First Record of Phoresy Or Possible Parasitism by the Fresh Water Leech

Herpetology Notes, volume 10: 717-719 (2017) (published online on 08 December 2017)

First record of phoresy or possible parasitism by the fresh water leech Helobdella stagnalis (Glossiphoniidae) on Lissotriton helveticus (Caudata: Salamandridae) in the Netherlands

Tariq Stark1,*, David Brouwer2, Remco Ploeg2 and Ton Lenders3

Leeches often share the same (aquatic) habitat as (Platt et al., 1993; Tiberti and Gentilli, 2010; Gandola amphibians, in which they may predate or parasitize and Hendry, 2014; Zimić, 2015). In addition, a male anurans and urodelans, or use them as a means of common spadefoot toad (Pelobates fuscus Laurenti, transport (Raffel et al., 2006; Tiberti and Gentilli, 2010; 1768) in the Netherlands was recently found carrying Gandola and Hendry, 2014). This latter phenomenon is leeches (not identified but most likely H. stagnalis) called phoresy (Platt et al., 1993; Tiberti and Gentilli, attached to the dorsum and hind legs (Struijk and van 2010; Gandola and Hendry, 2014). Leeches have been der Heijden, 2015). linked to local declines of amphibians and can act as In this paper, we present the first record of palmate vectors for diseases (Elliott and Tullett, 1984; Toledo, newts (Lissotriton helveticus, Razoumowsky, 1789) 2005; Raffel et al., 2006; Romano and Di Cerbo, 2007; as a host for H. stagnalis and we discuss prevalence, Wells, 2007; Ayres and Iglesias, 2008; Beukema and parasitism, phoresy and possible disease transmission. de Pous, 2010; Kutschera et al., 2010; Stead and Pope, Our observations were made in the context of an ongoing 2010). study on the effects of Dermocystid parasites (Class: The fresh water leech Helobdella stagnalis (Linnaeus, Mesomycetozoea) on palmate newts. The site where this 1758) is a predatory species which feeds on a wide array study takes place (Melickerheide; 51.17562; - 6.04373, of freshwater invertebrates, but especially oligochaetes, WGS84) is a partly forested area in National Park De chironomids and aquatic snails (van Haaren et al., 2004). Meinweg, located in the Dutch Province Limburg east The distribution of H. stagnalis is global (save Australia) of the city Roermond. A total of eleven semi-natural, and it is a very common species in Europe where this (semi-) permanent ponds (in an area of approximate +/- leech inhabits many fresh water habitats (Dresscher 1400 x 1700 m, with all ponds restricted to an area of and Higler, 1982; van Haaren et al., 2004). Helobdella +/- 500 x 300m) were monitored on a weekly basis from stagnalis has been identified as a (facultative) amphibian 27 February 2017 until 20 June 2017. Water surface area parasite in two anuran and two urodelan species: yellow- per pond ranged from 30 to 480 m2 with most ponds bellied toad (Bombina variegata Linnaeus, 1758), (n=8) having an average water surface of 100 – 150 m2 . common frog (Rana temporaria Linnaeus, 1759), Plant cover of each pond varied at the time, ranging from tiger salamander (Ambystoma tigrinum Green, 1825) 75-95 % (n= 4), 70-80% (n=1), 30-50% (n=3), 10-20% and smooth newt (Lissotriton vulgaris Linnaeus 1758) (n=2) and 0% (n=1). The local amphibian community consists of common frogs, pool frogs (Pelophylax lessonae Camerano, 1882), edible frogs (P. klepton esculentus Linnaeus, 1758), common toads (Bufo bufo Linnaeus, 1758), natterjack toads (Epidalea calamita 1 Reptile, Amphibian and Fish Conservation the Netherlands. Laurenti, 1768: rare), smooth newts, palmate newts and Toernooiveld 1 alpine newts (Ichthyosaura alpestris Laurenti, 1768). 6525 ED Nijmegen, the Netherlands Only palmate newts were found to carry leeches during 2 Van Hall Larenstein University of Applied Sciences,

Agora 1, 8934 CJ Leeuwarden, the Netherlands the current study. 3 Royal Natural History Society in Limburg. Godsweerderstraat Palmate newts were captured with a dip net, after 2, 6041 GH Roermond, the Netherlands which morphometrics and photographs for recapture * Corresponding author e�� purposes (by means of CMR software Wild-ID) were 718 Tariq Stark et al.

