Recent appearance and pathology of <i>Actinobdella pediculata</i> (Hirudinea) on freshwater drum, <i>Aplodinotus grunniens</i> Rafinesque, in Hay Bay, Lake Ontario

During late April and early May 2005, a mortality involving an estimated 25 000 adult freshwater drum, Aplodinotus grunniens Rafinesque, occurred in the shallow waters of the Bay of Quinte, Lake Ontario, near Kingston. A strain of viral haemorrhagic septicaemia virus (VHSV) was isolated from these fish by the Department of Fisheries and Oceans (Gulf Fisheries Centre, Moncton, New Brunswick; Miller-Dodd 2005) and thought to underlie the mortalities. During the outbreak, commercial fishermen on Hay Bay noticed huge leeches protruding from beneath the opercula of dead and dying freshwater drum. The leech was identified as Actinobdella pediculata (Hemmingway, 1908). The present study describes this first record of A. pediculata in Lake Ontario, assesses the gross pathology at the site of attachment through additional samples in 2006 and discusses the possible relationship of the infections to the epidemic. The Bay of Quinte is a z-shaped body of water (257 km2) in the northeastern corner of Lake Ontario, with Hay Bay (44°10′N, 77°56′W) being a shallow, marshy and lentic embayment at its western end. As a result of extensive agricultural practices and waterfront development since the 1950s, the Bay of Quinte is listed as an ‘area of concern’ by Environment Canada. Major environmental issues include excessive nutrients from sewage treatment plants, septic tanks and surface runoff, habitat loss, contaminated sediment, bacterial contamination and the recent spread of the zebra mussel, Dreissena polymorpha (Environment Canada 2005). Four moribund adult drum (25.2–66.5 cm long) were collected during the first week of May 2005 by a commercial fisherman operating on Hay Bay. The samples were frozen and shipped to Saint Mary’s University (Halifax, NS). Fish were thawed and total length recorded. Prevalence and intensity of infection with A. pediculata, and the distribution of leeches on the left and right sides of the head were documented. All leeches, most still attached to the host tissue, were fixed in 10% formalin. Fixed length and weight of 10 leeches were determined. The following 1–4 May 2006 20 live adult drum (12.7–75 cm long) were captured with hoop nets set overnight in Hay Bay. Fish length and the number and location of the leeches were again noted. Leeches were fixed in situ in 10% formalin and the lengths and weights of nine leeches recorded. Histological sections of attached leeches from both sampling periods were prepared using standard methods and stained with haematoxylin and eosin, Masson’s trichrome or Giemsa. In 2005, all four drum were infected with A. pediculata (Fig. 1). Intensity was 3.5 ± 4.4 (n = 4). Mean length and weight of the leeches were 2.5 ± 0.4 cm (n = 10) and 2.8 ± 0.75 g (n = 10), respectively. In 2006, 5 of 20 drum were infected. Intensity was 2.6 ± 2.1 (n = 5). Mean length and weight of the leeches were 1.0 ± 0.2 cm (n = 9) and 0.2 ± 0.3 g (n = 9), respectively. Adult Actinobdella pediculata in ventrolateral view showing the modified posterior sucker attached to the body of the leech via a narrowed, rigid posterior peduncle. Formalin fixed specimen (bar = 0.5 cm). Of 14 leeches collected in 2005, 13 were embedded in host tissue covering the cleithrum. One small leech lay free in the buccal cavity. Of 13 leeches collected in 2006, 11 were embedded in host tissue covering the cleithrum. Two were attached side-by-side on the dorsal inner face of an operculum. Live leeches were not easily removed when pulled with tweezers. A 2006 specimen, which was bent inwards ventrally so that its anterior and posterior ends met, left a distinct impression of its anterior end in host tissue adjacent to the cavity in which its caudal sucker was embedded. In multiple infections, the leeches often formed clusters on one side of the head. On one occasion when examining a live leech, a brooding young disappeared into the cavity within which an adult was attached. The presence of brooding young at the site of attachment was not confirmed in histological sections and thus this behaviour may have been an isolated case. In addition, there were two instances of co-embedment whereby a pair of leeches had their posterior suckers set in the same host tissue cavity. Host tissue was reddened up to a half-a-centimetre around the site of attachment. A pore with a diameter similar to that of the peduncle opened into a subsurface chamber in which the posterior sucker fitted (Fig. 2). Histologically, the tegument covering the cleithrum was composed of a thickened epidermis with a thin, but distinct, basal membrane overlying a vascularized dermal stratum spongiosum. At the site of attachment, tissue damage included degeneration, necrosis and sloughing of the epidermis, and central erosion (up to 5 mm deep), disruption, extravasation, and some cellular necrosis within the adjacent stratum