algeria (Hechtel and Sawyer, 2002), whereas H. orientalis was

found in Georgia, Armenia, Azerbaijan, and Iran (Stschegolew

and Fedorova, 1955; Lukin, 1976; Utevsky et al., 1998). This

incomplete picture relies on literature accounts of varying

reliability and even anecdotal sources, several decades or even

centuries old. The data can only be verified by field observations.

It nevertheless suggests that the ranges are, to a high degree,

exclusive of one another. A further question linked to the present-

day distribution and the conservation of wild populations is

whether these are the consequence of natural processes alone, or

whether they have been influenced by human activity. It has been

suggested that during the centuries of intense collecting and trade

of leeches across Europe and western Asia the human impact was

so strong that the distribution can no longer be considered

natural (Lukin, 1957, 1976; Elliott and Tullett, 1992).

Three hypotheses explaining the current ranges of the

different species of Hirudo can be put forward. They are not

mutually exclusive, but each of them should result in one

particular pattern prevailing over others in a certain area.

Anthropogenic

During times of greatest use, local sources of leeches had

become exhausted and transport over long distances was

required to meet the demand. To some countries, like France,

millions of leeches were imported from Eastern Europe every

year (Lukin, 1976). Since all four species are known to be used

medically, and people did not pay much attention to small

differences in coloration pattern, shifts in species ranges due to

translocations are expected. They should be visible (1) as

outliers of a contiguous range, and (2) sympatric occurrence of

two or more species in the surroundings of urban centres

where demand was highest.

Ecological

Under this hypothesis, the species’ ranges are being determined

by ecological factors at the continental scale. The distribution

of species is expected to be correlated with environmental

parameters that are constant across large areas, such as

temperature and precipitation. The ranges are likely to

correspond to major landscape types (e.g., Isachenko and

Shlyapnikov, 1989; Banarescu, 1991).

Historical

Under this hypothesis, the present-day distributions reflect

historical biogeographical events, for example an interplay of

glacial refugia and post-Pleistocene colonization. Scenarios

such as colonization from Mediterranean refugia, or invasion

from Asia would be corroborated by finding parallels among

known distribution patterns for groups of closely related

species (Banarescu, 1991; Taberlet et al., 1998; Hewitt, 1999;

Joger et al., 2007; Schmitt, 2007).

MATERIALS AND METHODS

Data sources

The information used to infer the distribution of medicinal

leeches in the Western Palaearctic was obtained from three

kinds of sources: (1) direct field results from several

expeditions to Ukraine, Russia, Azerbaijan, Kazakhstan,

Uzbekistan, and the Western Balkans, carried out from 2006

to 2008; (2) preserved samples with precise labels from our

own collections and provided by museums and colleagues; (3)

published data, Lukin (1957) and later publications were

considered. Unless mentioned elsewhere, the following sources

were used: Keim (1993), Dolmen et al. (1994), Kruglov (1997),

Nesemann (1997), Felix and van der Velde (2000), Kasparek

et al. (2000), Zapkuviene and Petrauskiene (2000), Akbulut

et al. (2001), Ramos et al. (2001), Merila and Sterner (2002),

G"owacinski and Nowacki (2004), Ruffo and Stoch (2005),

Grosser and Pesic (2006), Ben Ahmed et al. (2008), BUGS

(2008), Chobot (2008), EUNIS (2008), Greke et al. (2008),

Limnodata (2008), Merzlikin (2008), National Biodiversity

Network (2008), Saglam et al. (2008), Ramsar sites, Bulgaria:

List of wetlands of international importance in Bulgaria

(http://www.ramsar.org/wn/w.n.bulgaria_five_plus_three.htm),

Red Data Book of Bashkortostan (http://www.redbook.ru/

article124.html), and Red Book of the Republic of Belarus

(http://redbook.minpriroda.by/about.html).

