Master thesis in Veterinary Medicine

0

F A C U L T Y O F H E A L T H A N D M E D I C A L S C I E N C E S

U N I V E R S I T Y O F C O P E N H A G E N

Sara Sofia Lundberg VMK08075 / trj732

Master thesis in Veterinary Medicine

Use of strategic short-term grazing of bioactive forages in the control of gastrointestinal nematodes; Trichostrongylus colubriformis and

Teladorsagia circumcincta in organic lambs

By Sara Lundberg VMK08075/trj732

By Sara Lundberg VMK08075/trj732

Internal supervisor: Professor Stig Milan Thamsborg

External supervisor: Dr. Andrew Greer

Submitted: 22/06/2012

1

Name of department: Department of Veterinary Disease Biology

Author: Sara Lundberg

Dalslandsgade 8A-404

2300 Copenhagen S

[email protected]

Title: Use of strategic short term grazing of bioactive forages in the control of

gastrointestinal nematodes; Trichostrongylus colubriformis and Teladorsagia

circumcincta in organic lambs

Internal supervisor: Professor Stig Milan Thamsborg

Department of Veterinary Disease Biology

Faculty of Health and Medical Sciences

University of Copenhagen, Denmark

External supervisor: Dr. Andrew Greer

Faculty of Agriculture and Life Sciences

Lincoln University, New Zealand

Submitted: 22/06/2012

2

Preface

This Master thesis is the final project for my Master program in Veterinary Medicine at the Faculty

of Health and Medical Sciences, University of Copenhagen, Denmark. The purpose of the study

was to evaluate the effect of grazing sheep on bioactive forages for control of gastrointestinal

nematodes in organic farming in New Zealand. The thesis has been completed during six months

corresponding to 30 ETCS points. It is a product of cooperation between University of Copenhagen

and Lincoln University, New Zealand with the experimental work carried out between December

2011 and March 2012 in New Zealand and report writing completed in Denmark.

I would like to express my gratitude to all the people who have been involved in making this

project possible. First of all, thanks to my internal supervisor, Professor Stig Milan Thamsborg,

Faculty of Health and Medical Sciences, University of Copenhagen for guidance and assistance in

the initial planning phase in Denmark and for guidance and feedback through the process of

writing the thesis. Thank you for always taking the time to answer my questions. Thanks to my

external supervisor, Dr. Andrew Greer, Faculty of Agriculture and Life sciences, Lincoln University

who kindly allowed me to participate in this trial and who provided much support throughout the

process and also helped with all the statistical analysis. Thank you for your patience, generosity,

for answering my endless questions and for taking good care of me while in New Zealand. I would

further like to thank Technical Officer Robin McAnulty at JML, Lincoln University, who guided me

through the techniques in the laboratory and helped with the laboratory and field work. Thank

you for your collaboration and many good times together. I also wish to acknowledge the staff at

JML and Lincoln University. Thank you for your warm welcome and hospitality during my stay at

Lincoln University.

Thanks to my friends who have supported me whilst working on the thesis, with special thanks

Vibe Pedersen Lund for checking the Danish language and grammar, to Ann-Charlotte “Sessan”

Christensen for proofreading much of the material and giving your useful comments on it, and to

Sean Scully for checking language and grammar and for being an invaluable help and support and

my “male nurse” during my prolonged illness in New Zealand.

Finally I would like to thank my dear family for your great support and encouragement throughout

my whole education and especially this final part. Thank you for your endless patience, many

encouraging postcards and for always listening to and being there for me.

3

Abstract

Nematode parasitism of small ruminants is a major threat to ruminant farming systems throughout the

world, including New Zealand. Traditionally, parasite control has been performed through anthelmintic

treatments however the frequent use of anthelmintics has resulted in an increasing resistance against the

drugs. This is now a significant problem in most livestock producing countries. Numerous non-chemical

methods have been engaged to control nematodes in small ruminants including; grazing management,

supplementary feeding, biological control and bioactive forages. There have been field studies which have

shown that grazing sheep on certain bioactive forages may reduce their worm burdens and increase their

performance.

The objective of this study was to evaluate the effectiveness of targeted selective treatment using strategic

short term grazing on chicory, plantain and red clover on faecal egg count and liveweight gain in organic

lambs.

The trial was performed at Lincoln University, New Zealand during December 2011- March 2012. Sixty male

Coopworth lambs were used in the study. The lambs were split into two groups of thirty lambs and

introduced to two separate paddocks with ryegrass (Lolium perenne cv. Grasslands Nui) and white clover

(Trifolium repens cv. Grasslands Huia) contaminated with either Trichostrongylus colubriformis or

Teladorsagia circumcincta. On a fortnightly basis, the lambs were weighed and removed from the groups.

The lambs found not performing to a preset target weight were put to graze in two separate “hospital”

paddocks containing ryegrass and mix of chicory (Cichorium intybus cv. Grasslands Puna), plantain

(Plantago lanceolata cv. Grasslands Lancelot) and red clover (Trifolium pratense cv. Minshan) with minimal

contamination. Once they reached their target weight they were returned to graze in the main paddocks.

Faecal samples were collected from each lamb fortnightly to determine the extent of parasitic infection.

Observations showed very poor growth of the bioactive forages and did not reveal any antiparasitic effect

following time in the hospital paddocks. The most likely explanation for the lack of antiparasitic effect is the

poor growth of the forages. The mean daily liveweight gain increased after periods in the hospital paddock

which strongly suggests that grazing the lambs in the hospital paddocks did improve their performance. The

increasing LWG seen in lambs after periods in the hospital paddocks is however more likely to be a result of

grazing a pasture with lower contamination than being a result of the bioactive forages due to the poor

growth of the forages. Based on these findings the overall conclusion is that it was not possible in this study

to judge the effectiveness of the bioactive forages on liveweight gain or in reducing worm burdens.

4

Resumé

Nematodeinfektioner hos små drøvtyggere er et stort problem i produktionssystemer over hele verden.

Parasitkontrol har tidligere hovedsageligt bestået af anthelmintikabehandling, og det hyppige forbrug af

antibiotika har medført stigende resistensproblemer i de fleste lande med fåreproduktion. Den voksende

økologiske sektor er en drivkraft i udviklingen af alternativer til anthelmintikabehandling. En række

alternativer til anthelmintikabehandling hos små drøvtyggere er under udvikling, herunder

afgræsningsmanagement, supplerende fodring, biologisk kontrol og bioaktive planter. Studier har påvist, at

afgræsning af får på visse bioaktive planter kan reducere parasitbyrden hos fårene og øge deres tilvækst.

Det er også vist, at afgræsning af får på marker med lav parasitkontamination kan have positiv effekt på

tilvæksten.

Formålet med dette studie var at undersøge effekten af strategisk, kortvarig afgræsning af økologiske lam

på cikorie, lancet-vejbred og rødkløver udtrykt ved ægudskillelse i fæces og tilvækst.

Forsøget blev udført på Lincoln Universitet, New Zealand fra december 2011 til marts 2012. 60 Coopworth

vædderlam var inkluderet i studiet. De blev opdelt i to grupper, med 30 lam i hver gruppe, og sat til at

græsse på to forskellige folde med rajgræs (Lolium perenne) og hvidkløver (Trifolium repens),

kontaminerede med enten Trichostrongylus colubriformis eller Teladorsagia circumcincta. Hver fjortende

dag blev lammene vejet for at vurdere deres tilvækst. De lam, der opnåede en i forvejen udregnet målvægt,

forblev på de pågældende folde med rajgras/hvidkløver, mens de lam, der ikke opnåede målvægten, blev

flyttet til to adskilte ”hospitalsfolde” med rajgræs og en blanding af cikorie (Cichorium intybus), lancet-

vejbred (Plantago lanceolata) og rødkløver (Trifolium pretense), hvor kontaminationen var minimal. Efter

yderligere fjorten dage blev lammene atter vejet, og de lam, der nu opnåede deres målvægt, blev flyttet

tilbage til rajgras/hvidkløver-foldene. Fæcesprøver blev udtaget hver fjortende dag for at undersøge

parasitbyrden.

Observationerne viste en lav vækst af de bioaktive planter og der blev ikke fundet nogen antiparasitær

effekt efter afgræsning af ”hospitalsfoldene”. Dog tyder resultaterne på en positiv effekt på tilvæksten efter

tid på ”hospitalsfoldene” i 50% af tilfældene. Den øgede tilvæst efter afgræsning af ”hospitalsfoldene”

skyldes sandsynligvis reduceret parasitindtag fremfor en direkte effekt af de bioaktive planter. Baseret på

disse fund er den overordnede konklusion, at det ikke var muligt at bedømme effekten af de bioaktive

planter på tilvækst og parasitbyrde hos lammene. Imidlertid virker det sandsynligt, at afgræsning af lam i

kortere tid på folde med lavere parasitkontamination kan have positiv effekt på tilvæksten.

5

Table of contents

Preface ............................................................................................................................................................... 2

Abstract ............................................................................................................................................................. 3

Section I: Introduction ....................................................................................................................................... 6

I.1 Background .............................................................................................................................................. 6

1.1 Organic sheep farming in New Zealand .............................................................................................. 6

1.2 Importance of gastrointestinal nematodes in sheep farming in New Zealand .................................. 7

1.2.1 Trichostrongylus spp. ................................................................................................................. 10

1.2.2 Teladorsagia spp........................................................................................................................ 11

1.3 Control of gastrointestinal nematodes ............................................................................................. 12

1.3.1 Control based on the use of anthelmintics ............................................................................... 12

1.3.1.1 Anthelmintics and anthelmintic resistance........................................................................ 12

1.3.1.2 The concept of refugia ....................................................................................................... 12

1.3.1.3 Targeted and targeted selective treatments ..................................................................... 13

1.3.2 Non-chemical control of gastrointestinal nematodes ............................................................... 14

1.3.2.1 Grazing management ......................................................................................................... 14

1.3.2.2 Supplementary feeding ...................................................................................................... 15

1.3.2.3 Bioactive forages ................................................................................................................ 15

1.3.3 Integrated control ..................................................................................................................... 17

Section II: Own investigations ......................................................................................................................... 19

II.1 Introduction and objectives .................................................................................................................. 19

II.2 Materials and methods ......................................................................................................................... 20

2.1 Experimental design, study area and animals .................................................................................. 20

2.2 Sampling and analysis ....................................................................................................................... 22

2.3 Data handling and statistical analysis ............................................................................................... 23

II.3 Results ................................................................................................................................................... 23

3.1 Clinical and other observations ........................................................................................................ 23

3.2 Performance of hospitalised animals ............................................................................................... 25

3.2.1 Factors affecting time spent in hospital paddock ..................................................................... 28

II.4 Discussion .............................................................................................................................................. 30

II.5 Conclusion ............................................................................................................................................. 35

Section III: References ..................................................................................................................................... 36

Appendices

6

Section I: Introduction Nematode parasitism of small ruminants is a major animal health threat to ruminant farming systems

throughout the world causing big production losses (Waller 1997; Jackson & Coop 2000; Waller 2006).

Traditionally, parasite control has mainly consisted of anthelmintic treatments (Vlassoff & McKenna 1994)

and the frequent use of anthelmintics has resulted in increasing resistance to the drugs. This is now a

significant problem in most livestock producing countries, including New Zealand (Charleston & McKenna

2002). The escalating prevalence of populations resistant to anthelmintic and the requirement for reduced

anthelmintic usage in organic production systems suggest that there is a need for complementary

strategies and sustainable alternatives to anthelmintics in small ruminant production systems (Waller 1999;

Charleston & McKenna 2002; Athanasiadou et al. 2005). Several non- chemical methods have been

advocated to control nematodes including; grazing management, supplementary feeding, biological control

and vaccines. Another approach is the use of bioactive forages (Hoste et al. 2006; Stear et al. 2007). There

have been field studies suggesting that grazing sheep on certain bioactive forages might reduce their worm

burdens compared to grazing sheep on conventional forage (Marley et al. 2003; Waller 2006; Brunet et al.

2008; Lira et al. 2008). Results suggest that they may be a promising option for use in integrated control of

nematode parasitism (Hoste et al. 2006).

Integrated control aims at limiting the contamination on pastures (Vlassoff 1979) which seems to play a

main role in reducing production losses ( McAnulty et al. 1982; Brunsdon 1980) and increasing performance

in sheep (Thompson et al. 1982; McAnulty et al. 1982).

The aim of this thesis is to give a brief introduction to the importance of gastrointestinal nematodes in

sheep farming in New Zealand and different control methods, followed by results from experimental work

based on grazing lambs on a mix of chicory, plantain and red clover in order to control gastrointestinal

nematodes.

I.1 Background

1.1 Organic sheep farming in New Zealand

With the rapidly growing worldwide organic food market there is an ever increasing demand from

consumers that meat products will originate from farming systems that utilise lower levels of chemicals and

are more conscious towards the welfare of the animals and the sustainability of the environment. In these

systems where chemicals are not the primary source of controlling animal disease, the farmers must have

greater focus on a combination of grazing management and breeding animals that can produce under more

challenging circumstances. New Zealand farmers primarily rely on the use of anthelmintics to control

gastrointestinal nematodes in grazing sheep (Mupeyo et al. 2011). There is however an awareness and

7

increasing interest amongst New Zealand sheep and beef farmers towards the potential opportunity that

low-chemical and organic markets offer the livestock sector (Mackay et al. 2001). On some livestock farms

in New Zealand, farmers are changing their methods towards specialisation to these systems; however, the

growth of the organic sector is constrained due to a general lack of information amongst farmers (Morris &

Mackay 2002) and an inability to effectively control disease challenge from gastrointestinal parasites.

