School of Biological Sciences
Royal Holloway University of London
Egham, Surrey, TW20 0EX
United Kingdom

Tel: 01784-443182
Fax: 01784-414224
E-mail: j.w.lewis@rhul.ac.uk

Research areas: parasitology and aquatic toxicology

Research activities have continued on the ecology, ecophysiology and epidemiology of parasites in terrestrial and aquatic hosts.

Parasites of Terrestrial Hosts

In association with DEFRA, studies in the field of avian parasitology have focused on the establishment of macroparasites in piscivorous bird hosts and in particular the population biology of nematodes in the alimentary tract of cormorants. The dominance of one intestinal nematode species is of particular interest in view of the high degree of species richness in parasite communities of birds. In a separate project, parasitic infections have also been shown to have an impact on bird behaviour and may act to reduce the expression of sexually selected song traits in male birds such as the sedge warbler.

In the field of mammalian parasitology, and in collaboration with the University of Nottingham, frequency distribution and multivariate statistical techniques have been used to analyse patterns of dispersion, competitive interactions and co-occurrence of macroparasites in small mammal populations in the UK, the Middle East and the Far East (University of Malaya, Kuala Lumpur). In addition molecular techniques have been applied to identify and characterise DNA clones of wild and laboratory strains of nematodes including the trichostrongyle Heligmosomoides polygyrus from rodents and the ascarid Toxocara canis from feral carnivores such as the fox. This appropriately combines an ecological with a molecular approach to further our understanding of the epidemiology and immunology of these nematode species especially the zoonotic T. canis which can pose significant environmental health problems to human populations worldwide.

In association with CABI Bioscience UK Centre, Egham, Surrey, the genetic diversity and molecular phylogeny of steinernematid entomopathogenic nematodes are also being investigated.

Parasites of Aquatic Hosts

Recent research in fish parasitology has focused on the identification, dissemination and impact of introduced parasites on fisheries, following the expansion of fish farming and the increased importation of salmonid and cyprinid fish into the UK primarily from Europe. These parasites include the pathogenic blood fluke Sanguinicola inermis in carp and ectoparasitic ergasilid copepods in coarse fish. In particular, successful experimental transmission of the blood fluke S. inermis in carp in laboratory aquaria has provided an opportunity to investigate, by in vivo and in vitro methods, humoral and cellular immune responses of fish to macroparasites. In vitro cultures indicate that cellular attachment and surface damage are minimal in adult and larval flukes suggesting the presence of an immune evasion mechanism by the parasite. This S. inermis carp model represents the first experimental approach, in collaboration with Keele University and funded by the Leverhulme Trust, to evaluate the impact of aquatic pollution on cellular and immunological changes in a fish - macroparasite system; ammonia suppresses whilst cadmium stimulates the immune responses of fish to the blood parasite S. inermis. This will have important consequences in evaluating the potential role of fish and fish parasites as indicators of pollution and their role in ecosystem functioning.

The molluscan host of S. inermis (left) and the cercarial stage found within it.

Such a study on the role of fish macroparasites as potential indicators of pollution has recently been initiated with the Institute of Ecology and Conservation Biology, University of Vienna and the Austrian Environment Agency on the macroparasites of the barbel from the River Danube, funded by the Austrian Science Foundation. This project is also linked with heavy metal toxicity studies, being carried out in our laboratory on the survival and infectivity of larval digeneans parasitising molluscan intermediate hosts.

The impact of parasitism on fish growth

Collaborative programmes with the Natural History Museum, London and the University of Exeter have focused on the community ecology, molecular ecology and ecophysiology of macroparasites in the European eel and in particular the pathogenic swim bladder nematode Anguillicola crassus, funded by the Leverhulme Trust. This parasite, which is of oriental origin, was introduced into western Europe in the 1980's and first reported from the UK in 1987. It was believed to have a freshwater life cycle and we investigated the ecology, transmission and survivorship of A. crassus in eels maintained under estuarine and marine conditions and also determined the osmotic and ionic tolerance and regulatory ability of the parasite. We have demonstrated for the first time that A crassus can be transmitted in the marine environment and, therefore, could impair the success of the eel spawning migration to the Sargasso Sea - hence this may have a significant impact on eel conservation. Further studies on the community and molecular ecology of and other macroparasites in eels will commence in October 2002 with further funding from the Leverhulme Trust.