S. UTEVSKY ET AL.

Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. (2009)

DOI: 10.1002/aqc

Field investigations were designed to cover areas where range

boundaries had been expected but not yet confirmed, and in

areas where any reliable data on medicinal leeches were lacking

at large geographic scales. Of special interest was the vast

territory in Central Asia where the eastern and south-eastern

boundaries of three Hirudo species (H. medicinalis, H. verbana

and H. orientalis) were expected according to previous work

(Lukin, 1976; Utevsky et al., 1998; Nesemann and Neubert,

1999). Uzbekistan and Kazakhstan were included also because

of very scarce information on the occurrence of the medicinal

leech there (see Lukin, 1957, 1976). The localities were chosen to

cover the surveyed areas as evenly as possible. However, to

maximize the likelihood of success, we had to follow, to a

considerable extent, previous records and information provided

by local people, as the occurrence of medicinal leeches tends to

be sporadic and unpredictable (Lukin, 1976).

At each surveyed water body, attempts to collect leeches

were made at a series of points in different zones. The leeches

were attracted by agitating the water with the hand and by leg

movements in water no deeper than 1m. The sampling time at

each water body was 0.5–1 h. The specimens were identified

using differences in the coloration patterns described by

Trontelj and Utevsky (2005) and Utevsky and Trontelj

(2005). The same identification characters were used for the

samples obtained from collections. The coloration patterns are

species-specific characters. Their distribution correlates with

other biological properties such as molecular sequence data

(Trontelj and Utevsky, 2005; Siddall et al., 2007) and

chromosomes (S. Utevsky, unpubl. data).

A major problem with treating previous distribution

records from the literature was that until recently the name

H. medicinalis was used to denote any Hirudo species. Only

rarely the ‘coloration types’ were described as either officinalis,

serpentina, or orientalis (e.g. by Zapkuviene, 1972, Lukin,

1976). These can be reliably assigned to the species H. verbana,

H. medicinalis, and H. orientalis, respectively. Even in work

published after 1999 and 2004, when the independent status of

H. verbana was first formally re-established (Nesemann and

Neubert, 1999), and later corroborated by molecular

systematic approaches (Trontelj et al., 2004; Trontelj and

Utevsky, 2005), many authors did not take into account the

new systematics and continued to use a single name for all

medicinal leeches found in the region. The data were treated

according to their taxonomic reliability, ranked by probability

classes as proposed by Frey (2006), and slightly changed for

the purposes of this research (Table 1). Only data from

categories A, B, and C were used to infer species distribution

ranges and to test hypotheses. Records of the medicinal leech

with no or dubious taxonomic status (categories D and E) were

not used in the analyses, but are presented on the distribution

map, to assist inference of ranges based on biogeographical

considerations, where reliable species identifications are

missing.

GIS and statistical analysis

Geographical coordinates were assigned to all localities where

medicinal leeches were found. In the field, the geographical

position was determined using global positioning system

(GPS) devices. In other cases, localities were identified

according to the description in the literature or collection

labels. In most cases, the Google Earth (version 4.3) online

application (http://earth.google.com/) was used. In some

literature sources only distribution maps with point data or

presence in UTM squares were given, without naming exact

localities (see the Supplementary Data). These maps present

valuable information for a large-scale overview of distribution.

They were digitized and fitted to a known geographical

projection in order to determine the coordinates of points. In

the cases of UTM squares, coordinates of the square centroid

were taken. The Lambert Conformal Conic Projection

(Central Meridian: 251, Standard Parallels: 431 and 621,

Latitude of Origin: 301) was used to prepare distribution

maps and perform spatial analyses.

To investigate trends in species distribution ranges, various

approaches known from home range analysis are commonly

used (Fortin et al., 2005). Minimum convex polygons (MCPs)

were mapped for each species to present their ranges (Mohr,

1947; Fortin et al., 2005). To get a measure of range overlap,

the coefficient of areal association (CAA), the ratio between

the area where ranges overlap and the area of both species

ranges together (Metternicht, 2001; Maruca and Jacquez,

2002) was calculated The coefficient varies from zero (e.g. no

areal overlap) to one (perfect correspondence). Only non-sea

area within MCPs (as marked on Figure 2) was used in

calculations.

The Hirudo records were plotted on a map of landscape

types adapted from Isachenko and Shlyapnikov (1989). The

map was digitized and vectorized with GIS software.

