Biologia 69/4: 484—488, 2014 Section Zoology DOI: 10.2478/s11756-014-0329-0
Occurrence of the medicinal leech (Hirudo medicinalis) in birds’ nests ´ski1, Grzegorz Ton ´czyk2, Aleksander Bielecki3, Joanna M. Cichocka3, Pawel Buczyn Ignacy Kitowski4, Grzegorz Grzywaczewski5, Rafal Krawczyk 6, Marek Nieoczym5, ´ska2, Joanna Pakulnicka7 & Edyta Buczyn ´ska5 Aleksandra Jablon 1
Department of Zoology, Maria Curie-Sklodowska University, Akademicka Str. 19, 20-033 Lublin, Poland; e-mail:
[email protected] 2 Department of Invertebrate Zoology and Hydrobiology, University of L ód´z, Banacha Str. 12/16, 90-237 L ód´z, Poland; e-mail:
[email protected],
[email protected] 3 Department of Zoology, University of Warmia and Mazury, Oczapowskiego Str. 5, 10-718 Olsztyn, Poland; e-mail:
[email protected],
[email protected] 4 State School of Higher Education in Chelm, Pocztowa Str. 54, PL 22-100 Chelm, Poland; e-mail:
[email protected] 5 Department of Zoology, Animal Ecology and Wildlife Management, University of Life Sciences in Lublin, Akademicka Str. 13, 20-031 Lublin, Poland; e-mail:
[email protected],
[email protected],
[email protected] 6 Department of Nature Conservation, Maria Curie-Sklodowska University, Akademicka Str. 19, 20-033 Lublin, Poland; e-mail:
[email protected] 7 Department of Ecology and Nature Protection, University of Warmia and Mazury, Oczapowskiego Str. 5, 10-957 Olsztyn, Poland; e-mail:
[email protected]
Abstract: Occurrence and breeding of Hirudo medicinalis were recorded in birds’ nests in the fishing ponds and water bodies used extensively by anglers in south-eastern Poland, in 4 of 11 studied bird species (Circus aeruginosus, Fulica atra, Cygnus olor, Chroicocephalus ridibundus). Factors important for the distribution and density of this leech were: nest height, pH of the water and oxygen concentration in the water inside the nests, the body-length of the nesting birds. Our data show that (1) H. medicinalis chooses nests as habitats that are safe in water bodies rich in predators (particularly fish) and provide stable feeding conditions; (2) fishing ponds and other water bodies used extensively by anglers in a landscape modified by human pressure can be an important secondary habitat for the medicinal leech. As the nesting activity of some aquatic birds apparently favors the occurrence of H. medicinalis, active protection of aquatic birds and creating sites appropriate for their breeding may be an indirect way for the conservation of the leech in such areas. Key words: Hirudo medicinalis; birds’ nests; colonisation; refugium; conservation
Introduction Hirudo medicinalis L., 1758 is a leech commonly studied, e.g., for its influence on populations of vertebrates, sensibility to water pollution, use in environmental monitoring, and its role in medicine and associated exploitation of natural populations. Most data come from natural waters of high environmental quality, which are usually in focus of such studies, particularly those of inventory or monitoring character (e.g., Kasparek et al. 2000). However, equally interesting yet scarce data come from the waters heavily modified by humans or even artificial, often characterised by a strong pressure from fish predators and eutrophication (Buczy´ nski et al. 2008; Bielecki et al. 2011). Colonisation of such habitats proves the species adaptation to anthropogenic changes. Recently it appeared that H. medicinalis colonizes very specific and so far scarcely studied littoral microhabitats – nests of aquatic birds (Buczy´ nski et al. 2008;
c 2014 Institute of Zoology, Slovak Academy of Sciences