On low-chemical or organic sheep farms the major issue limiting production with respect to animal health is

the control of gastrointestinal nematodes (Mackay et al. 1999) There are several options for parasite

control according to organic farming standards and ethos, e.g. breeding for resilience to the parasites, using

high protein forages or forages with anthelmintic properties, bio-control such as nematophagus fungi and

grazing management. Most of the options offer a method for reducing the challenge of the parasites to the

animal but none will be an effective alternative to an anthelmintic drench once a nematode burden has

accumulated in the naïve animal (Mackay et al. 2001). High larval challenges are shown to have a

significantly reducing effect on liveweight gain (McAnulty et al. 1982; Thamsborg & Agergaard 2002). It is a

main factor in parasite reduced performance in growing lambs (Coop et al. 1982) and can cause great

production losses (Thamsborg & Agergaard 2002). Grazing sheep on pastures with low contamination plays

an important role for increasing the productivity of the lambs. Studies have shown an eightfold increase in

liveweight gain in lambs grazing a low contaminated pasture after drenching compared to lambs grazing on

a high contamination (Brunsdon 1976), benefits which presumably, at least in part, reflect a lesser degree

of anorexia of infection which is largely dose-dependent.

Putting many of these options into practice will require significant changes to the enterprise and a priority

change such as having more focus on pest management than on forage utilisation (Mackay et al. 2001).

1.2 Importance of gastrointestinal nematodes in sheep farming in New Zealand Gastrointestinal nematode (GIN) parasitism is a major threat to sheep farming throughout the world

(Jackson & Coop 2000; Waller 2006). The economic importance of GIN parasitism of sheep production in

New Zealand has been recognized since the late 19th century (Gilruth 1895). After a century of research on

GIN they are still a major factor limiting sheep production (Leathwick et al. 2001).

Twenty-six species of GIN have been identified from sheep in New Zealand (Vlassoff & McKenna 1994). The

most important species causing production loss and clinical disease are Trichostrongylus spp., Teladorsagia

spp., Haemonchus contortus and Nematodirus spp. and to some extent Cooperia curticei. The relative

abundance of GIN species can vary between districts (Vlassoff & McKenna 1994), with H. contortus mainly

being a problem in the North Island due to its relatively higher thermal requirement than other species for

larval development (Bruère et al. 1993; Hervé et al. 2003). Hervé et al. (2003) reported from a survey

conducted in New Zealand that Teladorsagia is the dominating genus in the South Island. Cooperia spp. is

found on both islands with the highest proportions in the northern North Island and southern South Island

8

and Trichostrongylus spp. vary within regions. Nematodirus spp. are common throughout the country but

because of their ability to survive cold winters, they may appear in larger numbers in the spring, especially

in the Canterbury, Otago and the Southland regions in the South Island (Bruère et al. 1993).

The life cycles of the GIN are very similar and the following description applies to Trichostrongylus spp.,

Teladorsagia spp., Haemonchus and Cooperia spp. The life cycle is direct, i.e. there is no intermediate host

(Fig.1). Adult female worms in the host lay eggs which are passed out in faeces. The eggs hatch and each

egg releases one first-stage larva, L1. The L1 develop and moult into a second stage larvae, L2. Both L1 and L2

feed on bacteria in the faeces. Eggs, L1 and L2 and require warmth and moisture to develop successfully.

Optimal development occurs in temperatures between 15˚C and 30˚C under adequate moisture conditions;

however eggs and larvae of most GIN species will tolerate cold temperatures although development is slow

and below 10˚C most eggs fail to hatch. First and second stage larvae are active feeders and vulnerable to

desiccation. In moist environments the mass of faeces protects from desiccation resulting in a large

proportion of eggs developing to the infective stage L3 which happens through a second moult from L2 to L3

(Familton & McAnulty 1997). At this moult the cuticle of the L2 remains as a sheath, protecting L3 until they

enter the host, but also preventing them from feeding. Usually it takes 2-3 weeks or more for eggs to hatch

and develop to L3 (Bruère et al. 1993). L3 migrate up the grass blades where they are ingested by sheep. In

the digestive tract L3 larvae exsheath and become L4 larvae. Small intestinal parasites normally exsheath in

the abomasum whereas abomasal parasites exsheath in the rumen. Over 8-10 days L4 larvae moult to form

immature adults, L5, which then moult once more to become mature adult worms. Female and male worms

mate inside the host, and females produce eggs that are passed out in the faeces (Familton & McAnulty

1997). The pre-patent period (the time from ingestion of larvae to egg production) is typically 21-28 days

(Bruère et al. 1993).

Fig. 1. Direct life cycle of gastrointestinal nematodes.

9

For Nematodirus spp. the preparasitic phase is different from other trichostrongyloids in that development

of L3 occurs within the egg shell. The development takes two months or more in temperate areas. The

combination of egg shell and L3 sheath makes the larvae resistant to dry and cold conditions (Urquhart

1987). Some species require extrinsic stimuli to hatch, for example the infective larvae of N. battus and N.

filicollis must be subjected to a prolonged period of chill followed by a warmer period. Thus, there may only

be one generation of N. battus and N. filicollis per year (Sutherland & Scott 2010). The other Nematodirus

spp. species do not have the same critical hatching requirements so L3 can appear on the pasture 2-3

months after the eggs have been excreted in faeces and more than one generation of parasites per year is

therefore possible (Urquhart 1987).

Some GIN can inhibit their development at L4 (or L3) stage and persist in hypobiosis until more favorable

conditions when they continue their development. This arrested stage of development is generally seen in

larvae ingested during late autumn and winter (Urquhart 1987). Resumption of larval development can be

induced by environmental factors, e.g. temperature and humidity suitable to the free-living development,

or be triggered by host factors such as depressed immunity or changes in hormone levels around

parturition (Urquhart 1987; Kassai 1999).

There is a minor peak in egg deposition on pasture seen in the spring. The larvae producing these eggs have

over-wintered in the ewes or developed from the ingestion of over-wintered L3 in early spring. A high

infectivity is seen on pastures in the autumn caused by eggs deposited by lambs in spring and early summer

(Taylor 1999). This leads to a minor peak in larval numbers on pasture occurring in late spring and with a

major peak in either summer or autumn, depending on the availability of moisture. This is because the

nematodes complete their life cycle faster in warm and wet conditions. During the colder winter months

fewer eggs develop and during hot dry summer weather many eggs and larvae are killed (Bruère et al.

1993). The minor peak in spring is caused by maturation of over-wintered larvae as well as larvae derived

from the peri-parturient rise in faecal egg counts explained by a temporary drop in immunity of ewes in late

pregnancy and early lactation. Worm numbers in the lambs build up slowly during spring and early summer

and peak in autumn. A rapid decline is seen in the winter when the lambs are 10-12 months of age and is

associated with development of immunity (Brunsdon 1970). Young lambs generally harbor mixed infections

of several species of the five genera discussed above with some seasonal changes in the relative abundance

of each genera. In late spring infections are generally dominated by Nematodirus spp. followed by

Teladorsagia spp., H. contortus and Trichostrongylus spp. in late summer/autumn. Cooperia spp. and T.axei

can occur in large numbers in autumn, but usually persists into winter and form a major part of the worm

burden of the animals in their second year (Brunsdon 1970).

10

GIN infections are characterized by reduced animal performance caused by reductions in both feed intake

and efficiency of feed utilisation (Sykes 1994). Anorexia associated with GIN infection may contribute

between 40% and 90% of the production losses seen in connection with parasitism (Sykes 1987). The cost

of parasitism to an animal may be considered the effects of all parasite species and stages present. It has

been estimated that the cost for an animal to maintain immunity against parasite challenges imposes a 15%

reduction in nutrient utilisation (Sykes 1994). The effects of GIN can be either direct or indirect. The direct

effects are related to the parasites’ metabolic requirements, such as damage of the abomasal mucosa

caused by migrating larvae. The indirect effects arise from the presence of the parasites and the host’s

response to invasion and the consequences of it. The adverse effects of parasitism can affect immune

adults but is generally of greatest importance in young immunologically naïve animals reared at pasture.

The development of immunity to the parasites varies with parasite species however there are some

common characteristics, such as the period of exposure to parasite challenge (Sutherland & Scott 2010). In

sheep, a significant immunity generally develops at an age of 10-12 months (Vlassoff et al. 2001).

Development of immunity require exposure to parasites and the stability of production systems depends

on keeping a balance between allowing adequate exposure to stimulate immunity and the prevention of

pathological damage severe enough to restrict performance (Sykes 1994).

Sheep in New Zealand farming systems are frequently exposed to GIN infections (Vlassoff et al. 2001).

Severe clinical parasitism may lead to sick moribund animals of which some will die despite anthelmintic

treatment with the rest of the mob usually suffering from chronic, subclinical parasitism (Sutherland &

Scott 2010). Although losses from clinical parasitism are still commonly seen, sub-clinical losses are of

greater economic importance (Bruère et al. 1993; Vlassoff et al. 2001). Brunsdon (1970) reported mortality

rates between 10% and 45% in lambs in intensive production systems where the lambs remained untreated

for their first year of life and it has been estimated that one third of New Zealand’s sheep production may

be dependent on anthelmintics for effective control of nematode infections (Vlassoff et al. 2001).

1.2.1 Trichostrongylus spp. Trichostrongylus spp. are very small and hair-like worms, usually less than 7 mm in length. Trichostrongylus

infections are often asymptomatic but when present in large numbers, between 10 000- 100 000 worms,

the parasites cause clinical disease (Bowman & Georgi 2009). T. colubriformis and T. vitrinus live in the

small intestine and cause damage to the intestinal mucosa (Familton & McAnulty 1997) when ingested L3

penetrate the epithelial glands and form tunnels in the mucosa. The tunnels rupture and lead to oedema

and loss of plasma proteins into the lumen of the intestines. Signs of heavy worm burdens are diarrhoea

and rapid weight loss caused by the loss of the plasma proteins. Common signs of lower infections are

inappetence and poor growth rates, sometimes soft faeces (Urquhart 1987). T. axei is the smallest of the

abomasal nematodes (Sutherland & Scott 2010). It lives in the abomasum and causes alteration in the

11

gastric pH and an increased permeability of the mucosa. Clinical signs of infection are ill-thrift, diarrhoea

and weight loss (Urquhart 1987).

Development of immunity varies, as mentioned above, with parasite species. An effective immunity to T.

colubriformis develops within 3-5 months subsequent continued parasite challenge where the immunity

against larvae first develops followed by expelling of the established adult worm burden (Urquhart 1987;

Dobson 1992; Sykes 1994)

1.2.2 Teladorsagia spp. Teladorsagia spp. previously referred to as Ostertagia spp. cause the disease ostertagiosis in sheep. The

adult worms are brownish in colour and up to 14 mm long (Bowman & Georgi 2009). There are two forms

of ostertagiosis, type I and type II. Type I ostertagiosis is acute and typically occurs in lambs during their

first season at grass as a result of ingestion of large numbers of infective larvae over a short time. Clinical

signs are watery diarrhoea, dehydration, loss of appetite and failure to gain weight (Aitken & Martin 2000).

In heavy infection the effects are primarily a reduction in the acidity of the abomasal fluid and an elevation

of the pH. Due to abomasal damage there is a loss of macromolecules such as pepsinogen and

plasmaprotein into the gut lumen leading to hypoalbumaemia and increased levels of pepsinogen in the

plasma. There is also a loss of bacteriostatic effect in the abomasum (Urquhart 1987). Type II ostertagiosis,

the subacute or chronic form for ostertagiosis, may occur in yearlings during late winter or spring when

hypobiotic larvae ingested during the previous autumn mature and break out of the abomasal mucosa and

cause damage to the mucosal wall. Clinical signs are loss of body weight and intermittent diarrhoea (Aitken

& Martin 2000).

Immunity against Teladorsagia circumcincta develops opposite that of Trichostrongylus colubriformis. Here

the immunity to resident adult worms develops initially and the worms are expelled after some time of

residence. This allows maturation of ingested or arrested L3 and L4 which is followed by development of

immunity to the larvae (Dobson 1992 ). Resistance against Teladorsagia spp. is acquired within 3-5 months

(Sykes 1994).

12

1.3 Control of gastrointestinal nematodes

1.3.1 Control based on the use of anthelmintics

1.3.1.1 Anthelmintics and anthelmintic resistance

Anthelmintics drugs are effective in removing existing burdens and preventing the establishment of

ingested L3 (Sutherland & Scott 2010). These drugs remain to be the main control method for

gastrointestinal nematodes in small ruminants, especially the broad spectrum anthelmintics (Kaplan 2004)

(Wolstenholme et al. 2004). Broad spectrum anthelmintics available for veterinary use can be divided into

three groups based on their chemical structure and mode of action; 1) Benzimidazoles; 2)

Imidathiazoles/tetrahydropyrimidines and; 3) Macrocyclic lactones. By combining two or more anthelmintic

families into one product it is possible to extend the spectrum of activity and reach an improved efficacy

(Sutherland & Scott 2010).

