What is the relationship between level of infection and ‘sickness behaviour’ in cattle?

https://doi.org/10.1016/j.applanim.2013.05.007Get rights and content

Abstract

We hypothesised that a range of parasite doses that cause subclinical disease would lead to similar behavioural changes in cattle. This was tested by infecting bull calves with one of four different doses of the gastrointestinal parasite Ostertagia ostertagi: 0 (control), 75,000 (L), 150,000 (M) or 300,000 (H) larvae, whilst measuring aspects of their behaviour, usually encompassed by the term ‘sickness behaviour’. For parasitised bulls faecal egg counts and serum pepsinogen levels were elevated from Day (D) 20, the latter being affected linearly by dose. The different doses had different effects on animal fitness: body weight gain (BWG) was reduced for treatments M and H from D23, with M animals showing a recovery after D30, whereas H bulls continued to have lower BWG. Behaviours were only affected for H animals. Average lying episode duration increased by 25% and lying and standing episode frequency decreased by 22% from around D29 when compared to uninfected controls. The number of steps taken by H animals decreased by 34% relative to the controls from D34–46. There was no significant effect on any parameters of feeding behaviour. The results suggest that, for a wide range of parasite doses, general posture, activity and feeding behaviour may be unaffected despite some effects on host fitness. However, higher doses which may lead to clinical disease result in effects that are possibly directly related to pathogen dose. The practical applications of detecting health challenges through behaviour may therefore depend on the level of infection and their pathophysiological consequences.

Introduction

It is now well established that health challenges, such as infection with a pathogen or stimulation of the immune response, may lead to changes in animal behaviour (Hart, 1990, Larson and Dunn, 2001, Weary et al., 2009, Szyszka et al., 2012). Such behavioural changes may have diagnostic value, as these can precede any clinical signs of the condition (Quimby et al., 2001, Huzzey et al., 2007, González et al., 2008, Kyriazakis and Tolkamp, 2010).

The question whether the onset and extent of the behavioural changes are related to the size of the health challenge, such as the infectious dose of a pathogen, remains largely unanswered. There is little information about the relationship between pathogen dose and change in behaviours. The few exceptions are studies, mainly in rodents, suggesting a negative relationship between challenge dose and social exploration (Edwards, 1988, Bluthé et al., 1996), anxiety (Bassi et al., 2012) or activity (Johnson and von Borell, 1994, Skinner et al., 2009). There is also indirect evidence of a possible relationship between pathogen dose and the different dimensions of feeding behaviour (González et al., 2008). In all these experiments, however, infection either occurred naturally, or only a narrow range of infective doses was used. As a consequence, these do not allow conclusions about the form of the relationship. Knowledge of such relationships has both theoretical and diagnostic value, as it would allow targeted interventions and will therefore enhance animal health and welfare.

There are at least two possible forms of the relationship, shown on Fig. 1. The first is that above a certain dose the change in behaviour is of the same magnitude for a wide range of doses that may lead to (subclinical) diseases. Only at high pathogen doses that may lead to clinical disease, further changes in behaviour become apparent and may be linearly related. This expectation comes from the studies on pathogen-induced anorexia; these have demonstrated that over a wide range of infective doses with macro- or micro-parasites the reduction in food intake is very similar for a variety of animals and pathogens (as summarised by Kyriazakis et al., 1998, Sandberg et al., 2006, Kyriazakis, 2010). The second possible form is that increasing pathogen doses lead to increasing changes in behaviour. These two relationships will have different (intervention) consequences when using behaviour as a predictor of the level of infection. The objective of this study was to investigate the relationship between the infective dose of a macro-parasite, Ostertagia ostertagi, and a number of behaviours in growing cattle. O. ostertagi is the most significant parasite affecting cattle in temperate climates (Anderson, 1988, Rinaldi and Geldof, 2012). As the selected range of macro-parasite doses was expected to lead to subclinical infections (Szyszka et al., 2012, Szyszka et al., 2013), we hypothesised that the relationship would be of the first form, i.e. that the effects on the behaviours would be of similar magnitude across all doses. The behaviours focused upon in this study and considered representative of ‘sickness behaviour’ were chosen on the basis that they had previously been found to change as a consequence of an O. ostertagi infection (Szyszka et al., 2012, Szyszka et al., 2013). They consisted of activity, general posture and feeding behaviour. The behavioural changes were expected to occur as a consequence of the pathophysiological consequences (abomasal damage) induced by the parasite.

Section snippets

Materials and methods

The experiment took place at the facilities of Newcastle University after approval of the experimental protocols by the Animal Experiments Committee and under license according to the UK Animals (Scientific Procedures) Act for regulated procedures.

