Comparative Morphology of Ancylostoma tubaeforme (Zeder, 1800) and Ancylostoma caninum (

Ercolani, 1859)
Author(s): Robert B. Burrows
Source: The Journal of Parasitology, Vol. 48, No. 5 (Oct., 1962), pp. 715-718
Published by: Allen Press on behalf of American Society of Parasitologists
Stable URL: http://www.jstor.org/stable/3275261
Accessed: 03-11-2015 16:28 UTC

REFERENCES
Linked references are available on JSTOR for this article:
http://www.jstor.org/stable/3275261?seq=1&cid=pdf-reference#references_tab_contents

You may need to log in to JSTOR to access the linked references.

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/
info/about/policies/terms.jsp

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content
in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship.
For more information about JSTOR, please contact support@jstor.org.

Allen Press and American Society of Parasitologists are collaborating with JSTOR to digitize, preserve and extend access to
The Journal of Parasitology.

http://www.jstor.org

This content downloaded from 132.203.227.62 on Tue, 03 Nov 2015 16:28:42 UTC
All use subject to JSTOR Terms and Conditions
 THE JOURNAL OF PARASITOLOGY
Vol. 48, No. 5, October 1962, p. 715-718

COMPARATIVE MORPHOLOGY OF ANCYLOSTOMA TUBAEFORME (ZEDER, 1800)

AND ANCYLOSTOMA CANINUM (ERCOLANI, 1859)

ROBERTB. BURROWS
The Wellcome Research Laboratories,BurroughsWellcome & Co. (USA) Inc., Tuckahoe, New York

ABSTRACT

As a result of studies of Ancylostoma from European, African, and Australian dogs and
cats, it was found that dogs harbored A. caninum and cats A. tubaeforme. A detailed study of
these hookworms from dogs and cats in the United States confirmed the observations made
by other investigators that A. caninum is not the common species in cats. A. tubaeforme
differs from A. caninum in the following features: smaller size, larger ventral and esophageal
teeth, shorter esophagus, thicker cuticle, smaller bursa, different arrangement of lateral
bursal rays, smaller costa dorsalis, longer spicules, and shorter, narrower female tail. The
two species apparentlyhave world-wide distributionand A. caninum is seldom or never found
as a natural infection of cats or A. tubaeforme as a natural infection of dogs.

In 1800 Zeder (Biocca, 1954) described
hookworms he found in a cat in 1783, giving
them the name Strongylus tubaeformis. Then
in 1859 Ercolani (Biocca, 1954) published a
description of the dog hookworm, naming it
Sclerostoma caninum. Later S. caninum was
transferred to the genus Ancylostoma, but S.
tubaeformis apparently was overlooked by
most investigators. For nearly 100 years the
common hookworm of both dogs and cats was
referred to as Ancylostoma caninum.
A number of investigators (Scott, 1928,
1929; McCoy, 1931; Foster and Cort, 1932;
and others) found that it was difficult to infect
dogs with larvae from cats and cats with larvae
from dogs. However, the differences were be-
lieved to be physiological rather than morpho-
logical, and the two were considered different
strains of the same species.
In 1954 Biocca published the results of his
detailed study of Ancylostoma from dogs and
cats in Italy. He found that there were two
species rather than two strains of one species.
In his paper he gave the original descriptions
of both Zeder and Ercolani, a redescription of
A. tubaeforme, and the major morphological
differences between the two species. Bohm
(1955) in Austria, Rohde (1959) in Germany,
and Fitzsimmons (1961a, b), who studied
hookworms from both African (Nyasaland)
and Australian dogs and cats, agreed with the
findings of Biocca.
In the United States the writer has noticed
in chemotherapeutic trials of several active
compounds that the activity is not always the
Received for publication 4 June 1962.
715
same against Ancylostoma from dogs and those
from cats. After consulting the papers by
Biocca and Rohde, a detailed examination was
made of hookworms obtained from dogs and
cats in this country. As the morphological dif-
ferences agree with those found by other in-
vestigators in Europe, Africa, and Australia,
it is evident that we are dealing with two dif-
ferent species, each of which appears to have
a world-wide distribution. The major differ-
ences are described and illustrated below.
MATERIALS AND METHODS
Ancylostoma were obtained from 12 dogs and
9 cats used in chemotherapeutictrials in this lab-
oratory. Numerous measurementswere made from
relaxed worms obtained either as a result of treat-
ment or at autopsy. Numbers of worms were fixed;
the anterior and posterior ends cut off; the middle
sections discarded; and the ends dehydrated,
cleared, and mounted for detailed study. The
best of the numerous mounted ends were photo-
graphed to illustrate the major differences between
the two species.
Ancylostoma from a number of other dogs and
cats were examined to determine whether natural
infections of A. caninum occurred in cats or A.
tubaeforme in dogs.
DIFFERENTIATION OF THE TWO SPECIES
(All measurements in millimeters,
unless otherwise stated)
Sizes of worms: Measurements of lengths
and widths of 20 mature males and 20 mature
females of each species gave the following
ranges and averages: A. tubaeforme: males,
9.5 to 11.0 by 0.30 to 0.35 (avg. 10.3 by 0.32);
females, 12.0 to 15.0 by 0.38 to 0.43 (avg. 13.2
by 0.41); A. caninum: males, 11.0 to 13.0 by