Environmental variables were obtained from global maps

of climate variables Worldclim, version 1.4 (http://

worldclim.org), which are available as raster files with a

30� 30 seconds resolution. Bioclimatic variables were derived

from monthly temperature and rainfall values (see Hijmans

et al., 2005 for further explanation of data derivation). The

following environmental information from this data source

was used: annual mean temperature, minimum temperature of

the coldest month in the year, temperature seasonality

(standard deviation), annual precipitation, precipitation of

the driest month in the year, and precipitation seasonality

(coefficient of variation) (Hijmans et al., 2005).

A circle with a 10 km radius around every record point was

used to gather information on environmental variables. This

resulted in an area of about 314 km2 from which ecological

information was averaged for each record. There were two

reasons for taking this wider area into account: first, the

positional inaccuracy of the determined localities was allowed,

and second, the near surroundings were included rather than

Table 1. Probability classes for evaluating the reliability of speciesdeterminations of four medicinal leech species from different sources(according to Frey (2006), slightly modified)

Class Description

A: Verified The authors’ evaluation of preserved physicalevidence that exhibits diagnostic characteristics

B: Highly probable Publications with reliable specific assignmentsbased on an expert’s decision

C: Probable Publications and other information sourceswith exact images depicting a species-specificcoloration pattern.

D: Possible Species assignment can be made based onbiogeographical considerations

E: Questionable Uncertain specific assignment, Hirudo sp.

DISTRIBUTION AND STATUS OF MEDICINAL LEECHES IN THE WESTERN PALAEARCTIC

Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. (2009)

DOI: 10.1002/aqc

taking measurements at the very exact point in space. After

overlaying the distribution data with environmental

information layers in GIS, the averages of a particular

variable for each circle polygon (Beyer, 2004) were calculated

and the distribution of these values for each species were

presented by box-plots. Differences in the distribution of

environmental variable values among species were examined

employing non-parametric test statistics (Kruskall–Wallis

for all, and Mann–Whitney U test for pairwise species

comparisons). All distribution maps and GIS analyses were

performed with the use of ArcGIS, version 9.1 (ESRI) and

Hawth’s Analysis Tools, version 3.26 (Beyer, 2004). Statistical

calculations were done in SPSS, version 14.0.

RESULTS

Distribution patterns

Altogether 855 localities of medicinal leeches were considered:

of them, 610 (71%) were sufficiently reliable to infer the ranges

of different species (categories A, B, and C): 461 for

H. medicinalis, 120 for H. verbana, 15 for H. troctina and

14 forH. orientalis (Figure 1). These constitute the core data of

the analyses. A detailed overview of all localities including

probability classes of species determination can be found in the

Supplementary Data Appendix.

The inferred ranges of the four species differ in size and

geographic position, and are to a great extent mutually

exclusive (Figure 2). The overlap between ranges of H.

medicinalis and H. verbana was small, with a coefficient of

areal association (CAA) of 0.14. It was even smaller for the

ranges of H. verbana and H. orientalis (CAA5 0.06), while

other species pairs had no area in common. In all four species

ranges the east–west axis exceeded the north–south axis.

Hirudo medicinalis is the northernmost of the four species,

reaching as far to the north as 6213007.40 0 in Norway, and

62112034.00 0 in Sweden (Figure 1). The largest east-to-west

distance between reliable localities was about 3600 km. It is

almost certain that localities in the Altai Territory, Russian

Federation (Irisova, 2006), belong to this species, broadening

the range to over 5700 km, from Great Britain in the west to

the Altai Mountains in the east. Nevertheless, the data to

obtain a clear impression of the species’ eastern boundary is

still lacking. Reliable records for the occurrence of H.

medicinalis were found for 17 European and Asian countries:

Norway, Sweden, United Kingdom, Netherlands, France,

Germany, Poland, Lithuania, Latvia, Belarus, Russian

Federation, Ukraine, Switzerland, Czech Republic, Austria,

Hungary, Slovenia and Croatia. According to Voskresensky

(1859), the medicinal leech occurred in West Siberia, where

it was collected for medicinal purposes. The present-day

occurrence of the medicinal leech there is questionable, as we

could not find it in the adjacent areas of northern Kazakhstan.

Obvious gaps in the distribution record in some countries (e.g.