McConnell 2000, unpublished report). It is an important phenomenon as the nests may be an important refugium for the leech, limiting the predatory impact from fish. The aim of the present study is to analyse the distribution of medicinal leech in birds’ nests in fishing ponds and in water bodies used by anglers in relation to environmental factors. Material and methods The studies were conducted in July in seasons 2007–2008. The material was sampled in 45 nests of 11 bird species: great crested grebe Podiceps cristatus (L., 1758) (5 nests), red-necked grebe Podiceps grisegena (Boddaert, 1783) (2), black-necked grebe Podiceps nigricollis (C.L. Brehm, 1831) (1), mute swan Cygnus olor (Gmelin, 1789) (5), western marsh harrier Circus aeruginosus (L., 1758) (5), Eurasian coot Fulica atra L., 1758 (6), common gull Larus canus (L., 1758) (1), black-headed gull Chroicocephalus ridibundus (L., 1766) (5), whiskered tern Chlidonias hybrida (Pallas, 1811)
Hirudo medicinalis in birds’ nests
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Table 1. The occurrence of H. medicinalis in studied bird nests. Bird species
Site
Date
Nn
Ni
Nc
L
Cygnus olor
Garbów
18.VII.2007
1
22* (7.3)
8 (2.6)
d
Fulica atra
Garbów Garbów Garbów
18.VII.2007 18.VII.2007 18.VII.2007
4 4 4
1 (0.3) 1 (0.3) 1 (0.6)
2 (0.6) 3 (1.0) –
d d d
Chroicocephalus ridibundus
Garbów
11.VII.2008
5
1 (0.3)
–
e
Czeslawice Zalesie Krasze´ nskie Niemienice
18.VII.2007 17.VII.2007 16.VII.2007
1 3 1
1 (0.6) 1 (0.6) 3 (1.0)
11 (7.3) 2 (2.0) 6 (2.0)
w d d
Circus aeruginosus
Explanations: Nn – number of nests with medicinal leeches; Ni – total number and density of individuals; Nc – total number and density of cocoons; L – layer of a nest: d – dry, e – entire nest (wet), w – wet. *while taking the samples in littoral additional 8 individuals attached to the investigator’s legs.
(5), black tern Chlidonias niger (L., 1758) (5) and common tern Sterna hirundo L., 1758 (5). The material was collected on 11 sampling sites in the Lublin District (eastern Poland, 50◦ 58 –51◦ 37 N, 22◦ 19 –23◦ 34 E): Garbów, Czeslawice, Samokl˛eski, Brus Stary, Wytyczno, Zahajki Kolonia, Zalesie Krasze´ nskie, ˙ lta´ Niemienice, Zó nce, Ignatów, and Sta´ nków. All the studied nests came from highly eutrophic or polytrophic waters (fishing and retention ponds, karst sinkhole). In the fishing ponds, intensive carp (Cyprinus carpio L., 1758) cultures were kept, other ponds were also constantly stocked by anglers with carp, pike Esox lucius L., 1758, tench Tinca tinca (L., 1758) and crucian carp Carassius carassius (L., 1758). The dimensions of nests were measured with respect to the height of their submerged and emerging parts. Several samples of volume of ca. 3 dm3 were collected from each nest, depending on its size and structural complexity. From the nests of western marsh harrier and mute swan, the samples were collected separately from three layers: emerging dry layer, emerging wet layer and submerged layer. Samples of two layers were collected from the nests of Eurasian coot and grebes: emerging wet layer and submerged layer. Each sample was collected in a way to avoid overlooking any leech that can run away very fast. After removing first layer of a nest one could see leeches in the narrow layer inside the nest. Samples were collected by hand and placed in the bucket. If small, the entire nests were collected. Around the nests, samples were collected with a benthic net from a surface of ca. 1 m2 , in the distance of 1 m and 5 m from the nest. The samples were conserved on the collection site in 5% formaldehyde solution. In laboratory volume of the sample was measured and each sample was washed on the sieve column (mesh: 0.5, 2.0 and 10.0 mm) and then sorted. The organisms were then fixed in 70% ethanol and identified with stereomicroscope Olympus SZ-ST. Maturity of the leeches was estimated by measuring and dissecting of some specimens. It was noted if alimentary tracts of the leeches were filled with blood and what was physiological condition of the ovaries. In the nests and around the nests we measured water temperature, conductivity, pH and oxygen concentration. All the measures were done with the multifunctional device Elmetron CX401 with conductivity probe EC-60, pH probe EPP-1 and oxygen probe COG-1. For the statistical analyses, we used Student t-test and Spearman’s rank coefficient (rS ). All means ± SD are given. All the standard measures of bird size were accepted after Busse (1990).