Anthelmintic resistance is the ability of an individual to survive the lethal effects of a chemical and is a

result of selection against the genetic variation within the population (Prichard et al. 1980; Martin 1987;

Sutherland & Scott 2010). “Anthelmintic resistance is present when there is a greater frequency of

individuals within a population able to tolerate doses of a compound than in a normal population of the

same species and is heritable” (Prichard 1980). It is a global problem in parasitic nematodes of small

ruminants and a threat to the production and welfare of grazing livestock (Jackson & Coop 2000; Waller

2006; Kaplan 2004). Resistance have been reported in nematodes to all of the broad spectrum

anthelmintics (Prichard 1990). The main contributing factor has been too frequent drenching often with

lower than recommended doses (Aitken & Martin 2000). Other factors affecting the development of

resistance are for example rate of larval intake, egg deposition, grazing management and dominance and

number of resistant alleles in population (Martin 1987; Barnes et al. 1995). As a consequence of

undetected resistance, production losses are likely to occur (Pomroy 2006).

1.3.1.2 The concept of refugia

As the problem with anthelmintic resistance increases one approach to conserving efficacy of the current

anthelmintic is to maintain parasite populations in refugia in order to sustain genetic susceptibility. Refugia

can be defined as a parasite population unexposed to control measure applied, thus escaping selection for

resistance (Besier 2008). In gastrointestinal nematodes this is primarily the free-living stages on pasture or

populations in untreated animals (van Wyk et al. 2006).

There are different ways of achieving refugia in nematode populations, such as, reducing the total numbers

of whole flock treatments (targeted treatments) or reducing the number of treatments through targeting

individuals within a mob and/or herd at any one time (targeted selective treatments), thus leaving a

proportion of animals untreated to create a ‘refuge’ for susceptible worms (Besier 2008). Other methods

13

include incorporating a small number of resilient animals into flocks thus providing untreated nematode

populations, or to leave animals on a contaminated pasture after drenching with an effective anthelmintic.

The population of resistant nematodes is thus diluted by the susceptible worms on pasture (Wyk 2001;

Jackson & Waller 2008).

1.3.1.3 Targeted and targeted selective treatments

Targeted treatments can be defined as optimised whole flock treatments where the approach is to reduce

anthelmintic usage and help maintain worm populations in refugia, hence minimising the resistant

genotypes on pasture (Jackson & Miller 2006; Kenyon et al. 2009). Targeted treatments differ from

strategic treatments in which are generally given prophylactic on the basis of the information about

parasitism in a given area and are used to protect against disease over a substantial period (Kenyon et al.

2009).

Targeted selective treatments (TST) are part flock treatment where only those individuals within a flock

that will gain most benefit from treatment are treated, leaving the rest of the flock untreated (Kenyon et al.

2009). Selective treatments should be aimed at disease susceptible animals. This however requires the

ability to identify these individuals within the flock and the main problem is the risk that some animals will

be left with parasite burdens that can cause clinical disease, production loss and compromised welfare.

A classical example of TST is FAMACHA, a system used for diagnosing haemonchosis. It is based on

assessment of the colour of the lower eyelid mucous membrane to estimate the degree of anaemia so that

treatment can be restricted to those individuals identified being at risk of the disease (Malan et al. 2001). It

has been successfully used in many countries and has shown a reduction in the cost of anthelmintics

compared to whole flock treatment although the effort needed to identify animals requiring treatment

must be simplified as much as possible for wide adoption to be achieved as this may be a limitation in

larger flocks (Molento et al. 2004). In areas where non-haematophagous parasites or other anemia-causing

pathogens are dominant species the FAMACHA system is not a well suited TST indicator and finding

suitable indicators for identifying animals in need of treatment is more challenging (Besier 2008). An ideal

indicator for use in targeted selective treatments would be quick, repeatable, cost effective and relevant

(Kenyon et al. 2009). Several methods have been suggested ranging from visually identifying animals

suffering from ill-thrift (with poorest body condition and clinical appearance, “poor doers”), to using dag

scores, faecal egg count (FEC), milk production and liveweight gain (LWG) (Wyk 2001; Besier 2008; Stafford

et al. 2009). Recent studies based on a model using a threshold of liveweight gain as an indicator for

treatment in lambs (the Happy factor model), calculated from their relative efficiency of energy utilisation

and taking factors such as temperature, feed quality and availability into account, showed a halving of the

numbers of anthelmintic treatments and small or no loss of production compared to a whole flock

14

treatment (Greer et al. 2009; Greer et al. 2010). An efficiency of energy utilisation is calculated as 1, less

this inefficiency in the model. By adjusting for environmental conditions this gives a Happy factor value.

Liveweight gain was the only parameter of the ones measured in these studies (besides liveweight gain also

liveweight and FEC) that consistently varied between sheep requiring and not requiring treatment and this

suggests that the Happy factor model can identify underperforming animals and that liveweight gain can be

used as an indicator for individual treatment (Greer et al. 2010).

1.3.2 Non-chemical control of gastrointestinal nematodes The increasing prevalence of anthelmintic resistance has urged the research about non-chemical control

methods in order to reduce the reliance of anthelmintics. The different methods either target the parasite

population in the host; e.g. via supplementary feeding, vaccination or use of bioactive forages, or on

pasture by using grazing management or predatory fungi (Jackson & Miller 2006).

1.3.2.1 Grazing management

Grazing management has been used to minimise the threat of nematode infestations in livestock for over

40 years (Jackson et al. 2009). The aim of grazing management is to provide clean pastures where stock can

graze safely (Barger 1999). Various forms of grazing management have been classified as being either

preventive, evasive or dilutive (Barger 1997).

Preventive strategies include introducing unaffected animals to a parasite free or clean pasture and

preventing infections from building up, or suppressing egg output by anthelmintic treatment in the early

part of the grazing season until the infective larvae level on pasture has declined to a safe level (Barger

1997; Thamsborg et al. 1999; Barger 1999). Clean pastures can be provided by alternate grazing between

two different species, not sharing the same parasite species, or by use of hay or silage aftermath, crops or

new pastures (Thamsborg et al. 1999). Especially in temperate areas this alternate grazing, most commonly

used with sheep and cattle, has achieved benefits for worm control. There have however been reports of

parasites of cattle infecting sheep and therefore a cautionary note should be taken when relying on these

strategies (Barger 1999).

Evasive grazing strategies, in contrast to the preventive, do not aim at restricting the contamination on

pasture but rather attempt to avoid parasitic infections by moving stock to a clean pasture before the eggs

contaminating the original pasture are likely to appear in substantial numbers (Barger 1997). Rotational

grazing is used as an evasive approach which involves the subdivision of a pasture where each section is

grazed for a short time and then spelled for a much longer period. It may be feasible to apply this in tropical

areas where development and survival time of nematode larvae is short, however a problem is to achieve a

short enough grazing time to prevent auto-infection within the grazing area since development from egg to

infective larvae can take as little as 4-5 days and their longevity is much shorter. Hence not many grazing

15

management schemes are seen in the tropics. Rotational grazing in temperate areas is generally considered

ineffective because the development and survival time of infective larvae on pasture are greatly influenced

by variations in temperature and moisture and are relatively much longer than in the tropics. Here it may

be a problem to achieve a long enough rotation length that the greater part of the larvae from the previous

grazing has died off (Barger 1999).

Dilution is a form for non anthelmintic control by grazing young susceptible animals with parasitologically

inert animals, either animals from a different species or older animals from the same species. Dilution can

also be achieved by reducing the number of animals in a given area (Thamsborg et al. 1999). Lambs and

hoggets are usually the main contributor to pasture contamination and display the most obvious effects of

parasitism. Parasitic disease may therefore be reduced simply by reducing the proportion of these animals

in a flock (Bruère et al. 1993). Until relatively recently it was highly recommended to use anthelmintic

treatment with all of the mentioned grazing strategies (Waller 2006).

1.3.2.2 Supplementary feeding

Several studies have shown that improved nutrition reduces production losses and mortality rates due to

nematode parasitism in livestock (Waller 1999; van Houtert & Sykes 1996). Supplementary feeding of

infected lambs with dietary protein has been shown to reduce the parasite burdens as a consequence of

enhanced immune response (Coop & Kyriazakis 2001; Sykes & Coop 2001). It is also believed to enhance

the ability of the infected host to repair mucosal damage (Stear et al. 2007). In addition to protein

supplementation it has also been found that some trace elements including copper, iron, zinc and

molybdenum influence host resistance to nematode infection (Koski & Scott 2003).

Supplementary feeding is a successful and valuable method of controlling nematode parasitism in sheep.

The barriers to more widespread adoption are mainly financial (Stear et al. 2007) and further research is

needed before nutritional manipulation can be exploited within the diverse production system that are

used by farmers (Jackson & Miller 2006).

1.3.2.3 Bioactive forages

The effect of bioactive forages against parasitism is considered to be caused by plant secondary

metabolites (PSM). The mode of action of these forages is not clear and is most likely different according to

type of forage. Two hypothesis are considered; the first suggesting that PSM have a direct anthelmintic-like

effect on larval and/or adult parasites, the second hypothesis suggesting that some PSM may have an

indirect effect by protecting the plant protein from degradation by the microorganisms in the rumen, hence

increasing the amount of protein reaching the small intestine which may stimulate the immune system (

Barry & McNabb 1999; Molan et al. 2003). In addition to their anthelmintic properties PSM also have anti-

nutritional properties, such as toxicity that may manifest as tissue damage, inhibited digestibility,

16

disruption of mineral balance and diurese. Whether the antiparasitic effects can outweigh the anti-

nutritional consequences depends on the strength of the effects of PSM (Athanasiadou & Kyriazakis 2004).

Many studies have focused on forages containing condensed tannins (CT) believed to have some

antiparasitic activity (Waghorn et al. 2006). It has been shown that consumption of tannin-rich forages is

associated with an improvement of host resistance and/or resilience (Heckendorn et al. 2007; Brunet et al.

2008; Athanasiadou et al. 2007). The results from tannin-rich plants seem to vary with nematode species.

Athanasiadou et al. (2000; 2001) reported a reduction in worm numbers in intestinal species whereas no

effect was seen in the abomasal species H.contortus and T.circumcincta. Recent studies have clearly

indicated a direct anthelmintic effect of tannin-rich forages with a reducing effect on adult worm

populations and a reduction in egg contamination on pasture on abomasal nematodes (Athanasiadou et al.

2007; Martinez-Ortiz-de-Montellano et al. 2010; Mupeyo et al. 2011). It is hypothesised that CT in a direct

mode of action react with the surface proteins on the nematodes and disturb their normal physiological

functions such as mobility, food absorptions and reproduction. CT has furthermore been considered to

have an indirect effect on immunity of the host. Since nematode parasitism lead to loss of protein and

decreased protein absorption, intake of tannin-rich plants may counteract protein losses and stimulate the

immune system. In most studies it has been difficult to determine whether the improvement of host

resistance and/ or resilience is due to improved nutrition or the role of specific biochemical compounds

(Hoste et al. 2006).

Other secondary metabolites have also been associated with anthelmintic properties. For example,

sesquiterpene lactones which are meant to be the main responsible PSM for the anthelmintic activity of

chicory forage (Molan et al. 2003). Chicory is a bioactive plant with a high nutritive value and it contains a

range of secondary metabolites but only a low content of CT (Molan et al. 2003). It is found to grow well

and appears to consistently reduce abomasal worm burdens of lambs grazing on it however, it appears not

to have an affect on intestinal worm burdens (Nietzen et al. 1993; Scales et al. 1995; Marley et al. 2003;

Tzamaloukas et al. 2005). Kidane et al. (2010) documented a lower FEC in T.circumcincta infected lambs

and ewes grazing chicory versus grass/clover and Miller et al. (2011) reported that lambs grazing chicory

and infected with H. contortus consistently exhibited a lower FEC compared to their contemporaries

grazing bermudagrass. Furthermore a reduced egg production of H. contortus and a tendency for reduced

worm burden has been documented after just two weeks in parasitised animals fed chicory (Heckendorn et

al. 2007). In a medium-term grazing trial Marley et al. (2003) observed no effect on FEC when feeding

lambs chicory however a reduction in the number of adult abomasal worms in lambs after 35 days of

grazing the forages compared to lambs grazing ryegrass/white clover was observed whereas Tzamaloukas

et al. (2005) reported a significant reduction of adult worm burden after only two weeks in sheep and

infected with T.circumcincta. Several studies have shown an increased performance in lambs grazing

17

chicory compared to other grass species suggesting increased resilience (the ability to withstand the effects

of infection to parasitism) (Nietzen et al. 1993; Scales et al. 1995;Marley et al. 2003; Athanasiadou et al.

2005; Athanasiadou et al. 2007; Miller et al. 2011). The delivery methods of the bioactive forages can vary

from purified plant bioactive compounds to grazing the plants in the paddock including; drenching with

partially purified or crude plant extract, incorporation of processed crude plant material into feed pellets or

solutions, application of plant material (fresh, processed or preserved) to the paddock/feedlot and growth

of plants in the field. Factors affecting the delivery options of the bioactives can be; compound stability,

potency, bioavailability, what type of plant the bioactives come from and seasonal and environmental

factors (Rochfort et al. 2008).

Alternatively, bioactive forages can be offered as fresh herbage to grazing animals. However, the adoption

of alternative forages such as chicory or plantain in extensive New Zealand production systems has been

low. In part, this reflects the relatively weak agronomical qualities of these forages, which include poor

persistence, delicate grazing management and poor matching of growth to animal demand due to its

relatively high thermal requirement as subsequent slow growth in spring when animals are lactating.

Consequently, although there are some animal health benefits to growing and feeding such forages, it is

simply impractical for farmers to have areas of their farm dedicated to growing either chicory or plantain

that are sufficiently large enough for all of their stock. However, if only a proportion of the animals needed

to be grazing such forages at any one time then both chicory and/or plantain may provide a useful tool in

reducing the reliance on anthelmintics (Greer 2012 personal communication).