This content downloaded from 132.203.227.62 on Tue, 03 Nov 2015 16:28:42 UTC
All use subject to JSTOR Terms and Conditions
716 THE JOURNAL OF PARASITOLOGY Vol. 48, No. 5

M._;_ o

< ,s ~ .~~~~~~~~~~~:
~~~~~~~~~~~~~~~~~
: E;
-i:

JIlf . s"i
l .:w.i000

!L
: -i R c Li;

::: ::: ..... P

:' "' i:ii:i:l
i' K :Rt : .i

iti: :,XS g tBS,- .~~~~~~~~~~~~?t;

* .i
-TDx'fflB.l
*p'::
.:::...S:X

'

,:iii:
''.C ,
.t.*>
s

ax:
: C atEaiiix:
.S'-~:
g.

:i
i/-::::i:i::l::
E ii
i::a:-. i:' .:

:i:: : : i

. .-ii_:::: -:
;::.

- .:..
:i :::

i::

....
g
.a.fs

-
:.
s

.;'
<
w

*'''*
s
-B s

a *

'.'w'1'M

Al

PLATE I

This content downloaded from 132.203.227.62 on Tue, 03 Nov 2015 16:28:42 UTC
All use subject to JSTOR Terms and Conditions
 BURROWS-THE CAT HOOKWORMIN THE UNITED STATES 717

0.34 to 0.39 (avg. 11.7 by 0.37), females, 14.0
to 20.5 by 0.50 to 0.56 (avg. 17.0 by 0.52).
In both sexes the upper limits of A. tubaeforme
are approximately the lower limits of A.
caninum.
Mouth: The mouth of A. tubaeforme is
smaller than that of A. caninum, which is in
keeping with the smaller over-all size. Each
species has a pair of prominent chitinous plates
bearing three teeth-the ventral teeth. Al-
though the mouth of A. tubaeforme is smaller,
the ventral teeth (A, C) are larger than those
of A. caninum (B, D). The distance from the
anterior border of the plate to the tip of the
middle tooth, when the mouth is oriented in
a horizontal position, ranges from about 50 to
58 /i in A. tubaeforme and about 45 to 52 t
in A. caninum. The esophageal teeth of A.
tubaeforme (E, G) are larger than those of
A. caninum (F, H), project farther into the
buccal cavity, and are generally convex on the
anterior margin; whereas the anterior margin
of these teeth in A. caninum is usually concave,
sometimes straight. The mouth of A. tubae-
forme is turned more dorsad than that of
A. caninum (E-H).
Esophagus: The esophagus was measured
in 30 worms of each species with approxi-
mately half being males. In A. tubaeforme the
range and average were 0.81 to 0.95 (avg.
0.87) and in A. caninum 1.13 to 1.26 (avg.
1.18). The proportionate length of the
esophagus to the entire worm is not the same
in the two species; for in some worms 14 to
15 mm long, the esophagus was 0.90 or less
in A. tubaeforme and 1.11 or more in A.
caninum.
Cuticle: Biocca (1954) stated that the
cuticle of A. tubaeforme appears thicker than
that of A. caninum due to the slenderer body
of the former. However, measurement of the
cuticle of the two species leads to the con-
clusion that the thicker cuticle of A. tubae-
forme is real rather than apparent. The meas-
urements, in microns, made on 20 worms of
each species produced the following average
thicknesses: base of buccal cavity, 7.2 for
A. tubaeforme vs. 3.1 for A. caninum; near
excretory pore, 9.6 vs. 7.2; above anus of
female, 13.7 vs. 6.2; below anus of female,
8.9 vs. 6.1; and above bursa of male, 17.2 vs.