Fig. 1. Individuals of Hirudo medicinalis collected in the nest of Circus aeruginosus (Niemienice, July 16, 2007).
Results Hirudo medicinalis (Fig. 1) was found altogether in 8 nests and samples (Table 1). It occurred in four pond complexes (36.4%). No leeches were found in the samples from vicinity of the nests. They were present only in eight nests (17.8%) – altogether 32 mature individuals were found. Mean length and width of the leech body were 85 mm and 17 mm, respectively. Moreover, the alimentary tracts of examined leeches were prominently filled with blood. Most of the nests inhabited by the leeches were found in Garbów (5 nests, 44% of all nests studied in this location). In other locations the medicinal leech was found only in single nests. Most of the nests inhabited by the leech belonged to western marsh harrier (3 nests) and Eurasian coot (3). The leeches were found in single nests of mute swan and black-headed gull. The leeches were found usually in the dry layer (6 of the 8 nests, 75%), less frequently (2 of the 8 nests, 25%) in the wet layer, yet always close to
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486
Fig. 2. Cocoon of the medicinal leech deposited in a nest of Fulica atra (Garbów, 17 July 2007), not cemented to plant substrate.
the borderline between these two layers (Table 1). Also, the highest densities of leeches were found in the dry layer. No medicinal leeches were found in the submerged layer of the studied nests. Moreover, in observed nests cocoons of the medicinal leech were found (Fig. 2). The highest total number of cocoons (11) was recorded in the wet layer of the western marsh harrier’s nest in Czeslawice. In nests of black headed gull and Eurasian coot none or only 2 cocoons were recorded, respectively (Table 1). Statistically significant differences were found for three variables describing conditions in the nest colonised and not colonised by the leech: height of the nests (0.525 ± 0.289 m and 0.326 ± 0.230 m, respectively, t = 2.124, df = 43, P = 0.003); pH of the water inside the nest (6.71 ± 1.18 and 8.53 ± 1.76, respectively, t = 2.772, df = 43, P = 0.008); dissolved oxygen concentration in the water inside the nest (2.00 ± 1.11 mg dm−3 and 3.753 ± 2.32 mg dm−3 , respectively, t = 2.00, df = 43, P = 0.045). No statistically significant differences were found for water conductivity (t = 2.005, df = 43, P = 0.133), however, on average it was higher by 100 units in nests colonised by the leech (mean 612 µS dm−3 ) versus those that were not colonised (mean 512 µS dm−3 ). In the colonised nests, a highly significant correlation was found between the length of the birds and density of leeches in their nests: rS = 0.864, P = 0.006. The dimensions of nests colonised by the leech as well as physical-chemical parameters of water inside the nests did not correlate significantly with leech density (e.g., nest diameter: rS = 0.506, P = 0.201; conductivity: rS = –0.445, P = 0.270; dissolved oxygen concentration: rS = 0.228, P = 0.587).