1.3.3 Integrated control Integrated control is based on a combination of suitable control systems to achieve effective parasite

control and reduce the use of anthelmintics to an absolute minimum (Thamsborg et al. 1999; Kahn &

Woodgate 2012).With the growing problem of anthelmintic resistance there is a need for other substantial

control methods (Hoste & Torres-Acosta 2011). By combining two or more less effective control methods it

may be possible to reduce infection levels substantially and reach appropriate control (Thamsborg et al.

1999). Examples of integrated control, additional to strategic use of anthelmintics at appropriate times,

include different forms of grazing management (to avoid heavy challenge by worm larvae), to breed sheep

for worm resistance, monitor worm egg counts, leave animals in refugia and, when feasible, use biological

control (Woodgate & Besier 2010; Woodgate & Besier 2010; Woodgate & Besier 2010).

The aim of integrated control is to limit the rate of infection in young lambs by preventing dangerous

numbers of infective larvae from building up on pasture by limiting the deposition of contamination and to

limit the rate of infection by removing the lambs from contaminated areas before a large number of

infective larvae occur (Vlassoff 1979). An early example of integrated control and a commonly used

18

strategy has been the “drench and move” system. Here the animals are treated with anthelmintics before

being moved onto a safe pasture (a pasture with low or zero numbers of L3) after drenching. This strategy

has been found to be highly effective for controlling gastrointestinal nematodes and keeping infection

levels low, however it has also been shown to select strongly for anthelmintic resistance in the surviving

parasites (Barger 1999; Wyk 2001). Frequent drenching is commonly considered to be sufficient to remove

effects of parasitism, but there is evidence that the effect of nematodes on performance is not entirely

removed by regular drenching (Brunsdon 1976) although it may reduce larval contamination of pastures

(McAnulty et al. 1982; Thompson et al. 1982). Brunsdon (1976) showed that lambs that were drenched and

moved to a safe pasture had an eight times higher liveweight gain than lambs that were drenched and

moved to a “dirty” pasture. It’s been observed significant reductions in liveweight gains in heavily infected

lambs (Symons et al. 1982; Thamsborg & Agergaard 2002). When lambs on pasture are exposed to a larvae

number high enough this may lead to anorexia and reduced performance (Thamsborg & Agergaard 2002).

Large production losses due to reduction in food consumption and utilisation have been found in

connection with larval challenge (Steel et al. 1982; Symons et al. 1982; Thamsborg & Agergaard 2002).

McAnulty et al. (1982) states that pasture contamination is the major factor responsible for reduced

liveweight gain and maximum animal performance can only be achieved in production systems with low

levels of pasture contamination. Reducing larval contamination on pasture therefore appears to play a key

role in reducing production losses in livestock (Brunsdon 1980). A reduced larval uptake can reduce the

effects of parasitism on performance in parasite-naïve lambs significantly (Coop et al. 1982). Several studies

have shown that lambs with a reduced food intake and liveweight gain due to parasitism had an increased

appetite and performance when larval challenge was removed (Coop et al. 1982; Symons et al. 1982;

Kyriazakis et al. 1996). In organic farming preventive use of anthelmintics is not possible and accordingly

integrated methods are likely to be the best control (Thamsborg et al. 1999). According to Waller (1999)

and Jackson (2006) integrated approaches to the control of nematode parasites is the only way to ensure

the sustainability of parasite control in the future. To date only a few studies have tested the combined use

of more than one method to suit the needs of different farming conditions (Hoste & Torres-Acosta 2011).

Integrated approaches such as the provision of a hospital area that has both minimal larval contamination

and the presence of bioactive herbs and/or forages may provide a useful integrated approach for use in

organic systems. Further, through targeting the use of such areas only to those animals that are most in

need, such areas could be optimally utilised while at the same time preserving the

longevity of the forages present (Greer 2012 personal communication).

19

Section II: Own investigations

II.1 Introduction and objectives Nematode parasitism of small ruminants is a major threat to ruminant productions throughout the world

(Waller 1997; Jackson & Coop 2000; Waller 2006). The availability of highly effective and cheap

anthelmintics has resulted in a worldwide problem with anthelmintic resistance due to the frequent use of

these drugs (Waller 1997). Because of the increasing anthelmintic resistance and the requirement for

reduced anthelmintic usage in organic production systems as well as the increasing concern of consumers

for drug residues in animal products there is a need for a sustainable alternative to anthelmintics in small

ruminant production systems (Waller 1999; Athanasiadou et al. 2005).

There have been field studies which suggest that grazing sheep on certain bioactive forages might reduce

their worm burdens compared to grazing sheep on conventional forage (Marley et al. 2003; Tzamaloukas et

al. 2005; Waller 2006; Athanasiadou et al. 2007; Brunet et al. 2008; Lira et al. 2008). The mode of action of

these forages is not however clear and is most likely different according to the type of forage but may also

be, at least in part, associated with the reduced larval challenge due to plant morphology and/or the

bioactive properties. Basically, an indirect effect as a consequence of nutritional effects upon immunity or a

direct anthelmintic-like effect could be considered (Hoste et al. 2006). Recent studies on tannin-rich forages

have clearly indicated a direct anthelmintic effect (Martinez-Ortiz-de-Montellano et al. 2010; Mupeyo et al.

2011). There are many approaches like this currently being investigated, but none are as effective as

anthelmintics and none of these will treat life-threatening disease. As non-chemical anthelmintic control

methods become available and widely used, anthelmintics will still be required for life-saving therapy when

alternative parasite control is unsuccessful (Kaplan 2004; Jackson et al. 2009) and should therefore be

considered highly valuable and limited resources to be preserved (Waller 1999). A combination of

development of non-chemical approaches that decrease the need for treatment and a more restricted use

of effective anthelmintics could be a realistic strategy for sustainable nematode parasite control (Waller

2006; Jackson et al. 2009).

The objective of this study was to evaluate the effectiveness of targeted selective treatment using strategic

short term grazing on chicory, plantain and red clover for effect on faecal egg count and liveweight gain in

organically reared lambs.

20

II.2 Materials and methods

2.1 Experimental design, study area and animals The trial was performed at the Biological Husbandry Unit of Lincoln University, Canterbury, New Zealand

during December 2011- March 2012. The experimental site had not been grazed by animals over the last 20

years or longer and hence was virtually worm-free. The area was divided into four paddocks (5 ha

altogether) (fig. 2); two main paddocks (1.6 and 2 ha respectively) sown with ryegrass (Lolium perenne cv.

Grasslands Nui) and white clover (Trifolium repens cv. Grasslands Huia) (Paddocks TCIR and TCOL) and two

smaller “hospital paddocks” (each about 0.7 ha) sown with ryegrass and a herb mix of chicory (Cichorium

intybus cv. Grasslands Puna), plantain (Plantago lanceolata cv. Grasslands Lancelot) and red clover

(Trifolium pratense cv. Minshan) (Paddocks H-TCIR and H-TCOL). 12 weeks prior to the start of trial each

main paddock was grazed by fifteen peri-parturient ewes which lambed on the paddocks. The ewes were

treated with anthelmintic, a mixture of abamectin (1g/l), albendazol (25g/l) and levamisol hydrochloride

(40g/l) (1 ml per 5 kg liveweight orally; Trio® Sheep, Ravensdown Animals Health, Christchurch) to remove

any residual parasite burden before being artificially infected with either Trichostrongylus colubriformis

(Paddock TCOL) or Teladorsagia circumcincta (Paddock TCIR) within seven days of lambing and kept on the

pastures for four weeks to seed the pastures with monospecific contamination. The ewes and their lambs

were removed before the trial started. The hospital paddocks were sown in the autumn and resown in the

spring (September) due to weed contamination. They were mown once in early February to maintain

pasture quality. In early February an irrigation system was set up in the hospital paddocks to increase the

growth of the forages.

Fig. 2. Schematic picture of the trial site. TCOL =paddocks grazed by lambs infected with Trichostrongylus colubriformis; TCIR = paddocks grazed by lambs infected with Teladorsagia circumcincta.

Sixty male Coopworth lambs with a mean liveweight of 27.0 kg (SD: 3.4 kg) and age of 12 weeks were

included in the study and arrived on 06 December 2011 (week 0). The lambs had been reared under normal

commercial conditions at the Lincoln University, Ashley Dene Research Farm and had been weaned on the

day of arrival. The lambs were drenched with a mixture of abamectin (1g/l), albendazol (25g/l) and

21

levamisol hydrochloride (40g/l) (1 ml per 5 kg liveweight orally; Trio® Sheep, Ravensdown Animals Health,

Christchurch) the same day and put in a quarantine area for two days. The lambs were fitted with

electronic ear tags and allocated hierarchically by liveweight into one of two groups of thirty lambs. The

groups were introduced to two separate paddocks with ryegrass and white clover contaminated with either

T.colubriformis or T. circumcincta and allowed to adjust for one week. From one week after entry into the

paddocks, on a fortnightly basis the liveweight gain of the lambs was assessed with individuals not

performing to a preset target removed and grazed on a separate paddock with herbs and minimal larval

contamination (hospital paddock). The target liveweight for each lamb was calculated at each weighing

following measurement of herbage mass and estimation of quality which allowed for the calculation of the

“Happy Factor” grazing efficiency as described by Greer et al. (2009). Target weights were calculated

assuming a happy factor of 0.74 (Greer et al., 2010) which were then uploaded onto a Tru-test head unit

(XR3000, Tru-Test Ltd, New Zealand). At the time of weight recording, animals were drafted according to

their ability to reach their target liveweight gains. The lambs from each parasite-species infected pasture

that achieved their target level of performance were returned to pasture. Those that did not reach their

performance target at each sampling time were drafted out and put to graze in the hospital area for the

next two week period. The study was terminated after 15 weeks on 16 March 2012.

The main pasture paddocks were rotationally grazed, with animals spending one week in each quadrant.

Animals were set-stocked in the hospital paddocks. Pre-grazing and post-grazing herbage masses were

collected on a weekly basis for all paddocks that either had been, or were about to be grazed. Pasture mass

was measured using a FILIP’s rising plate pasture meter (JENQUIP, Feilding, New Zealand) with

measurements taken every ten paces in a ‘W’ pattern down the field. The rising plate meter was calibrated

using eight forage cuts from each pasture taken using a quadrate (0.2m2). The dry matter (DM) of each

fraction was determined following drying the samples in an oven at 70 °C for 48 hours. The pasture mass

was estimated using the rising plate meter and a linear calibrations equation: y = 150x + c where y =

pasture mass (kg DM/ha), x = plate meter reading (counts/click) and c = a constant.

For calibration of the pasture meter these values were compared with the pasture mass determined by the

quadrate cutting. The pasture mass (kg DM per ha) was measured at every grazing rotation using the rising

plate meter and used for estimating the targeted liveweight of the lambs according to the Happy Factor

model (Greer et al. 2009).

Typical summer temperatures in the Canterbury region are warm. The mean rainfall is low and long dry

spells can occur. The summer 2011/2012 was cooler than average and dry. Mean daily temperature was

15.7˚C and mean rainfall 55 mm per month (NIWA Taihuru Nukurangi 2012). Meteorological data was not

recorded during the trial but irrigation was used from mid February to assist with maintain pasture quality

and growth in addition to parasite survival.

22

2.2 Sampling and analysis A pasture dissection of the hospital paddocks was performed every fortnight. Samples were collected at

random from the two paddocks with the procedure being one sample for every ten steps taken when

traversing the paddock in a ‘W’ pattern. Samples were placed into a plastic bag and later dried in an oven at

a temperature of 70°C for a period of 48 hours after which they were weighed and sorted according to their

individual species; ryegrass, clover, chicory, plantain and weed. Finally each different species was weighed

and the respective percentage of the entire sample calculated (% DM).

Pasture larval samples were collected and analysed once a week. The samples were collected at each

rotation shift from both the currently grazed areas and from the last grazed areas using the same sampling

technique as for pasture dissection discussed above. Pasture larval counts were thereafter performed using

a modified Baermann technique. Each sample was placed in a plastic bag and filled with 3 l of lukewarm

water. The bag was tied and washed in a small hand operated centrifuge. The centrifuge was operated at

230 rpm for 3 minutes. The grass was then removed from the bag and placed to dry in an oven for 48 hours

at 70 °C for future analysis of the dry matter. The bag was thoroughly washed and the water poured into a

beaker. The sample was refrigerated for 24 hours, siphoned down twice and refrigerated for 4 hours in

between. After the second time, the sediment was poured onto a filter paper and allowed to dry until all

the surface water had disappeared. The filter paper then was inverted and placed on a Baermann filter

funnel filled with lukewarm water. The sample was set in room temperature for 36 hours and then poured

into a 100 ml glass bottle which was refrigerated for 4 hours. Following refrigeration the sample was

siphoned down to approximately 10 ml and water was added until 20 ml. 1 ml was placed in a counting

chamber and a drop of iodine was added. The L3 parasitic larvae were counted and differentiated from free

living larvae microscopically by looking for four features typical for parasitic nematode larvae; presence of

sheath (double membrane), stain retention, completely enclosed anterior and posterior orifices and

presence of tail sheath. Two readings were performed for each sample and expressed as L3/kg dry herbage.

To determine the extent of parasitic infection, faecal samples were collected directly from the rectum of all

lambs 10 days after drenching upon entry to the experimental area and then at each fortnightly

sampling/weighing time thereafter. Following collection the samples were refrigerated at 4°C and the

faecal egg count (FEC) was determined within two days of collection using a modified McMaster technique.

