VETERINARY
PARASITOLOGY
SECOND EDITION G M URQUHART
JARMOUR
J L DUNCAN
A M DUNN
F W JENNINGS
,Veterinary
Parasitology
Second Edition
G. M. Urquhart
J. Armour
J. L. Duncan
A. M. Dunn
F. W. Jennings
The Faculty of Veterinary Medicine
The University of Glasgow Scotland
Blackwell
Science
,CONTENTS
Foreword to thefirst edition vii Suhorder CYCLORRHAPHA
Acknowledgements to the first edition ix Family MUSCIDAE
Foreword and acknowledgements lo the seco,zd xi Family CALLIPHORIDAE
edition Family SARCOPIIAGIDAE
Family OESTRIDAE
VETERINARY HELMINTHOLOGY Family HIPPOBOSCIDAE
Order PHlHlRAmERA
Phylum NEMATHELMINTNES 3 Suhorder ANOPLURA
Class NEMATODA 4 Suborder MALLOPHAGA
Superfamily TRICHOSTRON(iYLO1DEA 10 Order SIPHONAPTERA
Superfamily STRONCYLOIDEA 42 Class ARACHNIDA
Superfamily MBI'ASI'KONGYLOIDEA 57 Order ACARINA
Superfamily RHABUSIOIDEA 65 Family IXODIDAE
Superfamily ASCARIDOIDEA 67 Family AKGASIDAE
Superfamily OXYUROIDEA 77 Family SARCOPTIDAE
Superfamily SPIRUROIDEA 79 Family DEMODICIDAE.
Superfamily FlI.ARIOIDEA 85 Family 1.AMINOSIOPSIDAE
Superfamily TRICHUKOIDEA 95 Family PSOKOYIIUAE
Superfamily DIOCTOPHYMATOIDEA 99 Family CHEYLETIDAE
Phylum ACANTHOCEPHALA
100 Family DERMANYSSIDAE
Phylum PLATYHELMINTHES
1 02 Class PENTASTOMIDA
Class TREMATODA
102
Subclass DlGRNRA
102 VETERINARY PROTOZOOLOGY
Family FASCIOLIUAC:
103
Family DICROCOELIIDAE
113 Phylum PROTOZOA
Family PARAMPHISTOMATIDAE
115 Subphylum SARCOMASI'ICOPHORA
Family TROGLOTREMAIIDAE
116 Class SARCODINA
Family OPISTHORCHIIDAR 117 Class MASTIGOPHORA
Family SCHISTOSOMATIDAE 117 Subphylum SPOROZOA
Family DIPLOSTOMAIDAE 120 Class COCCIDIA
Class CESTODA 120 Family RIMERIIDAE
Order CYCLOPHYLLIDEA 120 Pamily SAKCOCYSnUAE
Family TAENIIDAE 122 Class P~KOPLASMIDIA
Family ANOPLOCEPHAIIDAC 130 Class HAEMOSPORIDIA
Family DILEPIDIDAE 133 Subphylum CILIOPHORA
Family DAVAlNElDAE 135 Subphylum MICROSPORA
Family HYMENOLEPIUIDAE
136 Order RICKETISIALES
Family MESOCESTOIDIDAE
136
Family THYSANOSOMIDAE
136 REVIEW TOPICS
Order PSEUDOPIIY1.LIDEA
137
The epidemiology ofparasitic
VETERINARY ENTOMOLOGY diseases Resistance to parasitic
disea,es Anthelmintics
Phylum ARTHROPOUA Ectoparasiticides (insecticides/acaricides)
Class INSECI'A 14' The luboratory diagnosi.~ofparasitism 142
Order DlflERA
143
Suborder NEMATOCERA
145 HOST/PARASITE LISTS
Family CERATOPOGONIDAE
145
Family SIMULIIDAE 146 Sources of further information
Family PSYCHODIUAE
147
Family CULlClUAE
Suborder BRACHYCERA 148 Index
Family TABANIDAE 151
,VETERINARY HELMINTHOLOGY
,PRINCIPLES OF CLASSIFICATION Thc names oI taxa must be adhered to according to
the international rules, but it is permissible to anglicize
All animal organisms are relatcd to one another, the endings, so that members of the supcrfamily
closely or remotely, and the study of the complex sys- Trichostrongyloidea in thc example above may also be
tems of inter-relationship is called systematics. It is termed trichostronevloids.
