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Interactions Between the Leech Helobdella Stagnalis (Linnaeus, 1758) and Amphibians: New Data from Poland

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Interactions Between the Leech Helobdella Stagnalis (Linnaeus, 1758) and Amphibians: New Data from Poland Herpetology Notes, volume 13: 1009-1012 (2020) (published online on 10 December 2020) Interactions between the leech Helobdella stagnalis (Linnaeus, 1758) and amphibians: new data from Poland Agata Starzecka1, Krzysztof Kolenda2, and Natalia Kuśmierek3,* Trophic relationships between amphibians and feature is the presence of a dark chitinized anterior leeches include parasitism on adult amphibians and scute, which allows this species to be easily identified larvae, as well as predation on adults, larvae and eggs (Fig. 1A; Sawyer, 1986; Kołodziejczyk and Koperski, (Mann and Tyler, 1963; Berven and Boltz, 2001; Schalk 2000). Another unusual feature of H. stagnalis, and et al., 2002; Burgin and Schell, 2005; Kutschera et al., glossiphoniids in general, is advanced parental care 2010; Elliott and Kutschera, 2011). Such interactions (Fig. 1B). Leeches lay eggs in special cocoons attached can sometimes cause declines in local amphibian to the ventral side of their body and oxygenated with populations (Brockelman, 1969; Merilä and Sterner, undulating body movements. After hatching, young 2002; Burgin and Schell, 2005). Leeches also serve leeches stay in these cocoons for about four weeks, as a vector of pathogens, including Ichthyophonus sp. using posterior suction to remain attached. During that or Trypanosoma pipientis (Siddall and Desser, 1992; period, the parent feeds its young with hunted prey Raffel et al., 2007). There are also reports of a mimetic (Kutschera and Wirtz, 2001). (McCallum et al., 2008) as well as phoretic relationship Although Helobdella is considered not to feed on blood between these two groups (Khan and Frick, 1997; (Siddall and Borda, 2003), its presence on amphibians Maia-Carneiro et al., 2012). However, in many cases has been noted several times. Surprisingly, a report determination of specific interactions is problematic on the observation of H. stagnalis on a common frog (Gandola and Hendry, 2014; Zimić, 2015). (Rana temporaria) in Italy, was described as a definite The Glossiphoniidae (Order Rhynchobdellida) case of parasitism due to the presence of skin abrasions, family includes predatory species that feed on the haemorrhages, and melanophore accumulations, haemolymph of invertebrates as well as blood parasites coupled with local dermic inflammation (Tiberti and of amphibians and reptiles (Siddall et al., 2005). One Gentili, 2010). Similarly, Platt et al. (1993) suggested of the most widespread species is Helobdella stagnalis a parasitic relationship with the tiger salamander, (Linnaeus, 1758). As a freshwater predator, this species Ambystoma tigrinum, in the United States, but their mainly feeds on oligochaetes, insect larvae, and aquatic assumption was based only on the documentation snails (Sawyer, 1986; Haaren et al., 2004). Helobdella of an accumulation of leeches in the body areas with stagnalis is a small-sized leech (10-12 mm length) with lymph nodes. Other cases, including the smooth newt one pair of eyes and a flattened body. Their characteristic (Lissotriton vulgaris) in Ireland (Gandola and Hendry, 2014), the yellow-bellied toad (Bombina variegata) in Bosnia and Hercegovina (Zimić, 2015), and the common spadefoot (Pelobates fuscus) and the palmate newt (Lissotriton helveticus) in the Netherlands (Struijk and Heijden, 2015; Stark et al., 2017), considered these 1 Stawowa 11, 43-400 Cieszyn, Poland. interactions as parasitism or phoresy but did not present 2 Amphibian Biology Group, Department of Evolutionary Biology any clear evidence of parasitism. Here, we present and Conservation of Vertebrates, Institute of Environmental another report of interaction between H. stagnalis and Biology, University of Wrocław, Sienkiewicza 21, 50-335 amphibians, showing for the first time the occurrence of Wrocław, Poland. this leech on several species that inhabit a single pond 3 Department of Parasitology, Institute of Genetics and Microbiology, University of Wrocław, Przybyszewskiego 63, and extending the recorded host list by three species. 