Michael R. Hutchings

Paratuberculosis Infection of Nonruminant Wildlife in Scotland

ABSTRACT Recent reports of natural paratuberculosis (or Johnes disease) in rabbits, foxes, and stoats has focused debate on the presence and importance of wildlife reservoirs in the epidemiology of this disease. This paper describes an extensive study investigating 18 nonruminant wildlife species for evidence of paratuberculosis. Using both culture and histopathological analysis, fox, stoat, weasel, crow, rook, jackdaw, rat, wood mouse, hare, and badger were found to harborMycobacterium avium subsp. paratuberculosis, the causative organism of paratuberculosis, suggesting that the epidemiology of this disease is more complex than previously realized.

Towards a functional explanation for the occurrence of anorexia during parasitic infections

The development and occurrence of anorexia, the voluntary reduction in food intake during parasitic infections in animals, is somewhat paradoxical and contrary to conventional wisdom and expectation. We take the view that its occurrence is an evolved, costly behavioural adaptation which serves a function. Five such functional and general hypotheses to account for it are developed: (1) anorexia is induced by the parasite for its own benefit; (2) food intake decreases to starve parasites; (3) the negative effect on the hosts energetic efficiency during parasitic diseases has a direct effect on food consumption; (4) food intake decreases for the purpose of promoting an effective immune response in the host; and (5) anorexia allows the host to become more selective in its diet, and thus select foods that either minimize the risk of infection or are high in antiparasitic compounds. Only hypotheses (4) and (5) survive the comparison for consistency with the physiological, metabolic and behavioural alterations that occur during the development of parasitic infections, and with the rule of generality (i.e. account for its occurrence in both protozoan and helminth infections). Both surviving hypotheses will need further experimental testing for their support or rejection, and such experiments are proposed. Also, the advantages and consequences of viewing anorexia during parasitic infections within a functional framework are discussed. These arise from the recognition that anorexia is a disease-coping strategy, part of the mechanism of recognition of parasite invasion by the immune system, which leads to a modification of the hosts feeding behaviour. Copyright 1998 The Association for the Study of Animal Behaviour

Effects of farm management practices on cattle grazing behaviour and the potential for transmission of bovine tuberculosis from badgers to cattle

Despite the large body of circumstantial evidence to suggest a link, the means by which bovine tuberculosis is passed from badgers to cattle remains unclear; pasture contamination with the urine, faeces and/or sputum of infectious badgers is believed to be the main route of transmission. Therefore the behaviour of grazing cattle was studied to determine whether they avoided investigating and/or grazing pasture contaminated with badger excreta, and whether different farm management practices enhanced the potential for disease transmission. Active latrines were avoided by most cattle until the sward length in the rest of the field was reduced, after which there was an increasing likelihood that active badger latrines would be grazed. Most of the cattle grazed active badger latrines, but cattle of low rank within the herd grazed latrines more heavily. Farm management practices that reduced the availability of long swards shortened the period of investigative behaviour and greatly enhanced the risk that cattle would graze active badger latrines. Cattle were more likely to graze pasture away from latrines that was contaminated either with badger urine or single faeces. Because bacilli remain viable in the soil for up to 2 years, there is the potential for bacilli to accumulate at active badger latrines, and these could pose a significant risk to cattle, even when the latrine is no longer being used by badgers. Cattle readily grazed the lush sward at disused latrines, during which they could ingest contaminated soil; the amount of soil ingested increases as sward length decreases.

Predicting Impacts of Climate Change on Fasciola hepatica Risk

Fasciola hepatica (liver fluke) is a physically and economically devastating parasitic trematode whose rise in recent years has been attributed to climate change. Climate has an impact on the free-living stages of the parasite and its intermediate host Lymnaea truncatula, with the interactions between rainfall and temperature having the greatest influence on transmission efficacy. There have been a number of short term climate driven forecasts developed to predict the following seasons infection risk, with the Ollerenshaw index being the most widely used. Through the synthesis of a modified Ollerenshaw index with the UKCP09 fine scale climate projection data we have developed long term seasonal risk forecasts up to 2070 at a 25 km square resolution. Additionally UKCIP gridded datasets at 5 km square resolution from 1970-2006 were used to highlight the climate-driven increase to date. The maps show unprecedented levels of future fasciolosis risk in parts of the UK, with risk of serious epidemics in Wales by 2050. The seasonal risk maps demonstrate the possible change in the timing of disease outbreaks due to increased risk from overwintering larvae. Despite an overall long term increase in all regions of the UK, spatio-temporal variation in risk levels is expected. Infection risk will reduce in some areas and fluctuate greatly in others with a predicted decrease in summer infection for parts of the UK due to restricted water availability. This forecast is the first approximation of the potential impacts of climate change on fasciolosis risk in the UK. It can be used as a basis for indicating where active disease surveillance should be targeted and where the development of improved mitigation or adaptation measures is likely to bring the greatest benefits.