L.,
essentially a study of the evolutionary process. The names of the genus and species are expressed in
When organisms are examined it is seen that they
form natural groups with features, usually morpho-
-
Latin form. the eeneric name havine a cauital letter,
and they must be in grammatical agreement. It is cus-
logical, in common. A group of this sort is called a tomary to print foreign words in italics, so that the
taxon, and the study of this aspecl of biology is called name of an organism is usually underlined or itali-
taxonomy. cized. Accents are not permitted, so that, if an organ-
The taxa in which organisms may be placed are ism is named aftcr a person, amendment may he
recognized by international agreement, and the chief neccssary; the name of Miiller, for example, has been
oncs are: kingdom, phylum, class, order, family, genus altered in the genus Muellerius.
and species. The intervals between these arc large, and The higher taxa containing helminths of veterinary
some organisms cannot be allocated to them precisely, importance are:
so that intermediate taxa, prefixed appropriately, have
been formed; examples of these are the suborder and Major
the snperfamily. As an instance, the taxonomic status Nemathelminthes (roundworms)
of one of the common abomasal parasites of ruminants Platyhelminthes (flatworms)
may he expressed as shown below.
Minor
Acanthocephala (thornyhcaded worms)
Kingdom Animalia
Phylum Nemathelminthes
Class Nematoda
Order Strongylida
Suborder Strongylina
Though the phylum Nemathelminthes has six
Superfamily Trichostrongyloidea classes only one of these, the nematoda, contains
Family Trichostrongylidae worms of parasitic significance. The nematodes are
Subfamily Haemonchinae commonly called roundworms, from their
Genus Iluvmonchus appearance in cross-section.
Species conlorlus
, 4 Veterinary Parasitology
Table 1 Paras I cNematooa of velerlnary mponance
PA
sfmD Ieo c asslflcar on
A system of classification of nematodes of veterinary
importance is given i n Table 1. Superfamily Typical features
I t must bc emphasized that this is not an exact ex-
pression of the general system for parasitic nema- Bursate nematodes
todes, hut is a simplified presentation intended for use
in the study of veterinary parasitology. I t is bascd on Trichostrongyloldea Buccal capsule small.
the ten superfamilies in which nematodes of vetcri- Trichostrongyius, Life cycle direct; infection
nary importance occur, and which are conveniently Osteftagia, Dicfyocaulus, by L,.
divided into bursate and non-bursate groups as shown Haemonchus, etc.
i n Table 1. Strongyloidea Buccal capsule well
Strongylus, Ancylostoma, developed; leaf crowns
STRUCTURE AND FUNCTION Syngamus, etc. and teeth usually present.
Most nematodes have a cylindrical form. taoerine at Life cycie direct; infection
hv I
"7 T
either end, and the body is covered by a colour~ss,
somewhat translucent, layer, the cuticle. Metastrongyloidea Buccal capsule small.
The cuticle is secrctcd by the underlying Mefastrongyius, Life cycle indirect;
hypodermis, which projects into the body cavity form- MUellerius, infection by L, in
ing two lateral cords, which carry the excretory canals, PrOfDStrongylus, intermediate host.
and a dorsal and ventral cord carrying the nerves (Fig.
1). The muscle cells, arranged longitudinally, lie be-
tween the hypodemis and the body cavity. The latter RhabditOidea Very small worms; buccal
contains fluid at a high pressure which maintains the
turgidity and shape of the body. Locomotion is ef- StrD"9Y10ides, Rhabdifis, capsule small. Free-living
fected by undulating waves of muscle contraction and and parasitic generations.
relaxation which alternate on the dorsal and ventral Life cycle direct; infection
aspects of the worm. by L.
Most of the internal organs are filamentous and ~ ~ ~ ~ ~ i d Large~ white dworms~. ~
suspended i n the fluid-filled body cavity (Fig. 2). Ascaris. Toxocara, Life cycle direct; infection
The digestive system is tubular. The mouth of many pamcarisris,etc. by L, in egg.
nematodes is a simple opening which may be sur- OxYuroidea Female has long, pointed
rounded by two or three lips, and leads directly into
the oesophagus. In others, such as the strongyloids, i t OxYUris, Skqabinema,etc. tail.
is large, and opens into a buccal capsule, which may Life cycle direct; infection
contain teeth; such parasites, when feeding, draw a by L, in egg.
plug of mucosa into the buccal capsule (Fig. 3), where spiruroidea Spiral tail in male.