Discussion Hirudo medicinalis may suck blood of all vertebrate animals. It feeds very often on mammals, amphibians and fish, while data on attacking reptiles and birds are rather scarce (Lukin 1976; Sawyer 1986). The leech may, in rare cases, parasitize nestlings fallen from nests to water. Nevertheless, such data are scarce as the findings of the leech on birds are very rare (Herter 1936). Although Herter (1936) assumed that occurrence of leeches on nestlings, which fell out of the nest, was casual, his information was the first hint for studying nests of aquatic birds. However, no-one have undertaken the study for over 70 years. Most of the medicinal leeches we found in nests, occurred in their dry layer yet close to its border with the wet layer (Table 1). The leeches usually lay their cocoons in epilittoral, on the border of water and land, in wet soil (Lukin 1976). In nests, the water evaporating from below apparently maintains enough humidity to prevent the leech and the cocoons from drying. Interesting is the occurrence of cocoons in dry layer. Apart of one finding of the leech in the wet layer, the cocoons were not found there – it proves that the cocoons are laid on the border of the layers, yet in the dry layer. Apparently, there is a correlation between the life cycle of the leech and of the birds (e.g., western marsh harrier, Eurasian coot and mute swan). Thus, the young leeches are secure with respect to feeding. In most nests no cocoons were found – possibly the leeches did not lay the cocoons yet. The time between feeding and deposition of cocoons takes 30–60 days, thus the leeches lay cocoons in July and August, and even in October and November in warmer regions (Sawyer 1986). Our
Hirudo medicinalis in birds’ nests study was conducted in July – at the beginning of the breeding season of H. medicinalis (Lukin 1976; Sawyer 1986). Thus, we suppose that the deposition of cocoons and hatching of this population of the leech is extended to August or further months. Measurements and dissections of some of collected specimens have confirmed our presumption that leeches were mature and ready to breed. Although their body lengths were slightly lower (71.5–97.2 mm), their bodies were wider (13.7–22.2 mm) than in literature data (100– 150 mm in length and 10 mm in width – Pawlowski 1936; Sawyer 1986). It could result from the fixation method, causing a significant contraction under impact of concentrated ethanol. Moreover, the ratio of the greatest length to the greatest width of the body (7.2–17.2/13.7–22.2 mm) has indicated a significant fulfilment of alimentary tract with blood – the leeches were cylindrical rather than flatted. Dissection of the specimens revealed free oocytes in ovisacs, which indicate readiness for fertilization (Ben Ahmed et al. 2010; ´ atek unpubl. data). It is very important for reproSwi˛ ductive success that leeches should feed in the period from May to July. Blood stimulates the leeches to copulate and initiates maturation of ovaries. It is impossible that the cocoons of leeches might be transferred with vegetation used in construction of those nests because the birds of studied species build their nests from mid March to mid April (Buczek & Keller 1994; Witkowski 1989). The occurrence of the cocoon of medicinal leech accompanied by 10 individuals in a moorhen’s nest was also reported by McConnell (2000, unpublished report). Moreover, the cocoons are not cemented to the substrate so they could be lost during transfer of plant material by birds. In nests colonized by the leech, a strong correlation between the bird body length and density of leeches was found. Bigger birds have bigger body surface and are emitting stronger thermal, chemical and mechanical signals, which are well sensed by the leech – hence there are more leeches in nests of bigger birds. However, no significant dependence was found between the sizes of nests colonised by the medicinal leech and density of individuals, yet the values or rS coefficient were highest for the nest diameter. That suggests a straight relation between the nest size (and thus the size of nesting birds) and leech density. Possibly, further studies based on larger sample sizes will reveal such statistically significant dependence. We can assume that nests of western marsh harrier are important secondary habitat for the medicinal leech. A difference between breeding of marsh harrier and three other studied species (Eurasian coot, mute swan and black-headed gull) in which leeches were found, lays mainly in the fact that the chicks of swans and Eurasian coots are able to abandon the nests relatively shortly after hatching. They are precocial birds in contrary to western marsh harrier which represents altricial birds with the chicks staying essentially longer at the nests (Busse 1990). The size of the bird and its nest as well as breeding