France, Germany, Romania) most probably reflect lack of

sampling effort rather than true absence of the species. High

densities of records in some countries (e.g. Netherlands,

Poland, Lithuania) may be the consequence of both better

national sampling coverage and the abundance of favourable

lowland wetland habitats.

Hirudo verbana is distributed south of H. medicinalis in an

almost parapatric fashion with little overlapping (Figures 1

and 2). The species was reliably found in 17 countries:

Switzerland, Austria, Germany, Italy, Slovenia, Croatia, Bosnia

and Herzegovina, Serbia, Montenegro, Macedonia, Greece,

Hungary, Moldova, Ukraine, Russian Federation, Turkey and

Uzbekistan. Moldova and Armenia were mentioned by Lukin

(1976) among countries where the officinalis form of the

medicinal leech (i.e. H. verbana) occurred, but exact data were

not provided. It is presumably present also in southern France

Figure 1. Distribution ofHirudo species records in the Western Palaearctic. Records ranked as ‘probable’, ‘highly probable’ or ‘verified’ (see Table 1)are taxonomically assigned, while records with lower taxonomic reliability ranks are left unassigned.

S. UTEVSKY ET AL.

Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. (2009)

DOI: 10.1002/aqc

and northern Spain. Obvious gaps with missing data from

Bulgaria and Greece most probably reflect lack of sampling

rather than true absence of the species. The easternmost records

were from Samarqand Province in Uzbekistan, resulting in an

east-to-west extent of about 4600km. The range of H. verbana

includes some areas in Central Asia where the leeches seem to

tolerate generally arid conditions.

Hirudo orientalis is an Asian species, restricted to

mountainous regions of the Caucasus, Central Asia and

Iran. So far, its presence has been confirmed for at least four

countries: Azerbaijan, Iran, Uzbekistan and Kazakhstan.

Most likely, it occurs also in Georgia, and probably in

Armenia. These countries are a part of Transcaucasia, which

was mentioned by Lukin (1976) as the range of the Persian or

Georgian medicinal leech, now considered as H. orientalis. The

known range extending from the eastern Caucasus to the

western Tien Shan (approximately 2000 km) is smaller than in

the first two species, but slightly larger than in H. troctina (see

below).

Hirudo troctina displays an essentially west Mediterranean,

rather than North African distribution as implied by some

recent accounts of this species (Nesemann and Neubert, 1999;

Hechtel and Sawyer, 2002). Blanchard (1893) listed H. troctina

among the Spanish leech species, but this had remained

unsubstantiated. Recent inspection of the Madrid Museum

Hirudinea collection revealed that all medicinal leeches from

Spain in fact belong to this species. However, the collection

contains no samples from the Atlantic north west of the

Iberian Peninsula where climatic conditions might favour the

existence of H. verbana. There is no information on whether

H. troctina directly borders with either H. verbana or

H. medicinalis. Thus, H. troctina appears to be limited to

Spain, Morocco, Algeria, and Tunisia, while data from Portugal

and Libya are currently lacking. Further to the east, reliable data

on any Hirudo species are lacking. El-Shimy (1986) questioned

several old records of the medicinal leech in the Nile system

and Levant attributing them to misidentifications with

Limnatis nilotica (Savigny, 1822).

Hypotheses

Anthropogenic

All four species ranges are largely or entirely mutually

exclusive (Figure 2). There were only three cases of obvious

outliers. The first two are occurrences of H. verbana in central

Europe in a clay pit in east-central Germany and at the

German–Swiss border (Figure 1). These two localities reach

far within the range of H. medicinalis, differing in

environmental variables and ecological conditions typical of

other parts of the H. verbana range (see below). The third is an

apparent outlier of H. verbana in Uzbekistan, 2000 km away

from its range in the west, and within the area of H. orientalis.

The habitat was frequented by cattle, and was reminiscent

of other H. verbana habitats — alluvial landscape with reeds

surrounding open water in the floodplain of the Karadarya

River, a tributary of the Zeravshan. There were no other

outliers that could be interpreted as the result of human

activity, such as deliberate or accidental translocation of

leeches. Furthermore, this hypothesis predicted concentrated

allopatric occurrence close to large cities, but no such records

were found. Consequently, transportation by humans does not

seem to be an important factor shaping the gross distribution

patterns of the four Western Palaearctic medicinal leech

species.