Spirocerca, Habronema, Life cycle indirect;
Thelazia, etc. infection by L, from
insect.
Filarioidea Long thin worms.
Dorsal nerve Dirofilaria, Onchomrca, Life cycle indirect;
Cuticle Parafilaria, etc. infection by L, from
Ovaw insect.
Intestine Trlchuroidea Whip-like or hair-like
Excretow THchuHs, Capillaria, worms.
Uterus Trichineiia, etc. Life cycle direct or
Muscle indirect; infection by L,.
H v P~ Dioctophymatoidea~~~~ ~~ Very large worms.
ventralnerve Dioctophyma, etc. Life cycle indirect;
infection by L, in aquatic
annelids.
Flg. 1 Transverse section of i. typical nematode
, Veterinary Helminthology 5
Nerve ring Oesophagus Intestine Rectum The oesophagus is usually muscular and pumps food
1 I into the intestine. It is of variable form (Fig. 4). and is
a useful preliminary identification character for groups
of worms. It may be filariform, simple and slightly
thickened poslcriorly, as in the hursate nema-todcs;
bulb-shaped, with a large posterior swelling, as
in the ascaridoids: or douhlehulb-shaned.. as in-the
,
oxyuroids. In some groups this wholly muscular fonn
does not occur: the filarioids and spiruroids have a
muscular-glandular ocsophdgus which is muscular
(bl anteriorly, thc posterior part being glandular: the
ray trichuroid oesophagus has a capillary form, passing
through a single column of cells, the wholc bcing
known as a stichosome. A rhabditifnrm oesophagus,
with slight anterior and postcriur swellings, is present
in the preparasitic larvae of many nematodes, and in
adult free-living nematodes.
Fig. 2 Longitudinal sections of a nematode illustrating: (a) ~ h intestine, is a tube ,,,hose lumen is enclosed by
Diges-tive, excretory and nervous system: (b) a singlc layer o l cells or by a syncytinm. Their lumiual
Reproductive system of female and male nematodes.
surfaces nossess microvilli which increase thc absorn-
tive capacity of the cells. In female worms the
intestine terminates in an anus whilc in males there is a
cloaca which functions as an anus, and into which 8
opens the vas deferens and lhrough which the
copulatory spiculcs may be extruded.
Fig. 3 Large buccal capsule of strongyloid nematode
ingesting plug 01 mucosa.
Rhabditiform Filariform Bulb
it is broken down by the action of enzymes which are
secrctcd into the capsule from adjacent glands. Somc
of these worms mav also secrete anticoaeulanl. and
L,
small vessels, ruptured in the digcslion oC the
mucosal olue. mav continuc to bleed for some minutes
after the worm has moved to a fresh site.
Those with verv small buccal caosules. like the
trichostrongy~oids.~orsimple oral openings, like thc
ascaridoids, generallv feed on mucosal fluid, uroducb
of host digestion and cell debris, while others, such as
the oxyuroids, appear to scavenge on the contents of
the lower gut. Worms living in the bloodstream or
tissue spaces, such as the filarioids, feed exclusively
on body fluids. forms of oesophagus found in nematodes
, 6 Vererinary Parasitology
The so-called 'excretory system' is very primitive,
consisting o f a canal within each lateral cord ioinine
at the excretory pore in the oesophageal region.
The reproductive systems consist of lilamcntous
lubcs. The female organs comprise ovary. oviduct and
uterus, which may be paired, cnding in a common
short vagina which opens at the vulva. At the junction
of uterus and vagina in some species lhcrc is a short
muscular organ. lhc ovejector. which assists in egg-
laying. A vulva1 flap may also be present (Fig. 5).