Faecal egg counts

The consistency of the faeces varied throughout the experiment both within and between treatments: up to Day 23 the faeces were similarly solid for all treatments. However, after Day 23 a number of animals in the H treatment showed signs of diarrhoea (maximum 5 out of 6 on Day 37), as did some in the M treatment (maximum 3 out of six on Day 34); this was not the case for the L and C treatments. The FEC of the C animals remained at zero throughout the experiment. For the other treatments, eggs

Discussion

The objective of this study was to investigate the form of the relationship between macro-parasite dose and a number of behavioural responses in growing cattle. The health challenge used was an O. ostertagi infection, previously shown to affect several aspects of the behaviours addressed here (Forbes et al., 2007, Szyszka et al., 2012, Szyszka et al., 2013). Three different infective doses of the parasite were used; as their range was expected to lead to subclinical infections, the null

Acknowledgement

This project was sponsored by EBLEX (English Beef and Lamb Executive).

References (50)

  • B.L. Hart

    Behavioral adaptations to pathogens and parasites: five strategies

    Neurosci. Biobehav. Rev.

    (1990)
  • B.L. Hart

    Biological basis of the behavior of sick animals

    Neurosci. Biobehav. Rev.

    (1988)
  • H. Hilderson et al.

    The presence of an early L4 larvae population in relation to the immune response of calves against Ostertagia ostertagi

    Vet. Parasitol.

    (1993)
  • J.M. Huzzey et al.

    Prepartum behavior and dry matter intake identify dairy cows at risk for metritis

    J. Dairy Sci.

    (2007)
  • A. Kidane et al.

    Consequences of infection pressure and protein nutrition on periparturient resistance to Teladorsagia circumcincta and performance in ewes

    Vet. Parasitol.

    (2009)
  • I. Kyriazakis

    Anorexia during infection in animals affected by food composition?

    Anim. Feed Sci. Technol.

    (2010)
  • I. Kyriazakis et al.

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

    Anim. Behav.

    (1998)
  • S.J. Larson et al.

    Behavioral effects of cytokines

    Brain Behav. Immun.

    (2001)
  • D.E.B. Lawton et al.

    Infection of sheep with adult and larval Ostertagia circumcincta: effects on abomasal pH and serum gastrin and pepsinogen

    Int. J. Parasitol.

    (1996)
  • G. Reiner et al.

    Suffering in diseased pigs as expressed by behavioural, clinical and clinical-chemical traits, in a well defined parasite model

    Appl. Anim. Behav. Sci.

    (2009)
  • G.W. Skinner et al.

    Avoidance of physical activity is a sensitive indicator of illness

    Physiol. Behav.

    (2009)
  • O. Szyszka et al.

    Do the changes in the behaviour of cattle during parasitism with Ostertagia ostertagi have a potential diagnostic value?

    Vet. Parasitol.

    (2013)
  • B.J. Tolkamp et al.

    Are cows more likely to lie down the longer they stand?

    Appl. Anim. Behav. Sci.

    (2010)
  • B.J. Tolkamp et al.

    To split behaviour into bouts, log-transform the intervals

    Anim. Behav.

    (1999)
  • M.P. Yeates et al.

    The use of mixed distribution models to determine bout criteria for analysis of animal behaviour

    J. Theor. Biol.

    (2001)
  • Cited by (29)

    • Ruminant Metabolic Diseases: Perturbed Homeorhesis

      2023, Veterinary Clinics of North America - Food Animal Practice
    • Impact of foot-and-mouth-disease on goat behaviour after experimental infection with serotype SAT1 virus

      2020, Preventive Veterinary Medicine
      Citation Excerpt :

      This study is part of a larger project concerning FMD vaccine efficacy and the vaccination might have reduced the FMD-induced behavioural changes especially in animals receiving the higher doses of the vaccine. In cattle, it has been suggested that a threshold dose of pathogens is required before behavioural changes secondary to a parasitic infestation can be detected (Szyszka and Kyriazakis, 2013). A potential limitation of the current study is that all behaviours were summarised by phase, creating one data point per individual per phase, thus reducing the statistical power to detect differences.

    • Behavioural assessment of sheep is sensitive to level of gastrointestinal parasite infection

      2020, Applied Animal Behaviour Science
      Citation Excerpt :

      The significant finding of experiment 1 was the identification of meaningful correlations between the relative position of sheep on GPA dimensions 1 and 3 and individual FEC. It is generally accepted that parasitised animals will not behave in a similar manner to an unchallenged animals, and any alterations in host behaviour could relate to parasite burden and the impact infection causes within the animal (Poulin, 1995; Szyszka and Kyriazakis, 2013). The tendency of observers to score sheep with higher FEC as more docile and at ease on GPA 1 may reflect fatigue or the lower energy state of the sheep.

    View all citing articles on Scopus
    View full text