Ecological

The places where the four species were recorded differ

significantly in temperature and precipitation (Table 2,

Figures 3, 4 and 5). Annual mean temperature and the

temperature of the coldest month are lowest in the range of

H. medicinalis, and highest in the range of H. troctina.

Figure 2. Ranges of Hirudo species visualized by minimal convex polygons for each species. Only reliable species determinations are considered.

DISTRIBUTION AND STATUS OF MEDICINAL LEECHES IN THE WESTERN PALAEARCTIC

Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. (2009)

DOI: 10.1002/aqc

Temperatures within the ranges of H. verbana andH. orientalis

are intermediate, but the areas differ in precipitation. While

the former species was found in areas with considerable

precipitation in the driest month of the year, H. orientalis can

deal with the most extreme droughts (Table 2). When mapped

on the landscape types proposed by Isachenko and

Shlyapnikov (1989), all four species showed distinct affinities

(Figure 6). While H. verbana is mainly distributed in the

Mediterranean and the sub-boreal steppe zone, H. medicinalis

prefers the deciduous arboreal zone. H. orientalis in the east is

associated with mountainous areas in the sub-boreal eremial

zone, and H. troctina with the Mediterranean zone in the

extreme west, thereby resembling ecologically H. verbana.

The ranges of H. medicinalis and H. verbana are positioned

parapatrically, sharing an extensive contact zone.

Nevertheless, we were not able to find any hybridization

zone, not even local hybrid populations. Only at two sites

syntopic occurrence of both species was recorded, in Hungary

(Nesemann and Neubert 1999) and eastern Ukraine (this

research). The general lack of distributional overlap combined

with occasional local sharing of habitats might be a sign of

competitive exclusion between both species, driven by

ecological preferences. Indeed, H. verbana and H. medicinalis

sites differ significantly in all studied variables, except median

annual precipitation (Table 2). Nevertheless, annual

precipitation is differently distributed among both species,

as indicated by results of the Kolmogorov–Smirnov Z test

(Table 3). Altogether, ecological factors such as temperature

and rainfall/aridity, either measured directly or expressed via

landscape types, seem to substantially correlate with the

distribution patterns of Hirudo species (Figures 4 and 5).

Historical

In order to search for potential historical parallels, several

examples of groups of closely related species and subspecific

taxa with postglacial dispersal from classic refugia (Taberlet

et al., 1998; Hewitt, 1999), and zoogeographical patterns of

aquatic and amphibian fauna (Banarescu, 1990, 1991; Trontelj

et al., 2005; Culling et al., 2006; Sediva et al., 2008)

were considered. The four paradigms of postglacial range

expansion — (i) the hedgehog, (ii) the bear, (iii) the butterfly,

(iv) the grasshopper (see Schmitt, 2007) — were also taken into

account. There are two commonalities to these examples

indicating their dependence on the same historical factors

acting during the Pleistocene and the subsequent period of

dispersal. First, there is a clear pattern of ranges of closely

related taxa spread from the west to the east of Europe for

terrestrial and amphibian animals. Second, there is a strong

correspondence with the recent and/or historical structure of

main river basins for fish, molluscs and some crustaceans.

Medicinal leeches match neither of these patterns. To the

extreme south west and east, H. troctina and H. orientalis,

respectively, are too localized to be considered as post-glacial

invaders. In the vast area between, the ranges of H. medicinalis

and H. verbana form a northern and southern belt, res-

pectively, reaching from the Atlantic west of Europe to beyond

the Urals and Caspian region. This type of distribution is

similar to that of many of the Entomostraca and other lower

Crustacea (Banarescu, 1991). The distribution pattern of these

crustaceans differs sharply from that of fish, molluscs, etc., and

does not depend on river basins. It seems to reflect climatic

zones. Anostraca, Conchostraca and calanoid Copepoda are

almost entirely confined to temporary water bodies. They have

resistant eggs and are capable of passive dispersal independent

of the riverine network. Consequently, the ‘historical’

hypothesis of medicinal leech distribution can be rejected,

and the recent influence of ecological factors finds further

support.