487 behaviour are factors influencing the selection of a nest by the medicinal leech in order to complete the life cycle. It should be pointed out that during food shortage, a strong sibling competition occurs in the harrier’s nest. As a result the weakest nestlings are usually wounded and eventually die, and before death they might easily become hosts for the leeches. The important role plays the bird female staying in a nest and incubating eggs for 31–38 days and then brooding the nestlings for even 2.5 weeks. It may be an easily accessible food source for the leeches, particularly at night. Moreover the nestlings covered only by a thin layer of down feathers may be parasitized – especially that altogether they stay in the nest for 35–44 days since hatching (Cramp 1980). Eurasian coot and the mute swan feed primarily on plants and are not able to offer the medicinal leech anything else but their own bodies. Most probably important is the fact that the nest is built on water so it may be easily attacked by the leeches. Both species show r-strategy in their life cycles – they have high number of offspring. The Eurasian coot may even produce two broods per year (Cramp 1980). Besides, both species build platforms serving the nestlings and adult birds for resting (Cramp 1980; Cramp & Simmons 1977). The platforms may be also used by leeches for laying cocoons. Mute swans incubate their eggs for ca. 7 weeks and the Eurasian coot only for ca. 3.5 weeks (Cramp 1980). This time may be used by leeches to parasitize the birds at night. To understand the role of Eurasian coot nests for medicinal leeches, one has to take into account one more aspect of the species ecology – the nests are usually constructed from dead and live plants found opportunistically by adult birds near the nesting site (Cramp 1980). However, the studies performed on two sites distant from each other show the same pattern – the larger nest, the easier it is to find a shelter from predators for the leech (Koshelev 1984; Rizi et al. 1999). If the birds use more rigid construction material, they build larger nests. In our study the leeches were found only in large nests of Eurasian coot. The nests of black-headed gulls are less important for the leech, however, it is more beneficial for the leeches if the gulls locate their nests on the water and not on the islands. Besides, black-headed gull is a typical precocial species. Thus, as in case of other gulls, terns and grebes, it may limit the use of nestlings as a food source by the leeches. The highest density of leech cocoons (7.3; Table 1) was recorded in the harrier’s nest in Czeslawice, and the lowest density of cocoons was noticed in the Eurasian coot’s and black-headed gull nests in Garbów (0.6 or none; Table 1). These observations also may results from the information about behaviour of the studied birds given above. Recently, it was suggested that most likely fast and efficient dispersal of medicinal leeches occurs by their mammalian hosts, for example cattle, as vectors of leech transfer between water reservoirs (Utevsky et al. 2010; Trontelj & Utevsky 2012). Our study suggests
488 that birds may play an important role in spreading of medicinal leech. Such possibility has not been taken into account until now. The results of studies by Utevsky et al. (2010) and Trontelj & Utevsky (2012) shed light on the cause of the genetic uniformity of medicinal leeches on vast areas, and this phenomenon can be explained by leech parasitism on birds and the dissemination of leeches by their bird hosts. Projecting the nesting area of the western marsh harrier over the distribution range of the leech shows that they overlap to a great extent. Such great overlap is not observed for the nesting area of Eurasian coot, mute swan and black-headed gull (Cramp & Simmons 1977; Minelli 2010; Utevsky et al. 2010). Our data corroborate the hypothesis that the fishing ponds and waters intensively used by anglers are important secondary habitats for the medicinal leech – species protected by law and endangered in many countries (e.g., category VU in Poland – Ja˙zd˙zewska & Wiede´ nska 2004). We can also assume that the nesting of aquatic birds favours presence of the leech, hence creating and maintaining proper conditions (e.g., reed belts) is an indirect way to protect the leech. Acknowledgements This study was supported by the Ministry of Science and Higher Education of the Republic of Poland (grant no. N304 109 31/3813). References ´ atek Ben Ahmed R., Fuchs A.Z., Tekaya S., Harrath A.H. & Swi˛ P. 2010. Ovary cords organization in Hirudo troctina Johnson, 1816 and Limnatis nilotica (Savigny, 1822) (Clitellata, Hirudinea). Zool. Anz. 249 (3-4): 201–207. DOI: 10.1016/j.jcz.2010.08.004 ´ atek P., Cichocka J.M., Ropelewska E., Jele´ Bielecki A., Swi˛ n I. & ˙ 2011. Pijawki (Hirudinea) wód powierzchAdamiak-Brud Z. niowych Olsztyna. Forum Faun. 1 (1): 12–34. Buczek T. & Keller M. 1994. Breeding ecology of the Marsh harrier Circus aeruginosus in eastern Poland. Part I. Population numbers and phenology of the onset of laying. Acta Ornithol. 29 (2): 67–80. Buczy´ nski P., D˛abkowski P., Zawal A., To´ nczyk G., Jaskula R., Grabowski M., Buczy´ nska E., Lewandowski K., Janicki D., Cios S., Pietrzak L., Mrowi´ nski P., Pakulnicka J., Guzik M. & Jablo´ nska A. 2008. Occurrence and threats of the medicinal leech (Hirudo medicinalis L.) in Poland (Annelida: Hirudinea). Fragm. Faun. 51 (2): 79–89.