Briefly, 1.7 grams of faeces was placed in a glass jar. 10 ml water was added and every sample was

homogenized to ensure that the eggs were uniformly distributed throughout the sample prior to

determination. Saturated NaCl was added as a flotation medium and a counting chamber was filled with a

subsample. The chamber was allowed to stand for a few minutes to allow the eggs to float to the surface

before the eggs were counted microscopically. Each egg counted was equivalent to 100 eggs/gram of

faeces (epg).

23

2.3 Data handling and statistical analysis Data was analysed using GENSTAT statistical package (GENSTAT 2010. GenStat Twelfth edition, version

12.2.0.3717. VSN International Limited, United Kingdom). Liveweight gain and faecal egg count were

analysed separately for each sampling time and for each nematode by analysis of variance (ANOVA) with

the paddocks (main vs. hospital), before/after (for LWG the fortnight before and after entry of paddock) as

explanatory variables, including their interactions. For the hospital paddocks further analyses were

performed comparing liveweight (LW), LWG and FEC for different time in the paddocks. Groups of 2 weeks,

4 weeks and “6 weeks or longer” were used. Each sampling was analysed as an independent event ignoring

previous drafting history. FEC were log transformed (log10 (n+1) prior to analysis to obtain a normal

distribution. The correlations between FEC and LWG were analysed in a linear regression in Microsoft

Office Excel 2007.

II.3 Results

3.1 Clinical and other observations Pasture dissection of the hospital paddocks (fig. 3 and 4), show an overall poor growth of clover, chicory

and plantain through the whole trial in both paddocks with ryegrass consistently contributing to greater

than 50% of the dry matter present. The proportion of clover and plantain increased from mid February

but each remained at less than 20% of the DM.

Fig. 3. The distribution of the different species found in the H-TCIR paddock At pasture dissections performed throughout the trial (% of DM).

H-TCIR= hospital paddock grazed by sheep infected with T. circumcinta

Fig. 4. The distribution of the different species found in the H-TCOL paddock at pasture dissections performed throughout the trial (% of DM).

H-TCOL= hospital paddock grazed by sheep infected with T. colubriformis

0102030405060708090

100

Ryegrass (%) Clover (%) Plantain (%) Chicory (%) Weed (%)

Pe

rce

nta

ge

Pasture dissection H-TCIR 14.12.2012

18-01-2012

25-01-2012

02-02-2012

09-02-2012

29-02-2012

0102030405060708090

100

Ryegrass (%) Clover (%) Plantain (%) Chicory (%) Weed (%)

Pe

rce

nta

ge

Pasture dissection H-TCOL 14-12 2012

18-01-2012

25-01-2012

02-02-2012

09-02-2012

29-02-2012

24

The pasture mass was in general higher for the TCIR and TCOL paddocks than for H-TCIR and H-TCOL

throughout the trial with a decrease seen in January, mid February and mid March and an increase in early

February for both main paddocks. The pasture mass per ha for the hospital paddocks were even and

constant throughout the trial (Fig. 5).

Fig. 5. Pasture mass registrations for TCOL, TCIR, H-TCOL and H-TCIR paddocks throughout the trial.

From the middle of January a problem with myiasis (flystrike) arose amongst the lambs and continued

throughout the trial. The affected lambs were crutched and treated cutaneously with Tea tree oil.

Five lambs died during January and February. They were all from the Teladorsagia infected group.

Lambs that were visually judged to be in too poor a condition were drenched with a mix of abamectin

(1g/l), albendazol (25g/l) and levamisol hydrochloride (40g/l) (1 ml per 5 kg liveweight orally; Trio® Sheep,

Christchurch) and hereafter put in the quarantine areas for 48 hours. 3 Trichostrongylus infected lambs and

13 Teladorsagia infected lambs were drenched in total.

The numbers of animals from each parasite species pasture, or respective hospital paddock that were

either returned to pasture or designated to graze the hospital paddock are given in table 1.

Day of trial H-TCIR (n) TCIR (n) H-TCOL (n) TCOL(n)

22 6 (6) 24 (17) 2 (1) 28 (16) 36 20 (6) 8 (6) 13(5) 17 (14) 50 3 (3) 24 (17) 8 (5) 22 (10) 64 7 (6) 20 (6) 17 (13) 13 (6) 78 15 (15) 10 (1) 20 (4) 10 (10) 92 20 5 4 26

Table 1. Distribution of the lambs drafted into the different paddocks (H-TCIR/TCIR/H-TCOL/TCOL) at every sampling time. The numbers in brackets indicate how many of the lambs that stayed in

the same paddock for the next grazing period.

The TCIR paddock was 0.4 ha smaller than the TCOL paddock (fig.2) hence the stocking rate was higher

most of the time.

Table 2 shows the distribution of lambs staying for different lengths of periods in the hospital paddocks.

47% and 58 % of the lambs in H-TCIR respectively H-TCOL returned to graze the main paddocks after two

weeks. 40% of the lambs in H-TCIR and 23% in H-TCOL stayed in the hospital paddocks for four weeks and

0

2000

4000

6000

06-12-2011 06-01-2012 06-02-2012 06-03-2012

Pas

ture

mas

s (k

gDM

/ha)

Date

Pasture mass for TCIR, TCOL, H-TCIR and H-TCOL TCIR

TCOL

H-TCIR

H-TCOL

25

13% respectively 19% stayed for six weeks or longer. There were lambs grazing the hospital paddocks at all

times whilst the main paddocks were rotationally grazed.

Time in hospital paddocks

Paddock 0 weeks 2 weeks 4 weeks 6 weeks 8 weeks 10 weeks 12 weeks Total

H-TCIR (n) 0 22 19 3 1 1 1 47

H-TCOL (n) 3 21 8 3 2 2 0 39 Table 2. Distribution of lambs staying in H-TCIR and H-TCOL for different periods of time.

Results from the pasture larval count were incomplete on the day of writing due to illness, too high a work

load for the laboratory staff and lack of time and are therefore not displayed in this section.

3.2 Performance of hospitalised animals The mean daily liveweight gains, estimated over fortnightly periods (light green bars in fig. 6-7), were

significantly different between TCIR and H-TCIR (p<0.05) as well as TCOL and H-TCOL (p<0.01) at every

sampling time. The overall mean LWGs were 0.252 kg/day and -0.077 kg/day for TCIR and H-TCIR

respectively and 0.292 kg/day and -0.035 kg/day for TCOL and H-TCOL. The mean LWGs were thus

consistently lower for the lambs in the hospital paddocks than for their counterparts. The results of the

ANOVA are summarized as p-values for TCIR/H-TCIR and TCOL/H-TCOL in Tables 3 and 4, respectively.

For T. circumcincta infections, there were paddock x time interactions at sample time 1 and 2 (p<0.05) and

a tendency for an interaction at time 3 (p=0.073) (Table 3) that reflected a benefit of hospitalisation on the

LWG, while the LWG of those remaining on pasture was decreased or not affected. For T. colubriformis

infected animals there were significant interactions between paddocks and time on sampling time 2

(p<0.05) and 3 (p<0.01) (Table 4)for TCOL and H-TCOL reflecting beneficial effects on LWG in hospitalised

animals with a decrease or no difference in non-hospitalised animals.

LWG p-value (1) day 22-36

p-value (2) day 36-50




Paddock (TCIR/H-TCIR) 0.056 0.645 0.270 0.236 0.776 Time (before/after) <0.001 0.895 0.393 0.617 0.794

Paddock x Time 0.020 0.019 0.073 0.479 0.831

n1/n2 24/6 8/20 24/3 20/7 10/15

Table 3. The statistical output for an ANOVA comparing mean LWG before and after time in T-CIR and H-TCIR paddocks on the five sampling times. n1 =number of lambs in TCIR, n2=number of lambs in H-TCIR.

Numbers in brackets indicate the sampling time. P-values indicate the level of significance.

LWG p-value (1) day 22-36





Paddock (TCOL/H-TCOL) 0.050 <0.001 <0.001 <0.001 <0.001 Time (before/after) <0.001 0.745 0.020 0.827 <0.001

Paddock x Time 0.228 0.033 0.003 0.246 0.107

n1/n2 28/2 17/13 22/8 13/17 10/20

Table 4.The statistical output for an ANOVA comparing mean LWG before and after time in T-COL and H-TCOL paddocks on the five sampling times. n1=number of lambs in TCOL, n2=number of lambs in H-TCOL.

Numbers in brackets indicate the sampling time. P-values indicate the level of significance.

26

Fig. 6. Mean daily liveweight gain for TCIR and H-TCIR estimated over fortnightly periods; two weeks before entry of the paddocks and two weeks after entry.

Fig. 7. Mean daily liveweight gain for TCOL and H-TCOL estimated over fortnightly periods; two weeks before entry of the paddocks and two weeks after entry.

Overall, FEC increased for all four groups after the first grazing period. The mean FEC was low (<500 epg)

on the first sampling time for TCIR and H-TCIR as well as TCOL and H-TCOL. It was moderate (600-2000 epg)

for TCOL and H-TCOL on all other occasions and for TCIR on day 78 and 92. On the rest of the sampling

times the mean FEC for TCIR and H-TCIR was high (>2000 epg). FEC classes according to McKenna (1981).

There was only a significant difference in mean faecal egg count (FEC) between the animals in the TCIR and

H-TCIR paddocks on day 78 (p<0.01) and on day 36 (p<0.05) between the TCOL and H-TCOL paddocks (light

green bars in fig. 8 and 9). There were no significant interactions between paddock and time on any

occasions. The individual FEC decreased for lambs during time in the hospital paddocks in 11 of 35

occasions (31%) for H-TCOL lambs and in 21 out of 41 occasions (51%) for H-TCIR lambs (Appendix V).

Fig. 8. Arithmetic mean faecal egg count for TCIR at the start and end of each grazing period. H indicates hospital paddock. * indicates significant difference (p<0.01) between TCIR and H-TCIR.

Note that there are different animals in each group at every sampling time.

-0,4

0,1

0,6

22-36 36-50 50-64 64-78 78-92

Live

we

igh

t ga

in (

kg/d

ay)

Days of trial

Mean liveweight gain TCIR/H-TCIR

before

after

H H H

H H

-0,4

-0,2

0

0,2

0,4

0,6

0,8

22-36 36-50 50-64 64-78 78-92Live

we

igh

t ga

in

(kg/

day

)

Days of trial

Mean liveweight gain TCOL/H-TCOL

before

after

H H H H H

0

2000

4000

6000

8000

10000

22-36 36-50 50-64 64-78 78-92

FEC

(e

ggs/

gram

)

Days of trial

Mean faecal egg count TCIR/H-TCIR

start finish

H H H H H

*

27

Fig. 9. Arithmetic mean faecal egg count for TCOL at the start and end of each grazing period. H indicates hospital paddock. *indicates significant difference (p<0.05) between TCOL and H-TCOL.

Note that there are different animals in each group at every sampling time.

There was a very weak negative association between FEC and LWG for both TCIR/H-TCIR and TCOL/H-TCOL;

the coefficient of determination, R2, was low for both groups (fig. 10 and 11).

Fig. 10. Linear regression indicating the correlation between liveweight gain and FEC of all lambs in the TCIR and H-TCIR paddocks.

Fig. 11. Linear regression indicating the correlation between liveweight gain and FEC of all lambs in the TCOL and H-TCOL paddocks.

0

2000

4000

6000

8000

10000

22-36 36-50 50-64 64-78 78-92

FEC

(e

ggs/

gram

)

Days of trial

Mean faecal egg count TCOL/H-TCOL

start

finishH H H H H

*

y = -3E-05x + 0,1414 R² = 0,1221

-1-0,8-0,6-0,4-0,2

00,20,40,60,8

1

0 5000 10000 15000 20000

LWG

(kg

/day

)

FEC (eggs/gram)

Correlation between FEC and liveweight gain TCIR/H-TCIR

y = -5E-05x + 0,2241 R² = 0,0824

-1-0,8-0,6-0,4-0,2

00,20,40,60,8

1

0 5000 10000 15000 20000

LWG

(kg

/day

)

FEC (eggs/gram)

Correlation between FEC and liveweight gain TCOL/H-TCOL

28

3.2.1 Factors affecting time spent in hospital paddock There were no significant differences (p>0.05) in mean liveweight of lambs at entry of the hospital

paddocks when comparing the groups staying at different length of periods in the paddocks (2 weeks,

4 weeks, 6 weeks or more) for neither H-TCIR (fig. 12) nor H-TCOL (fig.13).

Fig. 12. Mean liveweight of H-TCIR lambs at entry of the hospital paddock for different lengths of periods, from 2-12 weeks. The numbers in brackets above the bars indicate how many lambs were in each group.

Fig. 13. Mean liveweight of H-TCOL lambs at entry of the hospital paddock for different lengths of periods, from 2-10 weeks. The numbers in brackets above the bars indicate how many lambs were in each group.

When comparing mean LWGs (estimated over two weeks before entry of the paddock) in lambs that spent

different length of periods in the hospital paddocks (2 weeks, 4 weeks, 6 weeks or more) there were no

significant differences (p>0.05) between the different groups for H-TCIR (fig. 14). The lambs in the H-TCOL

paddock that stayed for 6 weeks or more had a lower liveweight gain than the other groups (fig.15).

Fig. 14. Mean daily liveweight gain of lambs in the H-TCIR paddock for different periods, from 2-12 weeks, measured of day of entry of the hospital paddock. The numbers

in brackets above the bars indicate how many lambs were in each group.