WGS84) which has a variable area (between 0-30 m2) dependent on rainfall, and often dries up completely in summer. Prevalence was 42.9% (n=7) for the single pond and 0.5% for all ponds (across all study ponds we collected 604 newts). Most leeches moved freely on the newts’ skin after capture although a few near the axial region, head and cloaca seemed to be attached to the newts. Some leeches seemed to be attached by the mouth parts (head and caudal region) and some by Figure 1. Lateral view of a female Lissotriton helveticus with the caudal sucker (Figure 1). Abrasions, haemorrhages two Helobdella stagnalis leeches attached to the head (Photo or other irregularities due to possible parasitism were by Remco Ploeg). not observed. However, it is possible that small or microscopic abrasions were present but remained undetected. In addition, the seemingly attached leeches were located near regions including many lymphatic taken and the presence, location and number of lesions vessels, such as the axial region and cloaca. Some of indicative of Dermocystid infection of each individual the leeches located on the head were darker and looked were assessed (González-Hernández et al., 2010; Fiegna more engorged than individuals found elsewhere on et al., 2017, Stark, unpublished data). Abiotic conditions the newts, which might indicate feeding. Therefore, of the pond and plant cover were also measured. On two we cannot rule out parasitism, while noting that our separate occasions (Febr. 27th, March 7th 2017), three observations however might solely indicate a phoretic palmate newts with leeches on various parts of the body interaction. None of the infected palmate newts were were observed in a single pond (Table 1). The leeches recaptured over the duration of the study. were identified as H. stagnalis due to the presence of Abrasions, haemorrhages, melanophore accumulations the chitinized nuchal scute and two eyes which are and local dermic inflammation in a common frog highly distinctive features of this species (Dresscher carrying leeches as described in Tiberti and Gentilli and Higler, 1982; Sawyer, 1986). None were collected. (2010) suggest that the proboscis of H. stagnalis is Palmate newts with leeches were only caught in the capable of successfully puncturing amphibian skin. smallest of the eleven ponds (51.1753527; - 6.0408016, Breaches in the skin due to feeding leeches might

Table 1. Details of three Lissotriton helveticus carrying Helobdella stagnalis leeches. The measured morphometrics were abbreviated1 Table as 1follows:: Details ofSnout three VentLissotriton Length helveticus (SVL), carrying Tail Length Helobdella (TL), stagnalis Filament leeches. Length The measured (FL). morphometrics were abbreviated as follows: Snout Vent Length (SVL), 2 Tail Length (TL), Filament Length (FL). 3 Species Lissotriton helveticus Lissotriton helveticus Lissotriton helveticus Sex Female Male Female Date 27-2-2017 27-2-2017 7-3-2017 SVL (mm) 36 33 32 TL (mm) 35 31 36 FL (mm) 1 3 0.5 Total length (mm) 72 67 68.5 Number of H. stagnalis 4 2 3 H. stagnalis location One on dorsal side of head, One on the belly and one One on the belly and two on one on lateral side of head, on the base of the tail the lateral side of the body one on the cloaca and on the base of the tail Presence Dermocystid lesions absent absent absent Pond temperature (°C) 10 10 7.4 Pond acidity (pH) 8.5 8.5 6.7 Electric conductivity (µS/cm) 52 52 39 Plant Cover (%) 70 70 80 4