BEHAVIOURAL STRATEGIES USED BY PARASITIZED AND NON-PARASITIZED SHEEP TO AVOID INGESTION OF GASTRO-INTESTINAL NEMATODES ASSOCIATED WITH FAECES

A study was instigated to test whether grazing herbivores have evolved effective strategies to reduce parasite ingestion and to assess the effects of parasitism on these strategies. Two choice trials, each using five animals parasitized with O. circumcincta and five parasite naive animals, were conducted to investigate cues used by sheep to avoid grazing swards contaminated with faeces. Animals were presented with pairs of artificial swards (36 X 21 cm) and allowed to graze for short periods. In the first trial, four quantities (0 g, 5 g, 25 g and 25 g), and in the second trial a control (no faeces) and three age classes (0, 10 and 21 days old), of faeces were tested against each other. Increasing amount of faeces per sward tray was associated with a reduced proportion of bites taken from the sward and reduced bite depth and mass. The minimum amount of faeces at which sheep showed significant levels of rejection was 15 g. Decreasing age of faeces was associated with a reduced proportion of bites taken from the sward, reduced bite depth and mass. This presented the paradox that grazing swards contaminated with young faeces presented least risk of parasitism, yet fresh faeces presented the strongest stimulus for sward rejection. Parasitism altered animal grazing behaviour with parasitized animals becoming more selective when avoiding contaminated swards, taking smaller bites at reduced bite rates compared with nan-infected animals. The enhancement of faeces avoidance behaviours shown by parasitized animals could act to reduce further intake of parasites and suggests that grazing behaviour is affected by nematode infection.

Can animals use foraging behaviour to combat parasites

Host-parasite interactions are often seen as an arms race, with parasites attempting to overcome host resistance to infection. Herbivory is a common route of transmission of parasites that represents the most pervasive challenge to mammalian growth and reproduction. The present paper reviews the foraging skills of mammalian herbivores in relation to their ability to exploit plant properties to combat parasites. The starting point is that foraging behaviour may ameliorate the impact of parasitism in three ways; hosts could: (1) avoid foraging in areas contaminated with parasites; (2) select diets which increase their resistance to parasites; (3) select for foods containing anti-parasitic properties (self-medication). Details are given of the pre-requisite skills needed by herbivores if they are to combat parasitism via behaviour, i.e. herbivores are able to: (a) determine their parasitic state and alter their behaviour in relation to that state (behaviours 1, 2 and 3); (b) determine the environmental distribution of parasites (behaviour 1); (c) distinguish plant species or plant parts that increase their resistance to parasites (behaviour 2) or have anti-parasitic properties (behaviour 3). Mammalian herbivores cannot detect the presence of the parasites themselves and must rely on cues such as faeces. Despite the use of these cues contacting parasites may be inevitable and so mechanisms to combat parasitism are necessary. Mammalian herbivores have the foraging skills needed to exploit the heterogeneous distributions of nutrients and parasites in complex foraging environments in order to avoid, and increase their resistance to, parasites. Current evidence for the use of plant secondary metabolites (PSM) by herbivores for self-medication purposes remains equivocal. PSM have both positive (anti-parasitic) and negative (toxic) effects on herbivores. Here details are given of an experimental approach using tri-trophic (plant-herbivore-parasite) interactions that could be used to demonstrate self-medication in animals. There is strong evidence suggesting that herbivore hosts have developed the foraging skills needed to take advantage of plant properties to combat parasites and thus use behaviour as a weapon in the host-parasite arms race.

Management of disease in wild mammals

1 The Science of Wildlife Disease Management Richard J. Delahay, Graham C. Smith, and Michael R. Hutchings 2 Wildlife Population Structure and Parasite Transmission: Implications for Disease Management Paul C. Cross, Julian Drewe, Victoria Patrek, Gareth Pearce, Michael D. Samuel, and Richard J. Delahay 3 Assessment of Transmission Rates and Routes, and the Implications for Management Peter Caley, Glenn Marion, and Michael R. Hutchings 4 Modelling Disease Dynamics and Management Scenarios Graham C. Smith, Glenn Marion, Steve Rushton, Dirk Pfeiffer, Hans H. Thulke, Dirk Eisinger, and Michael R. Hutchings 5 An Economic Perspective on Wildlife Disease Management Richard Bennett, Graham C. Smith, and Ken Willis 6 Options for the Control of Disease 1: Targeting the Infectious or Parasitic Agent Jean Blancou, Marc Artois, Emmanuelle Gilot-Fromont, Volker Kaden, Sophie Rossi, Graham C. Smith, Michael R. Hutchings, Mark A. Chambers, Steve Houghton, and Richard J. Delahay 7 Options for the Control of Disease 2: Targeting Hosts Stephen P. Carter, Sugoto S. Roy, Dave P. Cowan, Giovanna Massei, Graham C. Smith, Weihong Ji, Sophie Rossi, Rosie Woodroffe, Gavin J. Wilson, and Richard J. Delahay 8 Options for the Control of Disease 3: Targeting the Environment Alastair I. Ward, Kurt C. VerCauteren, W. David Walter, Emmanuelle Gilot-Fromont, Sophie Rossi, Gareth Edwards-Jones, Mark S. Lambert, Michael R. Hutchings, and Richard J. Delahay 9 Risk Assessment and Contingency Planning for Exotic Disease Introductions Vicky S. Jackson, Selene Huntley, Alex Tomlinson, Graham C. Smith, Mike A. Taylor, and Richard J. Delahay 10 Wildlife Disease Surveillance and Monitoring Marc Artois, Roy Bengis, Richard J. Delahay, Marie-Jose Duchene, J. Paul Duff, Ezio Ferroglio, Christian Gortazar, Michael R. Hutchings, Richard A. Kock, Frederick A. Leighton, Torsten Morner, and Graham C.Smith 11 Disease Management in Endangered Mammals Andrew C. Breed, Raina K. Plowright, David T. S. Hayman, Darryn L. Knobel, Fieke M. Molenaar, David Gardner?Roberts, Sarah Cleaveland, Dan T. Haydon, Richard A. Kock, Andrew A. Cunningham, Anthony W. Sainsbury, and Richard J. Delahay Glossary References Index