0

10

20

30

40

2 4 6 8 10 12

LW (

kg)

Number of weeks in hospital paddock

Mean liveweight H-TCIR (22)

(19) (3) (1)

(1) (1)

010203040

2 4 6 8 10

LW (

kg)


Mean liveweight H-TCOL (21) (8) (3)

(2) (2)

-0,15-0,1

-0,050

0,050,1

0,150,2

2 4 6 8 10 12

LWG

(kg

/day

)


Mean liveweight gain H-TCIR

(19) (3)

(1) (1) (1)

(22)

29

Fig. 15. Mean daily liveweight gain of lambs in the H-TCOL paddock for different periods,

from 2-10 weeks, measured on day of entry of the hospital paddock. The numbers in brackets above the bars indicate how many lambs were in each group.

When comparing the different periods in the hospital paddocks (2 weeks, 4 weeks, 6 weeks or more) no

significant differences (p<0.05) in mean FEC were found between neither the H-TCIR- (fig.16) nor the H-

TCOL groups (fig. 17).

Fig. 16. Arithmetic mean faecal egg count of lambs in the H-TCIR paddock for different periods, from 2-10 weeks, estimated over two weeks before they entered the paddock. The numbers

in brackets above the bars indicate how many lambs were in each group.

Fig. 17. Arithmetic mean faecal egg count of lambs in the H-TCOL paddock for different periods,

from 2-10 weeks, estimated over two weeks before they entered the paddock. The numbers in brackets above the bars indicate how many lambs were in each group.

-0,15-0,1

-0,050

0,050,1

0,150,2

2 4 6 8 10LW

G (

kg/d

ay)


Mean liveweight gain H-TCOL

(8) (2) (2)

0100020003000400050006000

2 4 6 8 10

FEC

(e

ggs/

gram

)


Mean faecal egg count H-TCIR

(19) (3) (1)

(1)

0100020003000400050006000

2 4 6 8 10

FEC

(e

ggs/

gram

)


Mean faecal egg count H-TCOL

(8) (3) (2) (2)

(8) (3)

(21)

(21)

(22)

30

II.4 Discussion The study was carried out in Lincoln, New Zealand with the objective to evaluate whether grazing organic

lambs on a hospital paddock that initially provided minimal contamination in addition to a mixture of

chicory, plantain and red clover could provide a means of mitigating the effects of infection in young lambs

with either Teladorsagia circumcincta or Trichostrongylus colubriformis. With this specific objective in

mind, it is worth noting that the provision of the bioactive herbage mix with chicory, plantain and red

clover was not successful in this instance. This was due to the very poor establishment and growth of these

forages in the hospital areas largely due to competition from weed species and ryegrass. A small amount of

ryegrass seed (4kg/ha) was included in the seed mix to minimise any impact of a rapid transition from

ryegrass to chicory or plantain on rumen microflora on animals that may be hospitalised (Greer 2012

personal communication). However, it appears that this level of ryegrass seed, in addition to the voluntary

contributions from dormant seeds within the soil profile, created too much competition for an effective

establishment of chicory or plantain in this instance. As such, the suitability of bioactive forages as a

hospital paddock cannot be determined from the current results. However, for the most part it is assumed

that the hospital areas did provide areas of low larval challenge given that they had not been grazed by

animals for 20 years or more before the trial started and hence was considered parasite free (although not

documented because of the missing pasture larval counts). Consequently, the suitability of removing larval

challenge as part of a hospital treatment to restore animal performance can still be evaluated.

Overall, placing parasitised animals into the hospital areas appeared to provide a benefit in terms of lamb

performance. For both TCIR and TCOL over 80% of animals that were identified as requiring treatment

returned to the original pasture within four weeks, while there were a number of time points when there

were interactions between paddock and time (tables 3 and 4), of note is that not once was that interaction

due to the hospitalised animals growing less than when they went into the hospital paddock. This suggests

that relieving challenge from an infected animal, even without drenching them first and removing the

worm burden is an effective way of at least preventing any further decline in performance. This is in

agreement with Githigia et al. (2001) who reported that moving lambs from an infective pasture to a clean

pasture will prevent parasitic gastroenteritis and improve their performance whether they were drenched

or not in connection with the move. Boa et al. (2001) also documented some positive effect on

performance when untreated lambs were moved to a pasture with lower parasite challenge and suggest

that moving animals to clean pasture without anthelmintic treatment may be an option for control in

organic systems.

Consequences of exposure to high larval challenge may be reduced appetite and reduced food utilisation

resulting in reduced performance (Steel et al. 1982; Symons et al. 1982; Thamsborg & Agergaard 2002).

31

Coop et al. (1982) pointed out the importance of removing the larval challenge to restore the appetite and

hence reduce the production losses. Symons et al. (1982), Steel et al. (1982) and Kyriazakis et al. (1996) also

showed results of increased appetite and performance when larval challenge was removed from

parasitised lambs. In accordance to these studies, although not measured it is presumed that the increased

LWG is due to a likely (partial) restoration of appetite when removed from the parasite challenge. Even if

appetite was restored through reduced challenge for the lambs in the hospital paddocks the additional

protein and energy supply would not be likely to result in an improved immune response in such a short

time span considering Bown et al. (1991) showed that at least 6 weeks of infusion with 50g/day casein is

required.

The mean daily LWGs of the lambs in the main paddocks were consistently higher than for the lambs in the

hospital paddocks. With the Happy factor including LWG in the calculations of the individual target

liveweights for the lambs it was not surprising that the lambs that did not reach their target weights and

were drafted into the hospital paddocks had lower LWGs than their counterparts. Herbage availability

could also be an influencing factor on LWG as number of lambs changed dramatically between different

paddocks throughout the study. The poorer pasture quantity of the hospital paddocks and the fact that

they were grazed by animals at all times whereas the main paddocks were rotationally grazed indicate that

the herbage availability was less in the hospital paddocks and this could possibly have caused lower LWGs.

The overall mean liveweight gain was slightly lower for the TCIR than TCOL which could be due to a higher

stocking rate and higher infection levels followed hereby and expressed in a higher FEC. Studies by

Thamsborg et al. (1996) and Brown et al. (1985) indicate a positive correlation between FEC and stocking

rate in sheep and other studies have reported that higher stocking rate and infection with nematodes

resulted in significant reductions in LWG of lambs (Thamsborg et al. 1996; Thamsborg et al. 1998). The

higher FEC in TCIR as well as a lower LWG could thus possibly be an effect of the higher stocking rate

although it’s worth mentioning that T.circumcincta is less pathogenic than T. colubriformis at equal rates of

infection and hence sheep can harbour a higher burden of this parasite (Steel et al. 1982; vanHoutert &

Sykes 1996).

It should be noted that a limitation with the trial was the lack of a positive control group given the organic

status. With the inability to drench animals for control the only possibility was to look for evidence that

suggested that grazing the lambs on the hospital paddocks helped alleviate some of the effects of infection,

such as reduced FEC and/or increased LWG. No literature could be found addressing this as a problem in

similar organic projects and with the effect on performance in hospitalised animals this suggests that there

was an effect from grazing animals in the hospital paddocks.

32

The incomplete pasture larval count is a shortcoming of the study. It would have been valuable for a

quantitative estimation of infective larvae on the different pastures to evaluate the infective status of the

pastures and to compare the different paddocks.

Hospitalisation did not appear to provide any antiparasitic benefits to the host. The FEC were similar

before and after for lambs in main and hospital paddocks for both the lambs infected with T.circumcincta

and lambs infected with T.colubriformis except on the first sampling where it increased after two weeks for

all groups. The lack of antiparasitic effect is not surprising given the poor growth of the bioactive plants.

The increase in mean FEC after the first grazing period was expected given that the lambs had been

drenched on the day of arrival and thereafter grazed on a contaminated pasture for three weeks which is

consistent with the pre-patent period of the nematodes.

Albers et al. (1987) define “resilient” as the ability to maintain a relatively undepressed production level

when infected and “resistant” as the ability of an animal to prevent establishment and/ or subsequent

development of a worm infection. The mean FEC was high for TCIR and H-TCIR and moderate for TCOL and

H-TCOL on most sampling times. It has been largely accepted that the performance of an animal with a

large parasite burden exhibiting a high FEC must have compromised performance. The lack of significant

difference in mean FEC between the main and hospital paddocks together with the higher LWGs in the

lambs in the main paddocks is in conflict with this and strongly indicates that those lambs were more

resilient than the hospitalised animals, i.e. they managed to maintain productivity and obtain the expected

LWG despite a high parasite burden. Studies in New Zealand by Morris et al. (1997) and Morris et al. (2005)

have shown that resilient animals can have a greater productivity than resistant animals despite the former

exhibiting higher FEC. Although with the mean FEC being consistently moderate or high throughout the trial

for all groups this does not reveal any signs of nematode resistance.

The major determinant for the length of time that animals required to stay in the hospital paddocks to

recover was unable to be determined from the measurements taken in this trial. Neither, liveweight, LWG

or FEC showed any consistent pattern as to how long an animal may take to recover.

Liveweight at entry of the hospital paddock could have been a candidate of determinant as McClure &

Emery (2007) showed that Merino lambs needed to have a liveweight of at least 23 kg at the time of first

parasite challenge to be capable of developing an immune response at a later challenge. It was

hypothesized in this study that lambs that were hospitalised and also had a low liveweight at entry would

take longer time to recover from parasitism than lambs entering the hospital paddocks with higher

liveweights. The only hint of this in this study is that the liveweights of those that needed 8 or 10 weeks to

recover (fig. 12 and 13) did tend to be a bit lower.

33

The small amount of animals in some of the groups created an imbalance between the groups and is

considered an inadequate number to detect a significant difference. This was taken into account when

running and interpreting the data and hence groups were merged (lambs hospitalised for 6-12 weeks were

looked at as one group) to give a more reliable result. By doing repeated observations the effectiveness of

the trial to detect differences between the groups increased and the study population is therefore

considered big enough for the purposes of this study.

LWG is suggested an alternative to FEC as an indicator for parasitism (Greer et al. 2009; Kenyon et al. 2009)

which the Happy factor model used in the current study is based on. It should be noted that with a

performance based TST system such as the Happy factor the method of identifying animals to receive

treatment is not able to separate the ill-thrift caused by factors other than the nematodes. It will therefore

identify animals suffering from ill-thrift rather than specifically detect losses in performance caused by

parasitism. However, parasitism is generally considered to be the most likely cause of ill-thrift in growing

lambs (Litherland et al. 2004) and previous research has shown that 85% of the animals that were deemed

to benefit from treatment also had an enhanced productivity and responded to treatment (Greer et al.

2009; Greer et al. 2010). The Happy factor model was not evaluated further in this trial, but the previous

studies suggest that this model is suitable for identifying animals suffering from parasitism. On the one

hand, it is surprising that LWG was not consistently more depressed in those that required longer time to

recover than those that took 2 weeks as this may be considered a fairly sensitive indicator of the parasite

status of animals with greater depression in LWG exhibiting a greater level of parasitism (Greer et al. 2009;

Greer et al. 2010).

FEC showed no consistent pattern, which may be surprising as it is generally considered that FEC= worm

burden (Roberts 1981), but there is plenty of evidence to show that this is not always the case (Douch et al.

1996). Flock FEC is often used by farmers and veterinarians as an indicator of parasitism and anthelmintic

treatment to minimise production losses. The results from this trial support the proposition that animals

that are considered to be in need of treatment do not necessarily have the highest FEC and considering that

T.circumcincta infections in lambs can cause a depression in performance which precedes the appearance

of FEC and clinical signs (van Houtert & Sykes 1996) the use of FEC as an indicator for parasitism can be

questioned. Taking in the poor correlations between LWG and FEC in this study, this furthermore support

the theory that FEC is not a particularly useful indicator and that it is more about how the animal is

responding that is important.

The results of the study indicate that there was no effect of the bioactive forages on worm burdens in any

of the groups. Several studies, both short-term and longer term grazing studies, have documented a clear

effect of chicory on abomasal worm burdens in lambs but not on intestinal worms (Marley et al. 2003;

34

Tzamaloukas et al. 2005; Kidane et al. 2010) and it was therefore expected to see an effect on at least the

lambs infected with T. circumcincta which was not the case. There was not seen an effect on any the

parasites. Based on these previous results and assuming that a true effect of chicory exists the result could

be attributed to the following explanations, individually or by combination:

1) Too low a proportion of chicory and plantain in the hospital paddocks and an intake of the forages below

a certain unknown threshold level to detect any antiparasitic effect

2) Too low a concentration of the bioactive components in the plants (however 1 and 2 was not measured)

3) Too short a grazing period in the hospital paddocks.

However, it is strongly believed that the lack of effect on FEC is related to the poor growth of the forages

and that the suitability of bioactive forages as a hospital paddock cannot be determined from the current

results.

The observed improvement in LWGs seen in lambs after periods in the hospital paddocks was similar for

the two groups and is considered to be a consequence of the reduced larval challenge and thus the

provision of a hospital paddock with a low level of larval contamination to provide animals with respite

from continued larval challenge does appear to present some benefits in terms of short-term responses in

liveweight gain.

35

II.5 Conclusion The suitability of bioactive forages as a hospital paddock cannot be determined from the current results

due to a poor establishment and growth of the forages. The study did not reveal any antiparasitic effect

following hospitalisation on neither intestinal nor abomasal parasites. The lack of effect on FEC may be

attributed to too short a grazing period, too low a proportion of the bioactive plants and/ or concentration

of their bioactive components, but is most likely due to the poor growth of the forages.

It appears that grazing the hospital paddocks provided a benefit to parasitised animals with an increase in

mean daily LWG on 50% of the occasions after time in the hospital paddock. The observed improvement in

LWG seen in lambs after periods in the hospital paddocks is considered to be a consequence of the reduced

larval challenge, rather than any direct benefit of bioactive forages.