10.7. The thicker cuticle of A. tubaeforme is
evident when Q and S are compared with R
and T.
Bursa: The lateral lobes of the bursa are
larger in A. caninum, being about 0.45 to 0.49
in width; whereas, those of A. tubaeforme are
about 0.35 to 0.39. In both species the three
lateral costae have a single origin, the postero-
lateral ray branching first and the other two
separating slightly farther down. In A. caninum
(J) the exterolateral ray is about 1.5 times as
far from the mediolateral as is the postero-
lateral. In A. tubaeforme (I) the postero-
lateral and mediolateral are close together, so
that the extemolateral is about 2 to 2.5 times
their distance from the mediolateral. The dor-
sal lobe of the bursa is larger in A. caninum,
and the costa dorsalis is both longer and
broader (L) than in A. tubaeforme (K).
Spicules: In cleared and mounted worms
the differences in the lengths of the spicules
become obvious. Those of A. caninum (N)
range in length from 0.73 to 0.96 (avg. 0.86);

PLATEI
(In each pair of figures A. tubaeforme is on the left, A. caninum on the right.)
FIGURES
A, C. Dorsal view of mouth of A. tubaeforme. X 100.
FIGURESB, D. Dorsal view of mouth of A. caninum. X 100.
FIGURESE, G. Lateral view of mouth of A. tubaeforme. X 100.
FIGURESF, H. Lateral view of mouth of A. caninum. X 100.
FIGUREI. Portion of lateral lobe of bursa of A. tubaeforme. X 100. e, externolateralray; m, medio-
lateral; p, posterolateral.
FIGUREJ. Portion of lateral lobe of bursa of A. caninum. X 100.
FIGUREK. Costa dorsalis of A. tubaeforme. X 100.
FIGUREL. Costa dorsalis of A. caninum. X 100.
FIGUREM. Spicules of A. tubaeforme. X 50.
FIGUREN. Spicules of A. caninum. X 50.
FIGUREO. Enlargement of anterior end of spicule of A. tubaeforme. X 300.
FIGUREP. Enlargement of anterior end of spicule of A. caninum. X 300.
FIGURESQ, S. Female tail of A. tubaeforme. X 100.
FIGURESR, T. Female tail of A. caninum. X 100.

This content downloaded from 132.203.227.62 on Tue, 03 Nov 2015 16:28:42 UTC
All use subject to JSTOR Terms and Conditions
718 THE JOURNAL OF PARASITOLOGY
whereas, those of A. tubaeforme (M) are 1.10
to 1.47 (avg. 1.29), or about 50% longer. The
anterior ends of the spicules are about 10 to
15 I in diameter in both species. However,
the scoop-shaped opening of the spicule of
A. caninum is 24 to 33 Ix in length (P), or
slightly more than twice the spicule diameter;
whereas, in A. tubaeforme it is 48 to 69 I
long (0), or over four times the spicule
diameter.
Female tail: The two species differ in the
shape and size of the female tail. In A.
caninum (R, T) the tail is longer and broader,
ranging in length from 0.25 to 0.32 (avg.
0.28); whereas, that of A. tubaeforme is shorter
and narrower, ranging from 0.16 to 0.23 (avg.
0.18) in length. In A. caninum the posterior
end of the body tapers gradually with the tail
being a continuation of the tapering. However,
