Abstract

The monogeneans Dermophthirius penneri (Microbothriidae) and Erpocotyle tiburonis (Hexabothriidae) are common ectoparasites on their hosts in the wild and are associated with host morbidity and mortality in aquariums. Herein we report results from light and scanning electron microscopic examinations that were conducted to characterize skin lesions associated with D. penneri on wild black tip sharks (Carcharhinus limbatus)¹ and gill lesions associated with E. tiburonis on wild and aquarium-held bonnet head sharks (Sphyrna tiburo).² Results of these studies were combined with general information regarding the life histories of related parasites and the anatomy of sharks to formulate hypotheses regarding these specific host-parasite relationships. Dermophthirius penneri attached to the placoid scales of its host by using organic cement and a simple unarmed cup-like sucker (i.e., the haptor). This mode of attachment helps to explain the associated dermatitis, as lesions were in the immediate vicinity of worms and the chronic proliferative character of the lesions suggested a semi-stationary lifestyle for these worms. Placoid scale and biological cement may act as a physical barrier between D. penneri and effector cells of the host's immune system. However, in chronic lesions an inflammatory component to the interaction between the shark and the worms was evidenced by the presence of lymphocytic interstitial dermatitis beneath epidermal lesions, presumably mediated by alterations in scale arrangement and epidermal integrity resulting from worm attachment and feeding. Regions having heavy worm burdens and exhibiting odd scale patterns, missing scales and proliferative epithelium about scales suggested that infections of D. penneri in the wild may be limited by a process of scale loss and proliferation of epithelium. In captivity, where hosts may become heavily infected due to an increased rate of autoinfection, scale loss may facilitate secondary bacterial or fungal infections and osmotic imbalance. E. tiburonis attached to gill lamellae or bronchial epithelium by using a haptor comprised of 3 pairs of armed cup-like suckers. Juvenile and adult E. tiburonis each inhabited different locations on the gills. This suggested that, as these worms mature, they migrate from between gill lamellae located along the proximal two-thirds of filaments to distal and more afferent (respective to water flow) positions along the distal one-third of gill filaments, with many of them congregating at the free distal tips of filaments. Juvenile worms were located in the proximal portion of filaments, i.e., a region of the bronchial chamber that theoretically exhibits low water flow, whereas adult worms resided at the distal tips of filaments in a region of high afferent water flow, perhaps facilitating the release of eggs into the environment. The equally-restricted distribution of severe lamellar reduction and epithelial hyperplasia to the distal one-third of filaments in aquarium-held sharks, wherein parasite numbers were markedly higher than those on wild sharks, suggests a pattern of ontogenetic migration rather than random dispersion along the gill. If so, this suggests an oropharyngeal pathway for colonization of the shark gill. In the heavily-infected aquarium-held sharks, juvenile E. tiburonis occluded many interlamellar water channels, suggesting that blockage of respiratory water caused by juvenile worms was potentially more debilitating with regards to the respiratory capacity of the host than the proliferative gill lesions caused by the worms.

Acknowledgements

We thank Jim Romanow (Electron Microscopy Laboratory, University of Connecticut) and Jeffrey Braswell (Dupont Corporation) for assistance with scanning electron microscopy and Robin Overstreet (Gulf Coast Research Laboratory, University of Southern Mississippi) for financial support and some laboratory supplies. Partial support from NOAA/NMFS (award no. NA86FL0476) and the Mississippi-Alabama Sea Grant Consortium.

References

1.  Bullard, S.A., S. Frasca Jr., and G.W. Benz. 2000. Skin lesions caused by Dermophthirius penneri (Monogenea: Microbothriidae) on wild-caught blacktip sharks (Carcharhinus limbatus). Journal of Parasitology 86(3):618-622.

2.  Bullard, S.A., S. Frasca Jr., and G.W. Benz. In review. Gill lesions associated with Erpocotyle tiburonis (Monongenea: Hexabothriidae) on wild and aquarium-held bonnethead sharks (Sphyrna tiburo). Journal of Parasitology.