51-148 Wrocław, Poland. During a herpetological monitoring survey carried out * Corresponding author. E-mail: [email protected] in 2018–19 in the Silesian Foothills (southern Poland), 1010 Agata Starzecka et al. Figure 1. Helobdella stagnalis: A – with a dark chitinized anterior scute, B – carrying their offspring, C – on Bufo bufo, D – on Ichthyosaura alpestris, E – on Lissotriton vulgaris, F – on Triturus cristatus. Photos by N. Kuśmierek (A, B), K. Kolenda (C, D), A. Starzecka (E, F). leeches were found on amphibians in a mid-forest pond on seven smooth newts (30%), eight great crested newts located in the Jasieniowa mountain range (49.7247, (25%), three alpine newts (21.4%), both of the common 18.7258, elevation 424 m). During six visits, we caught toads (100%), and none of water frogs (0%). The number a total of 81 amphibians, including 32 great crested of leeches per individual varied from one to more than newts (Triturus cristatus), 23 smooth newts (Lissotriton ten, and no differences in leech number by taxon were vulgaris), 17 alpine newts (Ichthyosaura alpestris), observed. They were located on limbs, the head, the seven water frogs (Pelophylax esculentus complex), and tail, and the ventral and dorsal sides of the hosts; some two common toads (Bufo bufo). Leeches were observed individuals were actively moving (Fig. 1C–F). Around on 20 individuals (total prevalence 24.7%), specifically 20 leeches were detached, preserved in 70% alcohol, Interactions between the leech Helobdella stagnalis and amphibians 1011 and deposited in the collection of the Department of H. stagnalis on amphibians, and that it extends the of Parasitology, University of Wrocław. They were list of amphibian species that can carry this leech. identified as H. stagnalis based on the available key to According to our observations and most reports from freshwater invertebrates (Kołodziejczyk and Koperski, the existing literature, we suggest that phoresy is the 2000). main interaction linking H. stagnalis and amphibians, During our observations, we did not find any symptoms but facultative parasitism under certain conditions of parasitism, such as skin lesions or haemorrhages, cannot be completely excluded. in the areas where the leeches were attached. As a consequence, we classified the interaction between Acknowledgements. We thank Jan M. Kaczmarek for providing these leeches and their amphibian hosts as phoresy. a pre-peer review of this note and anonymous reviewer for Attachment to amphibian skin enables leeches to easily constructive remarks. Tomasz Beczała helped with the fieldwork. Amphibian capturing and handling was performed under permit disperse through the water, increasing the possibility of from the Regional Directorate of Environmental Protection in finding mates or locations rich in prey. It also provides Katowice (permission no. WPN.6401.611.2017.TL.1). an opportunity for migration between water bodies. Phoresy may also protect attached adults and their eggs/ References young against attack from predators. This supposition is supported by the fact that the amphibian presence in Berven, K., Boltz, R. (2001): Interactive effects of leech (Desserobdella picta) infection on Wood Frog (Rana sylvatica) water bodies overlapped with the breeding and parental tadpole fitness traits. Copeia 2001: 907–915. care period of leeches. Indeed, we observed attached Brockelman, W.Y. (1969): An analysis of density effects and leeches caring for their offspring as well as self- predation in Bufo americanus tadpoles. Ecology 50: 632–644. sufficient young. Burgin, S., Schell, C.B. (2005): Frog eggs: unique food source for Observations of H. stagnalis on other ectothermic leech Bassianobdella fusca. Acta Zoologica Sinica 5: 344–348. vertebrates, such as the snapping turtle (Chelydra Elliott, J.M., Kutschera, U. (2011): Medicinal leeches: historical serpentina) and common musk turtle (Sternotherus use, ecology, genetics and conservation. Freshwater Reviews 4: odoratus) in the United States, also suggest a phoretic 21–41. Gandola, R., Hendry, C. (2014): Lissotriton vulgaris (smooth newt): relationship (Richardson et al., 2015). Additionally, parasitism or phoresy? Herpetological Bulletin 128: 22–23. molecular analyses of the stomach contents of leeches Haaren, T. van, Hop, H., Soes, M., Tempelman, D. (2004): The attached to a Sicilian pond turtle (Emys trinacris) freshwater leeches (Hirudinea) of The Netherlands. Lauterbornia excluded parasitism (Marrone et al., 2016). There are 52: 113–131. also known cases of other leeches using amphibians Khan, R.N., Frick, M. (1997): Erpobdella punctata (Hirudinea: as possible shelter and/or conveyance. Erpobdella Erpobdellidae) as phoronts on Ambystoma maculatum punctata was hosted on the spotted salamander (Amphibia: Ambystomatidae). Journal of Natural History 31: 157–161. (Ambystoma maculatum) and fed on the remains of prey Kolenda, K., Najbar, A., Kuśmierek, N., Maltz, T.K. (2017): A eaten by their amphibian host (Khan and Frick, 1997). possible phoretic relationship between snails and amphibians. Unidentified leeches were also found on neotropical Folia Malacologica 25: 281–285. toads (Rhinella abei), which were free of wounds or Kołodziejczyk, A., Koperski, P. (2000): Bezkręgowce słodkowodne scars, and the leeches empty of blood (Maia-Carneiro et Polski. Klucz do oznaczania oraz podstawy biologii i ekologii al., 2012). It is also noteworthy that amphibians can be a makrofauny. Warszawa, Polska, Wydawnictwo host for many other phoronts such
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