Recent interest in marine fish parasitology has been extended to studies on the identification and epidemiology of macroparasites in Red Sea fish in collaboration with Suez Canal University, Ismailia, Egypt.

Research in the field of fish toxicology originated from the Group's expertise on the ultrastructure and ecology of gill parasites and pathogens in freshwater and marine fish. We have shown how electron microscopy, and in particular, the scanning electron microscope (SEM) can be used as a diagnostic tool to detect specific patterns of surface damage on fish gills. This technique has been used by the UK Environment Agency, using deployed fish, for detecting pollutants and monitoring water quality in lakes and rivers following pollution incidents. Further research, funded by the UK Environmental Agency, is in progress to investigate the role of bacterial exotoxins in unexplained fish mortalities using this SEM technique.

			Furthermore, novel biosensing studies on freshwater mormyrid fish of the genus Gnathonemus (pictured at right) have indicated that behavioural and electrical responses of these fish to a broad spectrum of low level concentrations of toxic chemicals can be utilised as biosensors of environmental pollution. This research has demonstrated a direct correlation between the rate of pulsing, characterised by patterns of electric organ discharge (pictured below), and water quality. Such a system has considerable potential for real-time monitoring of toxic chemicals at river intake sites to protect drinking water supplies and a prototype is being developed for use in the tropical waters of Malaysia in collaboration with Petronas Oil and the Universiti Putra Malaysia, Kuala Terengganu.

In southern Africa using histopathological and physiological assays, the role of the freshwater crab Potamonautes warreni is being investigated as a potential bioindicator of heavy metal contamination especially waterborne cadmium. In north Africa, heavy metal toxicity is at the forefront of studies on direct toxicity assessment and remediation of Lake Maryut, Alexandria, Egypt in association with the Institute of Graduate Studies and Research, University of Alexandria.

Lewis JW, Morley NJ, Drinkall J, Jamieson BJ, Wright R, Parry JD. Toxic effects of Streptomyces griseus spores and exudate on gill pathology of freshwater fish. Ecotoxicol Environ Saf. 2008 [Epub ahead of print]

Morley NJ, Lewis JW. The influence of climatic conditions on long-term changes in the helminth fauna of terrestrial molluscs and the implications for parasite transmission in southern England. J Helminthol. 2008 4:1-11

Pal P, Abu-Madi MA, Lewis JW. Applying an aggregative dispersive dichotomy (ADD) model to parasitic infections in host populations. J Helminthol. 2008 82(3):187-92

Morley NJ, Adam ME, Lewis JW. The effects of temperature on the distribution and establishment of Echinoparyphium recurvatum metacercariae in Lymnaea peregra. J Helminthol. 2007 81(3):311-5

Prenner MM, Ibrahim H, Lewis JW, Crane M. Toxicity and trace metal concentrations of sediments from Lake Maryut, Alexandria, Egypt. Bull Environ Contam Toxicol. 2006 77(4):616-23

Morley NJ, Lewis JW, Hoole D. Pollutant-induced effects on immunological and physiological interactions in aquatic host-trematode systems: implications for parasite transmission. J Helminthol. 2006 80(2):137-49

Morley NJ, Crane M, Lewis JW. Toxicity of cadmium and zinc mixtures to the decaudized cercarial life span of Diplostomum spathaceum. J Helminthol. 2005 79(4):353-9