spongiosum. We found no evidence of feeding wounds within the wall of the opercular cavity or on the gill filaments and arches. Overall condition of infected and non-infected fish appeared the same. Histological section of the attachment site of Actinobdella pediculata on the cleithral tissues of freshwater drum (Masson’s trichrome stain, bar = 500 μm). The caudal sucker (CS) is embedded in dermal tissue (DT) with the resulting cavity being lined by necrotic tissue and partially filled with cellular debris. The isolated VHSV, a virus with a record of being highly infectious and pathogenic (de Kinkelin & Castric 1982; Castric & de Kinkelin 1984), is thought to be the principal pathogen involved in the epidemic (Miller-Dodd 2005). There is no evidence to suggest that A. pediculata was involved directly in the epidemic, for large numbers of leech-free fish died in the main channel of the Bay of Quinte that spring. However, leeches from the 2005 sample were huge and, as noticed by commercial fishers, often prevented closing of the operculum. We suspect that such infections reduce the efficiency of the respiratory pump because of their physical presence and thus the leech becomes another stressor to a host already compromised by high water temperatures and low oxygen uptake. Leeches are known to be mechanical vectors of spring viraemia of carp (Ahne 1985) and the fibropapilloma herpesvirus of marine turtles (Greenblatt, Work, Balazs, Sutton, Casey & Casey 2004). We believe A. pediculata had no involvement in the suspected 2005 VHS epidemic in the Bay of Quinte, for these leeches are more-or-less permanently attached to the freshwater drum host and thus have a life history that cannot serve horizontal transmission of the virus between fish. Lack of distinct feeding wounds in the vicinity of attached leeches suggests that they either feed sporadically, allowing healing, or that they feed more frequently, but over a more widespread area made possible by the large body size and ability to stretch significant distances. Our observation of the impression in the host cavity that was formed by the anterior end of a 2006 specimen, supports the likelihood that A. pediculata also feeds on the blood and tissue that is released during erosion of host tissue. Intact erythrocytes were found in the gut of all leeches sectioned, suggesting frequent feeding. Previous studies have reported that A. pediculata typically attaches to the region of the branchial isthmus, cleithrum, and inner wall of the operculum, and that this attachment involves penetration of the posterior sucker into host tissues (Sawyer 1986). Similar lesions have been reported in a number of other leeches of fish, most of which attach to a specific site on the host. Acanthobdella peledina, regarded as a proto-hirudinid (or ancestral rhynchobdellid), forms clusters of deep holes in tissues at the base of the dorsal fin of grayling, Thymallus arcticus (Pallas) (see Sawyer 1986). Infections of Actinobdella inequiannulata aggregate on the inner surface of the operculum of the white sucker, Catostomus commersoni (Lacepède), and form lesions similar to those reported in the present study, although slightly shallower and involving extensive cellular infiltration by eosinophilic granulocytes (Lester & Daniels 1976; Klemm, Daniels, Moser & Lester 2003). Appy & Cone (1982) reported similar lesions caused by attachment of Myzobdella lugubris on the logperch, Percina caprodes (Rafinesque), and brown bullhead, Ictalurus nebulosus (Lesuer). Sawyer (1986) draws attention to other examples and concluded that the posterior sucker of these leeches is no longer a principal organ of locomotion but rather an organ of attachment for a semi-permanent parasite. It appears that once this more or less permanent anchoring takes place, some degree of aggregation is required for sexual reproduction to be possible. Site specificity and large body size as seen in A. pediculata must further facilitate the chance of sexual reproduction. Actinobdella pediculata is expected to exhibit a life history similar to that of A. inequiannulata (Bur 1994; Smith & Klemm 2003) whereby hosts are parasitized by juvenile leeches in early spring, leeches mature and reproduce from May to August, and a second generation of leeches parasitizes fish in August and September (Smith & Klemm 2003). It is thought that cross-fertilization of A. inequiannulata occurs on the host during the summer months when leeches occur in aggregations on the operculum (Sawyer 1986). The same can be assumed for A. pediculata because of its close relationship to A. inequiannulata (Sawyer 1986; Smith & Klemm 2003) and by its clustering behaviour reported herein. After fertilization, A. inequiannulata detaches from its host and seeks refuge in sediment under rocks for egg laying and subsequent brooding of juveniles (Smith & Klemm 2003). Our observations suggest that A. pediculata may exhibit a brooding strategy that is different from that of A. inequiannulata. The unique