DISCUSSION

Human impact

One of the most important predictions concerning the

distribution of the medicinal leech and the status of its

populations was that both were greatly affected by human

impact. It is undoubtedly true that leeches were transported all

across Europe, northern Africa and western Asia, and after use

were usually discarded into the nearest ditch or pond (Lukin,

1957, 1976; Sawyer, 1981; Elliott and Tullett, 1992; Hechtel

and Sawyer, 2002). However, the analysed records do not

support the notion of large-scale human impact on the

distribution of any of the four species. Their ranges are

contiguous within the limits of available habitat, and show

surprisingly little overlap. A record of H. verbana in Germany,

nearly 600 km north of its common range, corroborates

that anthropogenic displacements did occur. The leeches had

been released to the wild during times of medicinal use at a

local hospital (C. Grosser, personal communication). Other

irregularities of the distribution at the extreme east of the

ranges of H. medicinalis and H. verbana are more difficult to

attribute to human activity because of the general scarcity of

records in Central Asia. The two documented cases of sympatric

occurrence of H. verbana and H. medicinalis are from remote

areas that were most probably never used for collection or even

release of satiated leeches. Moreover, no sympatric, displaced, or

in any other way suspicious records came from where such

discarding certainly did take place, i.e. in the surroundings of

bigger cities or medical centres. These observations, however, do

not bring any clarity about the fate of those millions of leeches

that were imported, used and discarded in areas far away from

Table 2. Descriptive statistics of environmental variables, as measuredwithin 10km around each locality of the four Hirudo species

T-av[1C]

T-min[1C]

T-se[1C]

P-an[mm]

P-min[mm]

P-se[%]

Hmed min 2.8 �18.7 3.7 487.6 20.8 10.5(n5 461) max 11.3 2.2 11.9 2762.2 122.3 44.9

median 8.0 �5.5 7.5 643.0 30.0 28.3Hver min 2.7 �15.2 5.5 304.3 0.0 14.6(n5 120) max 16.5 6.0 10.2 1300.3 82.4 76.3

median 11.2 �3.4 7.3 662.4 27.3 31.2Htro min 10.1 �5.3 4.9 238.6 1.0 32.5(n5 15) max 17.9 7.6 7.5 1078.9 11.0 81.6

median 15.3 3.1 6.4 559.6 5.1 49.5Hori min 10.1 �9.5 6.5 346.2 0.0 26.4(n5 14) max 15.7 3.0 10.3 1229.3 35.0 75.4

median 13.6 �2.6 8.5 368.3 8.0 52.7

Hmed – H. medicinalis, Hver – H. verbana, Htro – H. troctina, Hori –H. orientalis, T-av – annual mean temperature, T-min – minimaltemperature of the coldest month, T-se – temperature seasonality(standard deviation), P-an – annual precipitation, P-min – precipita-tion of the driest month, P-se – precipitation seasonality (coefficient ofvariation).

S. UTEVSKY ET AL.

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DOI: 10.1002/aqc

their origin. Given the extreme scarcity of such records, the

logical explanation is that those leeches did not survive. In most

instances, leeches from the south (H. troctina and H. verbana)

were imported to countries in northern parts of Europe, where

the local H. medicinalis populations had already been exhausted.

Whether the demise of the newcomers was caused by

unfavourable environmental conditions (for example, low

temperatures) or they were gradually outcompeted by the

better-adapted H. medicinalis, remains open to further

investigation. Notwithstanding, the lack of observable human

influence on the distribution of medicinal leeches presents a

strong case in favour of the ‘ecological’ hypothesis.

Biogeographical considerations

Medicinal leeches, being temporary external parasites, have

better dispersal possibilities than most other true freshwater

animals. Vertebrate hosts can disseminate leeches across land

and sea. The high mobility of their temporary hosts, in

combination with their ability to survive outside water for long

Figure 3. Comparison of environmental parameters as measured within 10 km around each locality of the four Hirudo species. T-av – annual meantemperature, T-min – minimum temperature of the coldest month, T-se – temperature seasonality (standard deviation), P-an – annual precipitation,

P-min – precipitation of the driest month, P-se – precipitation seasonality (coefficient of variation).