Based on these findings the overall conclusion is that it was not possible in this study to judge the

effectiveness of the bioactive forages on liveweight gain or in reducing worm burdens. However, the

provision of a hospital paddock with a low larval contamination to provide animals with respite from

continued larval challenge does appear to confer some benefits in terms of short-term responses in LWG.

With anthelmintic resistance continuing to be a major problem in sheep farming in New Zealand and with

the requirement for reduced anthelmintic usage in the increasing organic production systems more future

research about alternative control methods, such as bioactive forages, is needed.

36

Section III: References

Aitken, I.D. & W.B. Martin (2000): Diseases of Sheep. Oxford : Blackwell Science, Oxford.

Albers, G.A.A., G.D, Gray., L.R, Piper., J.S.F, Barker., L.F, LeJambre & I.A, Barger (1987). The genetics of

resistance and resilience to Haemonchus contortus infection in young Merino sheep. International Journal

for Parasitology. Vol 17, pp. 1355-1363.

Athanasiadou, S., D. Gray, D. Younie, O. Tzamaloukas, F. Jackson & I. Kyriazakis (2007): The use of chicory

for parasite control in organic ewes and their lambs. Parasitology. Vol. 134, pp. 299-307.

Athanasiadou, S. & I. Kyriazakis (2004): Plant secondary metabolites: antiparasitic effects and their role in

ruminant production systems. Proceedings of the Nutrition Society. Vol. 63:4, pp. 631-639.

Athanasiadou, S., O. Tzamaloukas, I. Kyriazakis, F. Jackson & R. Coop (2005): Testing for direct anthelmintic

effects of bioactive forages against Trichostrongylus colubriformis in grazing sheep. Veterinary Parasitology.

Vol. 127:3-4, pp. 233-243.

Barger, I. (1997): Control by management. Veterinary Parasitology. Vol. 72:3-4, pp. 493-500.

Barger, I.A. (1999): The role of epidemiological knowledge and grazing management for helminth control in

small ruminants. International Journal for Parasitology. Vol. 29:1, pp. 41-47.

Barnes, E., R. Dobson & I. Barger (1995): Worm Control and Anthelmintic Resistance - Adventures with a

Model. Parasitology Today. Vol. 11:2, pp. 56-63.

Barry, T. & W. McNabb (1999): The implications of condensed tannins on the nutritive value of temperate

forages fed to ruminants. British Journal of Nutrition. Vol. 81:4, pp. 263-272.

Besier, R.B. (2008): Targeted treatment strategies for sustainable worm control in small ruminants. Tropical

Biomedicine. Vol. 25:1, pp. 9-17.

Boa, M.E., S.M. Thamsborg., A.A, Kassuku, & H.O, Bøgh (2001): Comparison of Worm Control Strategies in Grazing Sheep in Denmark. Acta Veterinaria Scandinavica. Vol. 42, pp. 57-69.

Bowman, D.D. & J.R. Georgi (2009): Georgis' Parasitology for Veterinarians. St. Louis, Mo. : Saunders

Elsevier, St. Louis, Mo.

Bown, M.D.B., D.P, Poppi & Sykes, A.R (991): The Effect of Post-ruminal Infusion of Protein or Energy on the

Pathophysiology of Trichostrongylus colubriformis Infection and Body Composition in Lambs. Australian

Journal of Agricultural Research. Vol. 42, pp. 253-267.

Bruère, A.N., D.M. West & New Zealand Veterinary Association, Foundation for,Continuing Education

(1993): The Sheep, Health, Disease & Production, Written for Veterinarians and Farmers. Palmerston North :

Veterinary Continuing Education, Massey University, Palmerston North.

37

Brunet, S., F. Jackson & H. Hoste (2008): Effects of sainfoin (Onobrychis viciifolia) extract and monomers of

condensed tannins on the association of abomasal nematode larvae with fundic explants. International

Journal for Parasitology. Vol. 38:7, pp. 783-790.

Brunsdon, R.V. (1980): Principles of helminth control. Veterinary Parasitology. Vol. 6, pp. 185-215.

Brunsdon, R.V. (1976): Integrated control of internal parasites. New Zealand Journal of Agriculture. Vol.

133:2, pp. 9.

Brunsdon, R.V. (1970): Seasonal Changes in Level and Composition of Nematode Worm Burdens in Young

Sheep. New Zealand Journal of Agricultural Research. Vol. 13:1, pp. 126.

Charleston, W. & P. McKenna (2002): Nematodes and liver fluke in New Zealand. New Zealand Veterinary

Journal. Vol. 50:3, pp. 41-47.

Coop, R.L., A.R. Sykes & K.W. Angus (1982): The effect of three levels intake of Ostertagia circumcincta

larvae on growth rate, food intake and body composition of growing lambs. Journal of Agricultural Science.

Vol. 98, pp. 247-255.

Coop, R. & I. Kyriazakis (2001): Influence of host nutrition on the development and consequences of

nematode parasitism in ruminants. Trends in Parasitology. Vol. 17:7, pp. 325-330.

Dobson, R.J. & B (1992). Population dynamics of Trichostrongylus colubriformis and Ostertagia circumcincta

in single and concurrent infections. International Journal for Parasitolog,. Vol. 22; Vol.22:7; 7, pp. 997-1004.

Douch, P., R. Green, C. Morris, J. McEwan & R. Windon (1996): Phenotypic markers for selection of

nematode-resistant sheep. International Journal for Parasitology. Vol. 26:8-9, pp. 899-911.

Familton, A.S. & R.W. McAnulty (1997): Life cycles and development of nematode parasites of ruminants:

Sustainable control of internal parasites in ruminants: Animal industries workshop.

Gilruth, J.A. & New Zealand. Department of Agriculture. (1895): Anthrax. Govt. Printer, Wellington [N.Z.].

Greer,A. (2012): Lincoln University, New Zealand.

Greer, A.W., F. Kenyon, D.J. Bartley, E.B. Jackson, Y. Gordon, A.A. Donnan, D.W. McBean & F. Jackson

(2009): Development and field evaluation of a decision support model for anthelmintic treatments as part

of a targeted selective treatment (TST) regime in lambs. Veterinary Parasitology. Vol. 164:1, pp. 12-20.

Greer, A.W., R.W. McAnulty, C.M. Logan & S.O. Hoskin (2010): Suitability of the Happy Factor decision

support model as part of targeted selective anthelmintic treatment in Coopworth sheep. Proceedings of the

New Zealand Society of Animal Production. Vol. 70, pp. 213-216.

Heckendorn, F., D.A. Häring, V. Maurer, M. Senn & H. Herzberg (2007): Individual administration of three

tanniferous forage plants to lambs artificially infected with Haemonchus contortus and Cooperia curticei.

Veterinary Parasitology. Vol. 146, pp. 123-134.

38

Hervé, M., R. McAnulty, C. Logan & A.R. Sykes (2003): Regional variations in the nematode worm

populations of breeding ewes in New Zealand. New Zealand Veterinary Journal. Vol. 51:4, pp. 159-164.

Hoste, H. & J.F.J. Torres-Acosta (2011): Non chemical control of helminths in ruminants: Adapting solutions

for changing worms in a changing world. Veterinary Parasitology. Vol. 180:1-2, pp. 144-154.

Hoste, H., F. Jackson, S. Athanasiadou, S.M. Thamsborg & S.O. Hoskin (2006): The effects of tannin-rich

plants on parasitic nematodes in ruminants. Trends in Parasitology. Vol. 22:6, pp. 253-261.

Jackson, F., D. Bartley, Y. Bartley & F. Kenyon (2009): Worm control in sheep in the future. Small Ruminant

Research. Vol. 86:1-3, pp. 40-45.

Jackson, F. & R. Coop (2000): The development of anthelmintic resistance in sheep nematodes.

Parasitology. Vol. 120, pp. S95-S107.

Jackson, F. & P. Waller (2008): Managing refugia. Tropical Biomedicine. Vol. 25:1, pp. 34-40.

Jackson, F. & J. Miller (2006): Alternative approaches to control - Quo vadit? Veterinary Parasitology. Vol.

139:4, pp. 371-384.

Kahn, L.P. & R.G. Woodgate (2012): Integrated parasite management: Products for adoption by the

Australian sheep industry. Veterinary Parasitology. Vol. 186:1-2, pp. 58-64.

Kaplan, R. (2004): Drug resistance in nematodes of veterinary importance: a status report. Trends in

Parasitology. Vol. 20:10, pp. 477-481.

Kassai, T. (1999): Veterinary Helminthology. Oxford : Butterworth-Heinemann, Oxford.

Kenyon, F., A.W. Greer, G.C. Coles, G. Cringoli, E. Papadopoulos, J. Cabaret, B. Berrag, M. Varady, J.A. Van

Wyk, E. Thomas, J. Vercruysse & F. Jackson (2009): The role of targeted selective treatments in the

development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants.

Veterinary Parasitology. Vol. 164:1, pp. 3-11.

Kidane, A., J.G.M. Houdijk, S. Athanasiadou, B.J. Tolkamp & I. Kyriazakis (2010): Effects of maternal protein

nutrition and subsequent grazing on chicory (Cichorium intybus) on parasitism and performance of lambs.

Journal of Animal Science. Vol. 88:4, pp. 1513-1521.

Koski, K.G. & M.E. Scott (2003): Gastrointestinal nematodes, trace elements, and immunity. Journal of Trace

Elements in Experimental Medicine. Vol. 16:4, pp. 237-251.

Kyriazakis, I., D. Anderson, J. Oldham, R. Coop & F. Jackson (1996): Long-term subclinical infection with

Trichostrongylus colubriformis: Effects on food intake, diet selection and performance of growing lambs.

Veterinary Parasitology. Vol. 61:3-4, pp. 297-313.

Leathwick, D., W. Pomroy & A. Heath (2001): Anthelmintic resistance in New Zealand. New Zealand

Veterinary Journal. Vol. 49:6, pp. 227-235.

39

Lira, C.M.D., T.N. Barry, W.E. Porlaroy, E.L. McWilliam & N. Lopez-Villalobos (2008): Willow (Salix spp.)

fodder blocks for growth and sustainable management of internal parasites in grazing lambs. Animal Feed

Science and Technology. Vol. 141:1-2, pp. 61-81.

Litherland A. J., Layton D. L. & Boom C. J. (2004): Ill-thrift in young growing cattle and sheep. Proceedings of

the New Zealand Society of Animal Production. Vol. 64 pp. 197-202.

Mackay, A.D., K. Betteridge, B.P. Devantier, P.J. Budding & J. Niezen (1999): Chemical-free hill country

sheep and beef livestock production systems. Proceedings of the New Zealand Grassland Association.Vol

60: pp.15-18.

Mackay, A.D., T. Harrison, R.A. Moss, T.J. Fraser, A.P. Rhodes, D. Cadwallader, M.W. Fisher & R. Webby

(2001): Moving towards low-chemical and caring farming systems. Proceedings of the New Zealand

Grassland Association. Vol. 63, pp. 279-282.

Malan, F.S., J.A. Van Wyk & C.D. Wessels (2001): Clinical evaluation of anaemia in sleep: early trials.

Onderstepoort Journal of Veterinary Research. Vol. 68:3, pp. 165-174.

Marley, C., R. Cook, R. Keatinge, J. Barrett & N. Lampkin (2003): The effect of birdsfoot trefoil (Lotus

corniculatus) and chicory (Cichorium intybus) on parasite intensities and performance of lambs naturally

infected with helminth parasites. Veterinary Parasitology. Vol. 112:1-2, pp. 147-155.

Martin, P. (1987): Development and Control of Resistance to Anthelmintics. International Journal for

Parasitology. Vol. 17:2, pp. 493-501.

Martinez-Ortiz-de-Montellano, C., J.J. Vargas-Magana, H.L. Canul-Ku, R. Miranda-Soberanis, C. Capetillo-

Leal, C.A. Sandoval-Castro, H. Hoste & J.F.J. Torres-Acosta (2010): Effect of a tropical tannin-rich plant

Lysiloma latisiliquum on adult populations of Haemonchus contortus in sheep. Veterinary Parasitology. Vol.

172:3-4, pp. 283-290.

Mc Anulty, R.W., V.R. Clark & A.R. Sykes (1982): The effect of clean pasture and anthelmintic frequency on

growth rates of lambs on irrigated pasture: Proceeding of the NZ Society of Animal Production. pp. 187-188.

McKenna, P. (1981): The diagnostic value and interpretation of faecal egg counts in sheep. New Zealand

Veterinary Journal. Vol. 29 pp. 129-13,.

Miller, M.C., S.K. Duckett & J.G. Andrae (2011): The effect of forage species on performance and

gastrointestinal nematode infection in lambs. Small Ruminant Research. Vol. 95:2-3, pp. 188-192.

Molan, A., A. Duncan, T. Barry & W. McNabb (2003): Effects of condensed tannins and crude sesquiterpene

lactones extracted from chicory on the motility of larvae of deer lungworm and gastrointestinal nematodes.

Parasitology International. Vol. 52:3, pp. 209-218.

Molento, M., J. van Wyk & G. Coles (2004): Sustainable worm management. Veterinary Record. Vol. 155:3,

pp. 95-96.

40

Morris, C.A. & A.D. Mackay (2002): Moving towards low-chemical farming with sheep and cattle: the

potential of a breeding approach. Proceedings of the New Zealand Society of Animal Production. Vol. 62 pp.

81-85.