Norton J, Rollinson D, Lewis JW. (2005) Epidemiology of Anguillicola crassus in the European eel (Anguilla anguilla) from two rivers in southern England. Parasitology. 130: 679-86 [PubMed]

Morley NJ, Crane M, Lewis JW. (2005) Changes in survival characteristics of Diplostomum spathaceum cercariae emerged from cadmium-exposed Lymnaea stagnalis. J Helminthol. 79: 55-9 [PubMed]

Morley NJ, Crane M, Lewis JW (2004) Influence of cadmium exposure on the incidence of first intermediate host encystment by Echinoparyphium recurvatum cercariae in Lymnaea peregra.
J Helminthol. 78: 329-32 [PubMed]

Morley NJ, Crane M, Lewis JW (2005) Toxicity of cadmium and zinc mixtures to cercarial tail loss in Diplostomum spathaceum (Trematoda:Diplostomidae). Ecotoxicol Environ Saf. 60: 53-60 [PubMed]

Norton J, Lewis JW, Rollinson D (2004) Temporal and spatial patterns of nestedness in eel macroparasite communities. Parasitology. 129: 203-11 [PubMed]

Morley NJ, Adam ME, Lewis JW. (2004) The role of Bithynia tentaculata in the transmission of larval digeneans from a gravel pit in the Lower Thames Valley. J Helminthol. 78: 129-35 [PubMed]

Pal P, Lewis JW. (2004) Parasite aggregations in host populations using a reformulated negative binomial model. J Helminthol. 78: 57-61 [PubMed]

Morley NJ, Lewis JW, Adam ME. (2004) Metacercarial utilization of a naturally infected single species (Lymnaea peregra) snail community by Echinoparyphium recurvatum. J Helminthol. 78: 51-6 [PubMed]

Morley NJ, Irwin SW, Lewis JW. (2003) Pollution toxicity to the transmission of larval digeneans through their molluscan hosts. Parasitology. 126 Suppl: S5-26 [PubMed]

Morley SJ, Crane M, Lewis JW. (2003) Toxicity of cadmium and zinc to the decaudised cercarial life-span of Diplostomum spathaceum (Trematoda: Diplostomidae). Parasitology. 127: 497-506 [PubMed]

Norton J, Lewis JW, Rollinson D. (2003) Parasite infracommunity diversity in eels: a reflection of local component community diversity. Parasitology. 127: 475-82 [PubMed]

Schuwerack PM, Lewis JW, Hoole D. (2003) Cadmium-induced cellular and immunological responses in Cyprinus carpio infected with the blood parasite, Sanguinicola inermis. J Helminthol. 77: 341-50 [PubMed]

Morley NJ, Crane M, Lewis JW. (2003) Effects of cadmium and zinc toxicity on orientation behaviour of Echinoparyphium recurvatum (Digenea: Echinostomatidae) cercariae. Dis Aquat Organ. 56: 89-92 [PubMed]

Morley NJ, Crane M, Lewis JW. (2003) Cadmium toxicity and snail-digenean interactions in a population of Lymnaea spp. J Helminthol. 77: 49-55 [PubMed]

Schuwerack PMM, Lewis JW (2003) The mode of action of acute and chronic concentrations of waterborne Cd in the digestive gland of the acclimated infested freshwater crab (Potamonautes warreni). Cell Tissue Res. 312: 249-263. [View abstract]

Morley NJ, Crane M, Lewis JW (2003) Toxicity of cadmium and zinc to the cercarial activity of Diplostomum spathaceum (Trematoda : Diplostomidae). Folia Parasitol. 50: 57-60. [View abstract]

Morley NJ, Crane M, Lewis JW (2002) Toxicity of cadmium and zinc mixtures to Diplostomum spathaceum (Trematoda : Diplostomidae) cercarial survival. Arch. Environ. Contam. Toxicol. 43: 28-33. [View abstract]

Kirk RS, Morritt D, Lewis JW, Kennedy CR (2002) The osmotic relationship of the swimbladder nematode Anguillicola crassus with seawater eels. Parasitology 124: 339-347. [View abstract]

Schuwerack PMM, Lewis JW, Hoole D, Morley NJ (2001) Ammonia-induced cellular and immunological changes in juvenile Cyprinus carpio infected with the blood fluke Sanguinicola inermis. Parasitology 122: 339-345.