The male organs consist of a single continuous
tcstis and a vas deferens terminating in an ejaculatory
duct into the cloaca. Accessory male organs are
sometimes important in identification, especially of the
trichostrongyloids. thc two most important bcing the
spicules and gubernaculum (Fig. 6). l'he spicules are
chitinous organs, usually paired, which are inserted in
thc female genital opening during copulation. The
gubernaculum. also chitinous, is a small structure which
acts as a guide for the spicules. With the two sexes in
close apposition the amoeboid spcrm are transferred from
the cloaca of the male into the utcrus of the female. Fig. 6 Spicules, gubernaculurn and bursa of a trichaslrongyloid
nematode.
The cuticle may be modified to form various struc-
tures, the more important (Fig. 7) of which are:
Leaf crowns consisting of rows of papillae occurring
as fringes round the rim of the buccal capsule (cxter-nal
lcaf crowns) or just inside the rim (internal lcaf crowns).
They are especially prominent i n certain nematodes of
horses. Their function is not known, but it is suggested
that they may be used to pin a patch of mucosa in position
during feeding, or that they may prevent the entry of
forcign matter into the buccal capsule when the worm has
detached from the mucosa.
Cervical papillae occur anteriorly in the oesopha:
geal region, and caudal papillae posteriorly at the tail.
They are spine-like or finger-like processes, and are
usually diametrically placed. Their function may be
sensory or supportive.
Cervical and caudal alae arc flattened wing-like ex-
pansions of the cuticle in the oesophageal and tail regions.
Ce~halicand cervical vesicles are inflations of the
cuticie around the mouth opening and in the oesopha-seal
region.
The ~upulatorybursa, which embraces the female
during cowlation, is im~ortantin the identification of
certaih &lc nematodes and is derived from much
expanded caudal alae, which are supported by elon-
gated caudal papillae called bursa1 rays. It consists of
FIB. 5 Scanning electron micrograph of a vulva1 flap of a two lateral lobes and a singlc small dorsal lobe.
trichostrongyloid nematode. Plaques and cordons arc plate-like and cord-like
, Veterinary Helminrhology 7
ornamentations present on the cuticle of many nema-
todes of the superfamily Spiruroidea.
BASE LIFE CYCLE
In the Ncmatoda, the sexes are separate and the males
arc ecncrallv smaller than the females which lav cees
, .u
or larvae. During development, a nematode moults at
-
invervals sheddine its cuticle. In thc c o m ~ l e t life
cv-cle there are four moults, thc successive larval
stages being designated L,, L,, L,, L, and tinally L,,
which is the immature adull.
One feature of the hasic nematode life cycle is that
immediate transfer of infection from onc final host to
another rarely occurs. Some dcvclopment usually
takes place either in the faecal pal or in a different
species of animal, the intermediate host, before infec-
tion can take placc.
In thc common form of direct life cycle, the frcc-
living larvae undergo two moults after hatching and
infection is by ingestion of the free b.There are some
important exceptions however, infection sometimes
being by larval penetration of the skin or by ingestion
of the e r e containing a larva.
In in%ect lifc cycles, the first two moults usually
take lace in an intermediate host and infection of lhe
final Lost is either by ingestion of the intermediate
host or hy inoculation of the L, whcn the intermediate
host, such as a blood sucking insect, feeds.
After infection, two further moults take place to
produce thc L, or immature adult parasite. Following
copulation a Iurther life cycle is initiated.
In the case of gastrointestinal parasites, develop-
ment may take place entirely in the gut lumen or with
onlv limited movement into the mucosa.
However, in many spccies, the larvae travel consid-
erable distancca through the bodv before settling in their
final (predilection) site and ;his is the migratory
Corm oI life cycle. One of the most common routes is
the hepatic-tracheal. This takcs developing stages from
the gut via the portal system to the liver then via the
hepatic vcin and poslerior vena cava to the heart and
from thcrc via the pulmonary artery to the lungs.
Larvac then travel via the bronchi. trachea and
oesophagus to the gut. It should he emphasized that the
above is a basic descri~tionof ncmatode liCe.cvcles
) E n e r n d o r s a l ray Doroal ray Lateral rays
and that there are many ;ariations.
Fig. 7 Nematode cuticular modifications. (a) Anterior; (b) Posterior
of male. DEVELOPMENT OF THE
PARASITE EGG
Ncmatode eggs differ greatly in dze and shape, and the
shell is of variable thickness, usually consisting of
three layers.