´ski et al. P. Buczyn Busse P. 1990. Maly slownik zoologiczny. Ptaki. Tom 1, 2. Wiedza Powszechna, Warszawa, 801 pp. ISBN: 83-214-0563-0 Cramp S.1980. Handbook of the Birds of Europe, the Middle East and North Africa. Vol. 2. Hawks to Bustards. Oxford University Press, Oxford, 687 pp. ISBN-10: 019857505X, ISBN-13: 978-0198575054 Cramp S. & Simmons K. 1977. Handbook of the Birds of Europe, the Middle East and North Africa. The Birds of the Western Palearctic. Vol. 1. Ostrich to Ducks. Oxford University Press, Oxford, 722 pp. ISBN: 0-19-857358-8 Herter K. 1936. Die Physiologie der Hirudineen, pp. 123–319. In: Bronn H.G. & Autrum H. (eds), Klassen und Ordnungen des Tierreichs, Bd 4. Abt.3. Buch 4, Hirudineen, Teil 2, 4 lieferung, Akademische Verlagsgesellschaft M.B.H., Leipzig, 622 pp. Ja˙zd˙zewska T. & Wiede´ nska J. 2004. Hirudo medicinalis Linnaeus, 1758, pp. 33–34. In: Glowaci´ nski Z. & Nowacki J. (eds), Polska czerwona ksi˛ega zwierz˛at, Tom 2, Bezkr˛egowce, Instytut Ochrony Przyrody PAN, Akademia Rolnicza im. Augusta Cieszkowskiego, Kraków – Pozna´ n, 447 pp. ISBN: 83-8893460-0 Kasparek M., Demirsoy A., Akbulut A., Akbulut N.E., C ¸ ali¸skan M. & Durmu¸s Y. 2000. Distribution and status of the medicinal leech (Hirudo medicinalis L.) in Turkey. Hydrobiologia 441 (1): 37–44. DOI: 10.1023/A:1017555322002 Koshelev A.I. 1984. Lysukha v Zapadnoi Sibiri (ekologiya, povedenie i khozyaistvennoe znachenie). Nauka, Novosibirsk, 175 pp. Lukin E.J. 1976. Piyavki presnykh i solonovatykh vodoemov. Fauna SSSR. Piyavki. T. 1. Izdatelstvo Nauka, Leningrad, 484 pp. Minelli A. 2010. Fauna Europaea: Hirudinidae. In: Fauna Europaea, Version 2.4. http://www.faunaeur.org (accessed 09.07.2010) Pawlowski L.K. 1936. Pijawki (Hirudinea). Fauna slodkowodna Polski, Z. 26, Wyd. Kasy Imienia Mianowskiego Instytutu Popierania Nauki, Warszawa, 176 pp. Rizi H., Benyacoub S., Chabi Y. & Banbura J. 1999. Nesting and reproductive characteristics of Coots Fulica atra breeding on two lakes in Algeria. Ardeola 46 (2): 179–186. Sawyer R.T. 1986. Leech Biology and Behaviour. Vol. I, II, III. Clarendon Press, Oxford, 1065 pp. ISBN I.: 0198573774, 9780198573777, ISBN II.: 0198576226, 9780198576228, ISBN III.: 0198576234, 9780198576235 Trontelj P. & Utevsky S.2012. Phylogeny and phylogeography of medicinal leeches (genus Hirudo): Fast dispersal and shallow genetic structure. Mol. Phylogenet. Evol. 63: 475–485. DOI: 10.1016/j.ympev.2012.01.022 Utevsky S., Zagmajster M., Atemasov A., Zinenko O., Utevska O., Utevsky A. & Trontelj P. 2010. Distribution and status of medicinal leeches (genus Hirudo) in the Western Palaearctic: anthropogenic, ecological, or historical effects? Aquat. Conserv. Mar. Freshwater Ecosyst. 20 (2): 198–210. DOI: 10.1002/aqc.1071 Witkowski J. 1989. Breeding biology and ecology of the Marsh Harrier Circus aeruginosus in the Barycz valley, Poland. Acta Ornithol. 25 (3): 223–320. Received January 24, 2013 Accepted December 7, 2013