DISTRIBUTION AND STATUS OF MEDICINAL LEECHES IN THE WESTERN PALAEARCTIC

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DOI: 10.1002/aqc

periods (Epshtein, 1954; Banarescu, 1991), may explain why

the distributions do not follow any freshwater network or

basin. Instead, it seems that tolerance to ecological restrictions

such as low temperature and aridity, and interspecific

competition, might play more important roles in shaping the

current distributions. It should be noted that the duration of

leech–host contacts outside water is poorly known in natural

conditions. Based mostly on anecdotal reports and field

observations by the authors, some leeches attached to their

hosts for 20min or more, while other researchers reported

an immediate detachment after the host left the water

(Elliott, 2008).

The great extent of mutual exclusivity between ranges of

H. medicinalis and H. verbana is remarkable. A similar pattern

found for entomostracan crustaceans (Banarescu, 1991) is

attributed to the high mobility and ecological tolerance of

Figure 4. Distribution of Hirudo species in relation to annual mean temperature (T-av), temperature of the coldest month (T-min), and temperatureseasonality (T-se).

S. UTEVSKY ET AL.

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DOI: 10.1002/aqc

dormant stages (eggs). The distribution of H. verbana

corresponds to the steppe or eremial province extending

from Central Asia across southern Russia and Ukraine to

the Iberian Peninsula, but, in contrast to entomostracans, its

range does not include Spain and north-western Africa as these

areas are occupied by the vicariant H. troctina. In turn,

H. medicinalis can be assigned to the arboreal faunistic

complex as the range of this species corresponds to areas

initially covered by deciduous tree forests. Hirudo orientalis

can be treated as a south-eastern Euro-Mediterranean species,

reaching into the adjacent zoogeographical regions of western

Asia and high Asia (according to Banarescu, 1991).

Global status assessment

Ever since Sawyer’s (1981) alarming message about the decline

of the medicinal leech, conservation and threats have been two

major issues associated with this taxon. Latent concern

persisted even after Elliott and Tullett (1984) suggested that

the ‘species’ is under no threat of global extinction. Under

Figure 5. Distribution of Hirudo species in relation to total annual precipitation (P-an), precipitation of driest month (P-min), and precipitationseasonality (P-se).

DISTRIBUTION AND STATUS OF MEDICINAL LEECHES IN THE WESTERN PALAEARCTIC

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DOI: 10.1002/aqc

consideration of the new taxonomy, and a substantially larger

body of biological evidence, we conclude that there are no

grounds for assigning any of the four species to the global

IUCN categories Critically Endangered, Endangered, or

Vulnerable (IUCN, 2001). The two most widely spread and

medically applied species, H. medicinalis and H. verbana, occur

throughout their vast ranges where favourable habitats are

available. The same can be anticipated for H. orientalis in spite

of the relative scarcity of information on its occurrence and

biology. All three species prefer stagnant shallow waters with

dense submerged and emergent vegetation, gently sloping

banks, silty bottom and abundant hosts (frogs, cattle, sheep).

However, only some of the water bodies combining all of these

signs are populated by medicinal leeches (Utevsky et al., 2008).

Sporadic occurrence appears to be peculiar to the species of the

genus Hirudo. The scattered records can lead one to conclude

that the leeches are rare. It is hard to say whether the irregular

occurrence has been caused by human activity or is a natural

feature of these animals. The lack of records from Western

Europe, especially for France and Spain, is chiefly a

consequence of sampling inadequacy and thus does not

allow one to derive conclusions about the conservation

status of the medicinal leech there. On the other hand,

central and eastern Europe seem to offer lots of favourable

habitat for H. medicinalis and H. verbana, whereas the

Caucasus and Central Asian mountains harbour a number of

viable populations of H. orientalis. Little is known about the

distribution and status of H. troctina in its range in north-

western Africa and the Iberian Peninsula, not permitting

precise conservation status assessment. The appropriate

assignment for this species is therefore Data Deficient

(IUCN, 2001).

