Experimental infection of yellow stingrays Urobatis jamaicensis with the marine leech Branchellion torpedinis

Abstract

Infestations of elasmobranchs by the marine leech Branchellion torpedinis can be problematic in aquaria and negatively affect host health. To better characterize the extent and pathogenesis of disease, 12 yellow stingrays Urobatis jamaicensis were infected with 1 or 3 leeches for 14 d. Leeches were associated with anorexia, extensive cutaneous ulceration, decreased host packed cell volume (PCV) and serum total solids (TS), and mortality in 3 rays. Average decrease in host PCV positively correlated with ulcer size and parasite:host ratio. Average decrease in host serum TS positively correlated with parasite:host ratio. Blood chemistry and total white blood cell counts revealed no significant trends. Additional necropsy findings included gill and splenic pallor, pericardial edema, perirenal edema, and decreased hepatocellular lipid deposits. Microscopic evaluation of leeches demonstrated host erythrocytes and proteinaceous fluid within parasite intestines, confirming active blood feeding. Results indicate B. torpedinis has the potential to cause significant disease in elasmobranchs, including death in as few as 5 d, and identifies ulcer size and parasite:host ratio as risk factors for disease. Elucidation of this host-parasite interaction helps characterize host response to parasites and facilitate care of parasitized elasmobranchs in aquarium and wild settings. KEY WORDS: Branchellion torpedinis · Leech · Urobatis jamaicensis · Stingray · Infection Resale or republication not permitted without written consent of the publisherDis Aquat Org 101: [51][52][53][54][55][56][57][58][59][60] 2012 Although host mortality is often presumed to be from blood loss, there may be additional factors affecting fish health during leech infections. Ectoparasites can represent stressors for fish and have been associated with decreased foraging (Milinski 1984), impaired anti-predator behavior (Milinski 1985), and reduced fecundity and growth (Iwama et al. 1999). For example, shorthorn sculpin Myxocephalus scorpius infected with the leech Malmiana brunnea showed significantly lower energetics than uninfected sculpin: Energy deficiencies attributed to leech feeding, tissue damage, and loss of metabolites, accounted for an energy loss of ~750 cal wk −1 per gram of leech (Mace & Davis 1972).Leeches also play a role as vectors of disease in fish. Leech transmission of hematozoa including Trypanosoma spp. and Trypanoplasma spp. has been demonstrated in elasmobranchs and teleosts (Kruse et al. 1989, Burreson 2007. There is evidence implicating leeches as mechanical vectors of viruses in teleosts (Ahne 1985, Mulcahy et al. 1990, Faisal & Schulz 2009) and speculation that attachment site ulcers (Faisal et al. 2011), and perhaps transmission by leeches themselves (Bragg et al. 1989), may predispose hosts to bacterial infections. Further physiologic and pathologic effects may exist in the leechhost relationship, but are yet unidentified.Branchellion torpedinis is a marine leech that exclusively parasitizes elasmobranchs. Inadverten...

The marine leech Branchellion torpedinis parasitic on the angelshark Squatina squatina and the marbled electric ray Torpedo marmorata

“…The observed S. squatina and T. marmorata had a healthy appearance without unusual noticeable facts in their behavior. Skin sloughing as reported by Marancik et al (2012), after 7 days of attachment, and epidermal ulceration in the attachment area as shown in Marancik et al (2012) and Başusta et al (2015) were not observed on the individuals observed by us. This could be an indication of recent attachment to the host in the present study or better resistance of the S. squatina and T. marmorata epithelium to B. torpedinis feeding compared to U. jamaicensis and A. bovinus.…”

“…In this sense, the present report is the first reliable, long-term, record of B. torpedinis associations based on observations in its natural habitat during 10 years, including data on size, depth distribution, substrate, predation location, host age class, activity and season. Marancik et al (2012) associated infection of yellow stingray Urobatis jamaicensis, with a weight range between 315 to 550 g, by one to three B. torpedinis, in an aquarium environment during 14 days with anorexia, extensive cutaneous ulceration, decreased host packed cell volume and serum total solids, and mortality. However, to date, there is no conclusive data from the wild of the impact on the host's biological fitness and behavioral change when parasitized by B. torpedinis.…”

Protein and cholesterol electrophoresis of plasma samples from captive cownose ray (Rhinoptera bonasus)

“…22 The effects of leech infestation were examined in an experimental model using yellow stingrays. 21 During acute infestation, with mortality occurring within 3 days, animals exhibited anorexia, decreased PCV, and decreased total solids. While total WBC counts did not change, decreased hepatocellular lipid deposits were noted in addition to cutaneous ulceration and edema.…”

Parasite component community of smalltooth sawfish off Florida: diversity, conservation concerns, and research applications

“…In contrast, B. torpedinis, because it is a blood-feeding ectoparasite that must pierce the epidermis (which is nonvascular in elasmobranchs) to reach the vascular portions of the stratum compactum (deep dermis), causes ulcerative lesions even if only one leech is present. Marancik et al (2012) showed that a single specimen of the leech could be lethal in the yellow stingray Urobatis jamaicensis (Cuvier, 1816) under laboratory conditions. While we did not detect a leech when we first noticed the lesioned clasper of one host specimen, B. torpedinis apparently can temporarily hide in a body cavity, especially the orobranchial chamber and possibly the cloaca (A. D. Dove pers.…”

“…comm.). Further, these leeches are expected to move off and back onto the host during their life cycle (Benz & Bullard 2004), so additional leeches may have contributed to the lesion if the clasper is a preferred site of infection (but see Marancik et al 2012, who suggest that this species may form a more lasting association with a given host).…”