morphological characteristics of A. pediculata, including the anterior shift in the position of the anus, a pedicel and an enlarged caudal sucker, are regarded as adaptations to semi-permanent parasitism (Hemmingway 1912; Sawyer 1986). Finally, our finding of a brooding young and the two instances of co-embedment warrant further investigation into the possibility that A. pediculata broods young while attached to the host. How these leeches become partially burrowed into host tissue is not known, but secretory enzymes produced in gland cells located in the posterior sucker (Hemmingway 1912; Sawyer 1986) provide a possible mechanism. In the case of A. pediculata,Hemmingway (1912) described the initial wound made by young, recently attached leeches to be a shallow depression and that, with time, inflamed tissues form a collar around the peduncle while the posterior sucker works its way deeper into underlying tissues. It appears then that the form of the lesion is the result of joint activity of host and parasite, one characterized by surprisingly local pathology. The 2006 specimen that had left an impression of its anterior end in host tissue adjacent to the cavity in which it was embedded suggests that secretory enzymes may also be produced anteriorly. Actinobdella pediculata is host specific to the freshwater drum with a known distribution that includes much of the American midwest and southern Great Lakes region, with an isolated report from Maine (Hemmingway 1912; Meyer 1937; Branson & Amos 1961; Klemm 1972, 1982). It has been assumed that A. pediculata can be found throughout the range of the freshwater drum (Sawyer 1972; Klemm 1985), which extends from the Gulf of Mexico, through the Mississippi drainage, and into the Great Lakes and associated waters. Despite numerous surveys conducted in the 1960s, 1970s and 1980s throughout western Lake Erie (Bangham 1972; Dechtiar 1972; Dechtiar & Nepszy 1988) and the Bay of Quinte area of Lake Ontario (Dechtiar & Christie 1988), reports of A. pediculata are noticeably missing. In addition, fisheries biologists working for the past decade on freshwater drum in the Bay of Quinte do not recall seeing the leech (J. Casselman, personal communication). Actinobdella pediculata was first detected in western Lake Erie in 1991, leading Bur (1994) to believe that above-average water temperatures during the early summer of 1991 and better visibility in lake water because of the occurrence of zebra mussels may have resulted in increased leech activity in the lake. The present report of A. pediculata in Hay Bay is another case of the leech making a sudden appearance where it was previously not known to occur. The fact that it has occurred in widely separated geographical localities suggests a common underlying environmental cause. A review of the literature shows that the known distribution of A. pediculata has expanded since the 1970s, from Illinois, Minnesota, Wisconsin (Klemm 1977) and Lake St. Clair (Klemm 1972) to Michigan, Ohio and Lake Erie (Klemm 1991; Bur 1994) and now Lake Ontario. The freshwater drum population in the Bay of Quinte has increased substantially in recent years following the zebra mussel invasion of the 1980s (J. Casselman, personal communication). Increased zebra mussel densities have also been correlated with increases in invertebrate species diversity and abundance (Griffiths 1993; Stewart, Miner & Lowe 1998). In addition, the VHS outbreak of 2005 in Lake Ontario was linked with abnormally high water temperatures in early spring of that year (Miller-Dodd 2005); these high water temperatures may have also been responsible for the appearance of A. pediculata in Lake Ontario, just as was implicated by Bur (1994) in the appearance of the leech in Lake Erie in 1991. The apparent expansion of the leech’s range and/or recent increased prevalence of the leech may be explained by one or more of these documented environmental changes. It would be interesting to include A. pediculata as part of bio-monitoring of environmental health in the Great Lakes region. The authors thank Robert Shepard, Rodney Lloyd, Beryl Brooks and the staff of the Cedar Point Resort for helping organize the work, to Mr A. Mathers (Ontario Ministry of Natural Resources, Picton) for providing a scientific collecting licence, and to Dr J. Casselmann (Queens University, Kingston) and Dr D. Klemm (US EPA) for reviewing the manuscript. We thank Dr A. Rojo (Saint Mary’s University, Halifax) for help with identification of the cleithrum. The study was made possible through NSERC Discovery Grants awarded to M. Burt and to D. Cone. This report is dedicated to the late Robert A. Shepard who, in addition to a lifetime career of teaching, was an astute observer of natural phenomena. Many of his observations initiated research projects in which he became involved and which were published subsequently. Mr Shepard died shortly after leading our collecting expedition to Hay Bay.

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