1 First record of parasitism or phoresy by Helobdella stagnalis on Lissotriton helveticus 719 leave the host more vulnerable for infectious agents González-Hernández, M., Denoël, M., Duffus, A.J., Garner, in the environment though (Raffel et al., 2006). In a T.W., Cunningham, A.A., Acevedo-Whitehouse, K. (2010): recent study of European medicinal leeches (Hirudo Dermocystid infection and associated skin lesions in free- living palmate newts (Lissotriton helveticus) from southern medicinalis) in the Meinweg National Park (Lenders, France. Parasitology International 59: 344-350. 2015) it was established that this species feeds on Kutschera, U., Roth, M., Ewert, J.P. (2010): Feeding on bufoid common frog, common toad and spadefoot toad. It was toads and occurrence of hyperparasitism in a population suggested that young specimens most likely predate of the medicinal leech (Hirudo verbena Carena 1820). palmate newts, as being the most abundant and wide Research Journal of Fisheries and Hydrobiology 5: 9-13. spread amphibian species in the National Park. In this Lenders, A.J.W. (2015): The medical leech back in the Meinweg particular area leeches might have a larger impact on National Park. Is this protected parasite still under threat? Natuurhistorisch Maandblad 104: 61-67. the amphibian community than previously noted. Platt, T.R., Sever, D.M., Gonzalez, V.L. (1993): First report of From our observations we cannot determine if H. the predaceous leech Helobdella stagnalis (Rhynchobdellida: stagnalis has a parasitic or purely phoretic relationship Glossiphoniidae) as a parasite of an amphibian, Ambystoma with L. helveticus in this area. Our observations describe tigrinum (Amphibia: Caudata). The American Midland the first record of a phoretic relationship between H. Naturalist 129: 208-210. stagnalis and L. helveticus and the third case of phoresy Raffel, T.R., Dillard, J.R., Hudson, P.J. (2006): Field evidence of H. stagnalis on a urodelan host. for leech-borne transmission of amphibian Ichthyophonus sp. Journal of Parasitology 92: 1256-1264. Romano, A., Di Cerbo, A.R. (2007): Leech predation on amphibian Acknowledgements. This study was performed under permit eggs. Acta Zoologica Sinica 53: 750-754. FF/75A/2016/015 issued by Reptile, Amphibian and Fish Sawyer, R.T. (1986): Feeding biology, ecology and systematics. In: Conservation the Netherlands. We would like to thank S. Holland, Leech biology and behaviour, 2nd Edition, p. 419-793. Clarendon P. van Soest, A. Spitzen-van der Sluijs, A. A. Cunningham and Press, Oxford. the management of National Park De Meinweg. Rob Gandola is Stead, J.E., Pope, K.L. (2010): Predatory leeches (Hirudinida) thanked for the insightful discussion and for proof reading the may contribute to amphibian declines in the Lassen region, manuscript. California. Northwestern Naturalist 91: 30-39. Struijk, R.P.J.H., van der Heijden, F. (2015): Parasitisme door References bloedzuigers bij de knoflookpad. �� 17: 42. Ayres, C., Iglesias, J. C. (2008): Leech presence on Iberian brown Tiberti, R., Gentilli, A. (2010): First report of freshwater leech frog, Rana iberica, (Amphibia: Anura: Ranidae) from north- Helobdella stagnalis (Rhyncobdellida: Glossiphoniidae) as a western Spain. Acta Herpetologica 3: 155-159. parasite of an anuran amphibian. Acta Herpetologica 5: 255- Beukema, W., de Pous, P. (2010): Exceptional leech predation on 258. Amietophrynus mauritanicus (Anura, Bufonidae) in Tunisia. Toledo, L.F. (2005): Predation of juvenile and adult amphibians Herpetology Notes 3: 289-290. by invertebrates: current knowledge and perspectives. Dresscher, T.G., Higler, L.W.G. (1982): De Nederlandse Herpetological Review 36: 395-400. bloedzuigers Hirudinea. Koninklijke Nederlandse van Haaren, T., Hop, H., Soes, M., Tempelman, D. Natuurhistorische Vereniging 154: 1-64. (2004): The freshwater leeches (Hirudinea) of the Elliott, J.M., Tullett, P.A. (1984): The status of the medicinal leech Netherlands. Lauterbornia 52: 113-131. Hirudo medicinalis in Europe and especially in the British Isles. Wells, K.D. (2010): The ecology and behavior of amphibians. Biological Conservation 29: 15-26. University of Chicago Press. Fiegna, C., Clarke, C.L., Shaw, D.J., Baily, J.L., Clare, F.C., Gray, Zimić, A. (2015): Commensalism, predation or parasitism: A., Garner, T.W.J., Meredith, A.L. (2017): Pathological and First report of the leech Helobdella stagnalis Linnaeus, phylogenetic characterization of Amphibiothecum sp. infection 1758 on yellow-bellied toad, Bombina variegata (Linnaeus, in an isolated amphibian (Lissotriton helveticus) population on 1758). Ecologica Montenegrina 2: 62-63. the island of Rum (Scotland). Parasitology 144: 484-496. Gandola, R., Hendry, C. (2014): Lissotriton vulgaris (smooth newt): Parasitism or phoresy? Herpetological Bulletin 128: 22-23.

Accepted by Wouter Beukema