The inner membrane, which is thin, has lipid charac-
, leristics and is impermeable. A middle layer which is ?'he optimal temperature for the development of the
tough and chitinous gives rigidity and, when thick, maximum numher of larvae in the shortest feasible
imparts a yellowish colour lo the egg. In many species time is generally in the range 18-26'C. At higher tem-
this layer is interrupted at one or both ends with an peratures, development is faster and the larvae are
operculum (lid) or plug. The third outer layer consists
of protein which is very thick and sticky in the hyperactive, thus depleting their lipid reserves. The
ascaridoids and is important in the epidemiology of mortality rate then rises, so that few will survive to L,.
this superfamily. As the temperature falls the process slows, and below
In contrast, in some species thc egg shell is very 10°C the development lrom egg to L, usually cannot
thin and may be merely present as a sheath around the take place. Below 5 "C movement and metabo-lism of
larva. L, is minimal, which in many species favours survival.
The survival potential of the egg outside the hody The optimal humidity is 100%. although some de-
varies, but appears to be connected with the thickness velopment can occur down to 80% relative humidity.
of the shell, which protects the larva from desiccation. It should be noted that even in dry weather where the
Thus parasites whose infective form is the larvated amhient humidity is low, the microclimate in faeces or
egg usually have very thick-shelled eggs which can at the soil surface may be sufficiently humid to permit
survive for years on the ground. continuing larval dcvelopment.
In the trichostrongyloids and strongyloids, the
emhryonated egg and the ensheathed L, arc best
HATCHING equipped to survive in adverse conditions such as
on the species, eggs may hatch outside the freezing or dcsiccation: in contrast, the L, and L,arc
body or after ingestion. particularly vulnerable. Although desiccation is gener-
outside the body, hatching is controlled partly by ally considered to be the most lethal influence in larval
factors such as temperature moisture and part]y survival, there is increasing evidence that by entering
by the larva itself. the process of hatching, the inner a state of anhydrohiosis, certain larvae can survive se-
impermeable shell membrane is broken down by en- vere desiccation.
zymes secreted by the larva and by its own movement. o n t h e ground most larvae are active; although they
l-he larva is able to take up water from the ronmcnt require a iilm o l water for movement and are stimu-
and enlarges to rupture the remaining layers and hted light and temperature, it is now thought that
escape. larval movement is mostly random and encounter with
When the larvated egg is the infective form, the host g'a" accidental.
initiates hatching after ingestion by providing stimuli
for the larva which then comnletes ihe orociss. It is mlF~rTlnAr
en., L"
important for each nematode species that hatching
s , u s .
should occur in appropriate regions of the gut and Asnoted previously, infection may be by ingestion of
hence the stimuli will differ, although it appears that thc free-living L,,and this occurs in the majority of
dissolved carbon dioxide is a constant ecsential. trichostrongyloid and strongyloid nematodes. In these,
the L, sheds the retained sheath of the L, within
the alimentary tract of the host, the stimulus for
LARVAL DEVELOPMENT AND SURVIVAL exsheathment being provided by the host in a manner
Three of the important superfamilies, the tri- similar to the hatching stimulus required by egg-infec-
chostrongyloids. the strongyloids and the rhab-ditoids, live nematodes. In response to this stimulus the larva
have a complctcly free-living prcparasitic phase. The releascs its own exsheathing fluid, containing an en-
first two larval stages usually feed on bac-teria, but the zyme lcucine aminopeptidase, which dissolves the
L,, sealed olI from the environmcnt by the retained sheath horn within, either at a narrow collar anteriorly
so that a cap detaches, or by splitting the sheath longi-
cuticle of the L,cannot feed and must survive on the
tudinally. The larva can then wrigglc free of the
stored nutrients acquired in the early stages. Growth of sheath.
the larva is interrupted during moulting by periods of As in the preparasitic stage, growth of the larva
lethargus in which it neither feeds nor moves. during parasitic development is interrupted by two
The cuticle of the L, is retained as a sheath around moults, each of these occurring during a shorl period
the L,; thisisim~ortantinlarval survival with a orotec- of lethargus.
tlve role analogouq to that of the egg shell jn egg- The time taken for developmcnt from infection un-
infective groups. til mature adult parasites are producing eggs or larvae
The two most important components o l the external is known as the prepatent period and this is of
environment are temperature and humidity. known duration for each nematodc species.