In spite of the optimistic conclusions about the overall

status of different Hirudo species, at least some of them

can be definitely endangered locally by collecting pressure. For

example, an estimated four-fold decline was observed from

2000 to 2004 in the Krasnodar Territory (Russian Federation),

a traditional area of commercial harvesting of the medicinal

leech (probably H. verbana) (Kamenev, 2006). However, on a

global scale the data obtained suggest neither a reduction in

population sizes nor a decline in the geographical ranges in

comparison with previous records (Lukin, 1957; Elliott and

Tullett, 1984). On the other hand, the potential and actual loss

of wetland habitats, the global decline of amphibians (Beebee

and Griffiths, 2005; Cushman, 2006), abandonment of

traditional grazing practices and the scarcity of mammalian

Figure 6. Distribution of Hirudo species in relation to major landscape types (adapted from Isachenko and Shlyapnikov, 1989). Numbers refer to:1 – Mediterranean landscapes, 2 – subtropic moist arboreal landscapes, 3 – deciduous arboreal landscapes, 4 – forest steppe landscapes, 5 – sub-boreal steppe landscapes, 6 – sub-boreal semi-eremial landscapes, 7 – sub-boreal eremial landscapes, 8 – subtropic eremial-steppe and eremiallandscapes, 9 – sub-taiga landscapes, 10 – taiga landscapes, 11 – forest tundra landscapes, 12 – tundra landscapes. The parts in northern Africa were

not mapped in the used source (grey), but they can be regarded as parts of Mediterranean landscapes.

Table 3. Comparisons of environmental variables, as measured within10 km around each locality, among all four Hirudo species andseparately for the pair H. medicinalis and H. verbana

Environmentalvariable

Amongfourspecies

H. medicinalis - H. verbana

w2 Mann-Whitney U Kolmogorov-Smirnov Z

T-av 206.9� 7938.5� 6.8�

T-min 26.2� 17580.5� 3.4�

T-se 68.7� 26566.5 (p5 0.504) 1.8 (p5 0.002)P-an 21.5� 25053.5 (p5 0.112) 2.5�

P-min 87.3� 20446.5� 3.3�

P-se 75.2� 20664.5� 3.0�

�Significant at po0.001.T-av – annual mean temperature, T-min – minimal temperature of thecoldest month, T-se – temperature seasonality (standard deviation), P-an – annual precipitation, P-min – precipitation of the driest month,P-se – precipitation seasonality (coefficient of variation).

S. UTEVSKY ET AL.

Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. (2009)

DOI: 10.1002/aqc

blood in leech diet (Elliott, 2008) are likely to affect

populations and geographical ranges. Indeed, it seems very

likely that such losses have already happened, but have

remained unnoticed because of the lack of field research and/

or taxonomic expertise. Our own observations on recent

collecting trips in the Kharkiv Region (Ukraine) were that

drained and agriculturally ameliorated stretches of alluvial

plains were devoid of medicinal leeches. Although more

research is needed to estimate the true impact on habitat

alteration, this adds to the array of real or potential threats.

We therefore believe that H. medicinalis, H. verbana and H.

orientalis are close to qualifying, or are likely to qualify, for a

threatened category in the near future, and therefore propose

listing them as Near Threatened (IUCN, 2001).

ACKNOWLEDGEMENTS

We thank Abdumalik Abdullaev, Erkin Abdullaev, Raja Ben

Ahmed, Matjaz Bedjanic, Vasily Dyadichko, Clemens

Grosser, Mair Huseynov, Sergey Il’inov, Sergey Kolechkin,

Alessandro Minelli, Hasko Nesemann, Boris Sket, Bahadir

Ugural, Heinrich Vicentini, Oleksandr Voloshkevych and

Magdalene Westendorff for providing information on the

distribution of medicinal leeches, and Miguel Villena Sanchez-

Valero and Javier Sanchez Almazan for lending the specimens

from the Museo Nacional de Ciencias Naturales, Madrid. The

work was supported by INTAS through grant No. 05-

1000008-8147 entitled ‘The medicinal leech (Hirudo spp.),

famous and unknown: taxonomy, conservation, and medical

applications’, and by grants from the Slovenian–Ukrainian

Intergovernmental Science & Technology Cooperation

Programme.

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