Morris, C.A., M. Wheeler, T.G. Watson, B.C. Hosking & D.M. Leathwick (2005): Direct and correlated

responses to selection for high or low faecal nematode egg count in Perendale sheep. New Zealand Journal

of Agricultural Research. Vol. 48:1, pp. 1-10.

Morris, C.A., S.A. Bisset, A. Vlassoff, R.L. Baker, T.G. Watson, D.M. Lethwick & M. Wheeler (1997):

Correlated responses in fleece weight to selection for high or low faecal egg count in New Zealand Romneys

and Perendales. New Zealand Journal of Agricultural research. Vol. 57, pp. 26-28.

Mupeyo, B., T.N. Barry, W.E. Pomroy, C.A. Ramirez-Restrepo, N. Lopez-Villalobos & A. Pernthaner (2011):

Effects of feeding willow (Salix spp.) upon death of established parasites and parasite fecundity. Animal

Feed Science and Technology. Vol. 164:1-2, pp. 8-20.

Nietzen, J.H., T.S. Waghorn, G.C. Waghorn & W.A.G. Charlston (1993): Internal parasites and lamb

production - a role for plants containing condensed tannins? Proceedings of the New Zealand Society of

Animal Production, pp. 235-238.

NIWA Taihuru Nukurangi (2012): NIWA Taihuru Nukurangi, 14-06-2012, NIWA Taihuru Nukurangi, New

Zealand [cited 14-06-2012]. Available at the Internet.

<http://www.niwa.co.nz/sites/default/files/climate_summary_summer_2011_2012_final.pdf>.

Pomroy, W.E. (2006): Anthelmintic resistance in New Zealand: a perspective on recent findings and options

for the future. New Zealand Veterinary Journal. Vol. 54:6, pp. 265-270.

Prichard, R. (1990): Anthelmintic Resistance in Nematodes - Extent, Recent Understanding and Future-

Directions for Control and Research. International Journal for Parasitology. Vol. 20:4, pp. 515-523.

Prichard, R., C. Hall, J. Kelly, I. Martin & A. Donald (1980): The Problem of Anthelmintic Resistance in

Nematodes. Australian Veterinary Journal. Vol. 56:5, pp. 239-251.

Roberts, J.L. & S (1981): Quantitative studies of ovine haemonchosis. I. Relationship between faecal egg

counts and total worm counts. Veterinary Parasitologi.Vol.8:2, pp. 165-171.

Rochfort, S., A.J. Parker & F.R. Dunshea (2008): Plant bioactives for ruminant health and productivity.

Phytochemistry. Vol. 69:2, pp. 299-322.

Scales, G., T. Knight & D. Saville (1995): Effect of Herbage Species and Feeding Level on Internal Parasites

and Production Performance of Grazing Lambs. New Zealand Journal of Agricultural Research. Vol. 38:2, pp.

237-247.

Stafford, K.A., E.R. Morgan & G.C. Coles (2009): Weight-based targeted selective treatment of

gastrointestinal nematodes in a commercial sheep flock. Veterinary Parasitology. Vol. 164:1, pp. 59-65.

41

Stear, M.J., M. Doligalska & K. Donskow-Schmelter (2007): Alternatives to anthelmintics for the control of

nematodes in livestock. Parasitology. Vol. 134, pp. 139-151.

Steel, J.W., W.0. Jones & L.E.A. Symons (1982): Effects of a Concurrent Infection of Trichostrongylus

colubriformis on the Productivity and Physiological and Metabolic Responses of Lambs Infected with

Ostertagia cirumcincta. Australian Journal of Agricultural Research. Vol. 33 pp. 131-140.

Sutherland, I. & I. Scott (2010): Gastrointestinal Nematodes of Sheep and Cattle, Biology and Control.

Chichester : Wiley-Blackwell, Chichester.

Sykes, A.R. (1987): Endoparasites and herbivore nutrition. The Nutrition of Herbivores. pp. 211-232.

Sykes, A.R. & R.L. Coop (2001): Interaction between nutrition and gastrointestinal parasitism in sheep. New

Zealand Veterinary Journal. Vol. 49:6, pp. 222-226.

Sykes, A. (1994): Parasitism and Production in Farm-Animals. Animal Production. Vol. 59, pp. 155-172.

Symons, L.E.A., J.W. Steel & W.0. Jones (1982): Effects of Level of Larval Intake on the Productivity and

Physiological and Metabolic Responses of Lambs Infected with Ostertaqia circumcincta. Australian Journal

of Agricultural Research. Vol. 32, pp. 139-148.

Taylor, M. (1999): Use of anthelmintics in sheep. In Practice. Vol. 21:5, pp. 222-.

Thamsborg, S.M. & N. Agergaard (2002): Anorexia and food utilization in nematode infected lambs on

pasture. Animal Science Journal. Vol. 75, pp. 303-313.

Thamsborg, S.M., R.J. Jørgensen, H. Ranvig, P. Bartlett, P.J. Waller & P. Nansen (1998): The performance of

grazing sheep in relation to stocking rate and exposure to nematode infections. Livestock Production

Science. Vol. 53, pp. 265-277.

Thamsborg, S.M., R.J. Jørgensen, P.J. Waller & P. Nansen (1996): The influence of stocking rate on

gastrointestinal nematode infections of sheep over a 2-year grazing period. Veterinary Parasitology. Vol.

67, pp. 207-224.

Thamsborg, S., A. Roepstorff & M. Larsen (1999): Integrated and biological control of parasites in organic

and conventional production systems. Veterinary Parasitology. Vol. 84:3-4, pp. 169-186.

Thompson, K.F., W.H. Risk, P. Mason & S. Crosbie (1982): The effects of drenching regimen and pasture

larval contamination on gastrointestinal parasitism of lambs: Proceedings of the N.Z Society of Animal

Production. pp. 189-191.

Tzamaloukas, O., S. Athanasiadou, I. Kyriazakis, F. Jackson & R. Coop (2005): The consequences of short-

term grazing of bioactive forages on established adult and incoming larvae populations of Teladorsagia

circumcincta in lambs. International Journal for Parasitology. Vol. 35:3, pp. 329-335.

Urquhart, G.M. (1987): Veterinary Parasitology. Essex : Longman, Essex.

42

van Wyk, J.A., H. Hoste, R.M. Kaplan & R.B. Besier (2006): Targeted selective treatment for worm

management - How do we sell rational programs to farmers? Veterinary Parasitology. Vol. 139:4, pp. 336-

346.

van Houtert, M.F.J. & A.R. Sykes (1996): Implications of nutrition for the ability of ruminants to withstand

gastrointestinal nematode infections. International Journal for Parasitology. Vol. 26:11, pp. 1151-1167.

Vlassoff, A. (1979): Integrated control of gastro-intestinal nematodes of sheep: Proceedings of the 2nd

Australasian conference on grassland invertebrate ecology. pp. 188-191.

Vlassoff, A., D.M. Leathwick & A.C.G. Heath (2001): The epidemiology of nematode infections of sheep.

New Zealand Veterinary Journal. Vol. 49:6, pp. 213-221.

Vlassoff, A. & P. McKenna (1994): Nematode Parasites of Economic Importance in Sheep in New Zealand.

New Zealand Journal of Zoology. Vol. 21:1, pp. 1-8.

Waghorn, T.S., D.M. Leathwick, A.P. Rhodes, K.E. Lawrence, R. Jackson, W.E. Pomroy, D.M. West & J.R.

Moffat (2006): Prevalence of anthelmintic resistance on sheep farms in New Zealand. New Zealand

Veterinary Journal. Vol. 54:6, pp. 271-277.

Waller, P. (2006): Sustainable nematode parasite control strategies for ruminant livestock by grazing

management and biological control. Animal Feed Science and Technology. Vol. 126:3-4, pp. 277-289.

Waller, P. (1999): International approaches to the concept of integrated control of nematode parasites of

livestock. International Journal for Parasitology. Vol. 29:1, pp. 155-164.

Waller, P. (1997): Anthelmintic resistance. Veterinary Parasitology. Vol. 72:3-4, pp. 391-405.

Wolstenholme, A., I. Fairweather, R. Prichard, G. von Samson-Himmelstjerna & N. Sangster (2004): Drug

resistance in veterinary helminths. Trends in Parasitology. Vol. 20:10, pp. 469-476.

Woodgate, R.G. & R.B. Besier (2010): Sustainable use of anthelmintics in an Integrated Parasite

Management Program for sheep nematodes. Animal Production Science. Vol. 50:5-6, pp. 440-443.

Wyk, J.A. (2001): Refugia - overlooked as perhaps the most potent factor concerning the development of

anthelmintic resistance. Onderstepoort Journal of Veterinary Research. Vol. 68:1, pp. 55-67.

43

Appendix I

The different bioactive forages that were sown in the hospital paddocks in the trial.

Fig A 1. Chicory (Cichorium intubus cv. Grasslands Puna.

Fig A 2. Plantain (Plantago lanceolata cv. Grasslands Lancelot).

Fig A 3. Red clover (Trifolium pratense cv. Minshan).

44

Appendix II

Larvae and eggs from the gastrointestinal nematodes that the lambs in the trial were infected with.

Fig A 4. Infective L3 larva of Trichostrongylus colubriformis.

Fig A 5. Infective L3 larva of Teladorsagia circumcincta.

Fig A 6. A ruminant strongyle egg.

45

Appendix III

The experimental area at the Biological Husbandry Unit of Lincoln University, New Zealand.

Fig A 7. The trial site with the drafting system setup. The TCOL paddock is seen in the background.

In the pictures: the author, Robin Mc Anulty and Andrew Greer.

46

Fig A 8. The drafting system and Tru-test setup with scales and the yellow Tru-test head unit. Andrew Greer and the author in the pictures.

47

Appendix IV

Estimation of pasture mass and calibration of the rising plate meter in the main paddocks before the trial

start.

Fig A9. Calibration of plate meter for estimation of pasture mass (kg DM per ha)

in the TCOL- and TCIR paddocks, based on 8 measurements per paddock.

y = 150x + 2E-12

0

500

1000

1500

2000

2500

3000

3500

4000

4500

5000

0 5 10 15 20

DM

(kg

/ha)

counts/ click

Actual values

Estimated values

48

Appendix V

Individual mean FEC for all lambs in TCIR/H-TCIR over the entire study period, with individual lamb IDs displayed on top of each graph. Red arrows indicate the time each lamb stayed in the hospital paddock.

010002000300040005000

1 2 3 4 5 6 7

FEC

(e

pg)

Sampling time

235

0

5000

10000

15000

1 2 3 4 5 6 7

236

010002000300040005000

1 2 3 4 5 6 7

237

010002000300040005000

1 2 3 4 5 6 7

238

010002000300040005000

1 2 3 4 5 6 7

241

010002000300040005000

1 2 3 4 5 6 7

243

0

2000

4000

6000

8000

10000

1 2 3 4 5 6 7

246

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

247

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

248

010002000300040005000

1 2 3 4 5 6 7

252

010002000300040005000

1 2 3 4 5 6 7

253

010002000300040005000

1 2 3 4 5 6 7

254

0

5000

10000

15000

1 2 3 4 5 6 7

258

010002000300040005000

1 2 3 4 5 6 7

265

010002000300040005000

1 2 3 4 5 6 7

266

49

0

2000

4000

6000

8000

10000

1 2 3 4 5 6 7

FEC

(e

pg)

Sampling time

268

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

269

0

2000

4000

6000

8000

10000

1 2 3 4 5 6 7

272

02000400060008000

10000

1 2 3 4 5 6 7

274

0

5000

10000

15000

1 2 3 4 5 6 7

277

02000400060008000

10000

1 2 3 4 5 6 7

278

010002000300040005000

1 2 3 4 5 6 7

279

02000400060008000

10000

1 2 3 4 5 6 7

280

010002000300040005000

1 2 3 4 5 6 7

282

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

285

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

286

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

291

0

5000

10000

15000

20000

1 2 3 4 5 6 7

292

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

293

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

300

50

Individual mean FEC for all lambs in TCOL/H-TCOL over the entire study period, with individual lamb IDs displayed on top of each graph. Red arrows indicate the time each lamb stayed in the hospital paddock.

010002000300040005000

1 2 3 4 5 6 7

232

010002000300040005000

1 2 3 4 5 6 7

233

02000400060008000

10000

1 2 3 4 5 6 7

239

010002000300040005000

1 2 3 4 5 6 7

240

010002000300040005000

1 2 3 4 5 6 7

242

010002000300040005000

1 2 3 4 5 6 7

244

010002000300040005000

1 2 3 4 5 6 7

245

010002000300040005000

1 2 3 4 5 6 7

249

010002000300040005000

1 2 3 4 5 6 7

250

010002000300040005000

1 2 3 4 5 6 7

251

010002000300040005000

1 2 3 4 5 6 7

255

010002000300040005000

1 2 3 4 5 6 7

256

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

257

010002000300040005000

1 2 3 4 5 6 7

259

010002000300040005000

1 2 3 4 5 6 7

260

51

010002000300040005000

1 2 3 4 5 6 7

FEC

(e

pg)

Sampling time

261

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

262

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

263

010002000300040005000

1 2 3 4 5 6 7

264

010002000300040005000

1 2 3 4 5 6 7

267

010002000300040005000

1 2 3 4 5 6 7

270

010002000300040005000

1 2 3 4 5 6 7

271

010002000300040005000

1 2 3 4 5 6 7

273

010002000300040005000

1 2 3 4 5 6 7

275

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

276

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

283

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

284

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

287

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

288

0

1000

2000

3000

4000

5000

1 2 3 4 5 6 7

290

Master thesis in Veterinary Medicine

Documents