Schuwerack PMM, Lewis JW, Jones P (2001) The potential use of the South African river crab, Potamonautes warreni, as a bioindicator species for heavy metal contamination. Ecotoxicology 10: 159-166.

Schuwerack PMM, Lewis JW, Jones PW (2001) Pathological and physiological changes in the South African freshwater crab Potamonautes warreni Calman induced by microbial gill infestations. J. Invertebr. Pathol. 77: 269-279.

Richards DT, Lewis JW (2001) Fecundity and egg output by Toxocara canis in the red fox, Vulpes vulpes. J. Helminthol. 75: 157-164.

Morley NJ, Crane M, Lewis JW (2001) Toxicity of cadmium and zinc to miracidia of Schistosoma mansoni. Parasitology 122: 81-85.

Morley NJ, Crane N, Lewis JW (2001) Toxicity of cadmium and zinc to encystment and in vitro excystment of Parorchis acanthus (Digenea : Philophthalmidae). Parasitology 122: 75-79.

Morley NJ, Crane M, Lewis JW (2001) Toxicity of cadmium and zinc to Diplostomum spathaceum (Trematoda : Diplostomidae) cercarial survival. Int. J. Parasit. 31: 1211-1217.

Kheir R, Ibrahim H, Lewis J, Callaghan A, Crane M (2001) Comparison of acetylcholinesterase and glutathione S- transferase activity in Chironomus riparius Meigen exposed to chemical-spiked sediments. Bull. Environ. Contam. Toxicol. 66: 603-610.

Abu-Madi MA, Lewis JW, Mikhail M, El-Nagger ME, Behnke JM (2001) Monospecific helminth and arthropod infections in an urban population of brown rats from Doha, Qatar. J. Helminthol. 75: 313-320.

Abu-Madi MA, Behnke JM, Lewis JW, Gilbert FS (2000) Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. J. Helminthol. 74: 7-15.

Abu-Madi MA, Mohd-Zain SN, Lewis JW, Reid AP (2000) Genomic variability within laboratory and wild isolates of the trichostrongyle mouse nematode Heligmosomoides polygyrus. J. Helminthol. 74: 195-201.

Kirk RS, Kennedy CR, Lewis JW (2000) Effect of salinity on hatching, survival and infectivity of Anguillicola crassus (Nematoda : Dracunculoidea) larvae. Dis. Aquat. Org. 40: 211-218.

Kirk RS, Lewis JW, Kennedy CR (2000) Survival and transmission of Anguillicola crassus Kuwahara, Niimi & Itagaki, 1974 (Nematoda) in seawater eels. Parasitology 120: 289-295.

Behnke JM, Lewis JW, Zain SNM, Gilbert FS (1999) Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. J. Helminthol. 73: 31-44.

Buchanan KL, Catchpole CK, Lewis JW, Lodge A (1999) Song as an indicator of parasitism in the sedge warbler. Animal Behaviour 57: 307-314.

Abu-Madi MA, Behnke JM, Lewis JW, Gilbert FS (1998) Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in southeast England. J. Helminthol. 72: 93-100.

Ibrahim H, Kheir R, Helmi S, Lewis J, Crane M (1998) Effects of organophosphorus, carbamate, pyrethroid and organochlorine pesticides, and a heavy metal on survival and cholinesterase activity of Chironomus riparius Meigen. Bull. Environ. Contam. Toxicol. 60: 448-455.

Kirk RS, Lewis JW (1998) Histopathology of Sanguinicola inermis infection in carp, Cyprinus carpio. J. Helminthol. 72: 33-38.