Sheep avoidance of faeces-contaminated patches leads to a trade-off between intake rate of forage and parasitism in subsequent foraging decisions

Abstract We tested the hypotheses that the avoidance of faeces by herbivores leads to a grazing trade-off between nutrition and parasitism, and that the relative costs and benefits of the trade-off in relation to animal parasitic state determines their subsequent grazing behaviour. We divided 30 female sheep, Ovis aries, into three treatment groups, each of 10 animals. A parasitized and an immune treatment were created by daily dosing two groups of 10 sheep with the abomasal parasiteOstertagia circumcincta , for 3 weeks and 14 weeks before the experiment, respectively. The remaining sheep were maintained as nonparasitized (controls). Each of the three treatment groups was divided into two subgroups, each of which was placed in an experimental field plot and rotated around on a daily basis for 2 weeks. Each experimental plot was divided into a chequerboard of 100 patches with alternate patches contaminated with sheep faeces. Initially, all animals significantly selected to graze the noncontaminated patches resulting in disproportionate sward depletion. The significant avoidance of the faeces-contaminated patches by parasitized and nonparasitized sheep remained throughout the experiment. However, immune animals reduced their avoidance of faeces-contaminated patches during the latter stages of the experiment, resulting in a nonselective grazing strategy by the end. Compared with nonparasitized control sheep, immune sheep had increased rates of herbage intake and activity, and vice versa for parasitized sheep. We discuss the differences in grazing behaviour in relation to the sheeps state of parasite infection and the relative costs and benefits of the grazing trade-off. The behaviours used by herbivores to avoid the ingestion of parasites affects sward structure, creating a grazing trade-off between nutrition and parasitism, their response to which will determine their subsequent intake of nutrients and parasites, and thus fitness and survival.

Do non-ruminant wildlife pose a risk of paratuberculosis to domestic livestock and vice versa in Scotland?

Paratuberculosis (Johnes disease) was long considered only a disease of ruminants. Recently non-ruminant wildlife species have been shown to harbor Mycobacterium avium subsp. paratuberculosis, the causative organism of paratuberculosis. We review the known non-ruminant wildlife host range of M. avium subsp. paratuberculosis and consider their role in the epidemiology of paratuberculosis in domestic ruminant livestock. Mycobacterium avium subsp. paratuberculosis has been isolated from lagomorph, canid, mustelid, corvid, and murid species. In agricultural environments domestic ruminants may contact wildlife and/or their excreta when grazing or feeding on farm-stored feed contaminated with wildlife feces, opening up the possibility of inter-species transmission. Of the wildlife species known to harbor M. avium subsp. paratuberculosis in Scotland, the rabbit is likely to pose the greatest risk to grazing livestock. Paratuberculosis in domestic ruminants is a notoriously difficult disease to control; the participation of non-ruminant wildlife in the epidemiology of the disease may partially account for this difficulty.

The herbivores’ dilemma: trade-offs between nutrition and parasitism in foraging decisions

Abstract An experiment was carried out using a trade-off framework to determine the rules of sward selection, in relation to gastrointestinal parasite dispersion, used by mammalian herbivores, and the effect of level of feeding motivation and parasitic status on these rules. Twenty-four sheep divided into four animal treatment groups resulting from two levels of feeding motivation (high and moderate) and two parasitic states (parasitised with Ostertagia circumcincta and non-parasitised) were presented with pairs of experimental swards which varied in N content (high and low), sward height (tall and short) and level of contamination with faeces and thus parasites (contaminated and non-contaminated). The selection for tall swards outweighed both the selection for N-rich swards and the avoidance of faecal contaminated swards. The selection for N-rich swards could not completely overcome faecal avoidance. Parasitism in animals with a moderate feeding motivation reduced their bite rates and grazing depths, thereby probably reducing the rate of ingestion of parasitic larvae. In contrast, highly feeding-motivated animals (including those parasitised) increased their bite rates and grazing depths, thereby increasing the rate of ingestion of parasites. The inclusion of parasite distributions, both in the environment and within herbivore host populations, is likely to advance optimal foraging theory by enhancing its predictive power.