in A. tubaeforme there is an abrupt narrowing
posterior to the anus, and the tail often is
curved ventrad.
Eggs: Measurements were made of 25 con-
secutive eggs from each of five stools from dogs
with A. caninum and from each of five stools
from cats with A. tubaeforme. The ranges and
averages of the eggs of the two species are:
A. tubaeforme, 55.0 to 75.7 Ix by 34.4 to
44.7 tJ (avg. 61.3 by 40.0 ux); A. caninum,
55.0 to 72.2 ut by 34.4 to 44.7 Ix (avg. 62.2
by 38.8 I). The measurements are so similar
that it is impossible to distinguish the two
species on the basis of eggs alone.
Prevalence and intensity of infection: Dur-
ing a 6-year period stool examinations were
done on 1,331 dogs and 1,568 cats from New
Jersey. Eggs of A. caninum were found in
24% of the dogs and eggs of A. tubaeforme
in 37% of the cats. In 213 of these Ancylos-
toma-infected dogs which were autopsied, the
number of A. caninum ranged from 1 to 547,
with an average of 49.7 per dog. In 235
Ancylostoma-infected cats autopsied, the num-
This content downloaded from 132.203.227.62 on Tue, 03 Nov 2015 16:28:42 UTC
All use subject to JSTOR Terms and Conditions
Vol. 48, No. 5
ber of A. tubaeforme ranged from 1 to 124
with an average of 20.1 worms per cat. Al-
though cats had 1.5 times the incidence of
Ancylostoma found in dogs, the latter had an
average worm burden approximately 2.5 times
that of cats.
Nonspecific infections: In all the dogs and
cats examined carefully for species of Ancylos-
toma present there was no evidence of A.
tubaeforme in dogs or of A. caninum in cats.
LITERATURE CITED
BIOCCA, E. 1954. Ridescrizione di Ancylostoma
tubaeforme (Zeder, 1800) parasitta del gatto,
considerato erroneamente sinonimo di Ancylos-
toma caninum (Ercolani, 1859), parassita del
cane. Riv. Parassit. 15: 267-278.
BOHM, L. K. 1955. Uber die in Osterreich ver-
breitete Ancylostomosisder Katzen und ihren
Erreger, den spezifischen Katzen-Hakenwurm
Ancylostoma tubaeforme (Zeder, 1800). Wien.
Tierarztl. Monatschr. 42: 760-763.
FITZSIMMONS, W. M. 1961a. Observations on
the parasites of the domestic cat. Vet. Med.
56: 68-69.
. 1961b. The so-called cat and dog
strains of Ancylostoma caninum. Vet. Rec.
73: 585-586.
FOSTER, A. O., AND W. W. CORT. 1932. The
effect of a deficient diet on the susceptibility
of dogs and cats to non-specific strains of
hookworms. Am. J. Hyg. 16: 582-601.
McCoY, O. R. 1931. Immunity reactions of the
dog against hookworm (Ancylostoma cani-
num) under conditions of repeated infection.
Am. J. Hyg. 14: 268-303.
ROHDE, K. 1959. Vergleichende Untersuchungen
iiber die Hakenwiirmer des Hundes und der
Katze und Betrachtungen iiber ihre Phy-
logenie. Ztschr. Tropenmed. Parasit. 10: 402-
426.
SCOTT, J. A. 1928. An experimental study of
the development of Ancylostoma caninum in
normal and abnormal hosts. Am. J. Hyg. 8:
158-204.
1929. Experimental demonstrationof
a strain of the dog hookworm, Ancylostoma
caninum, especially adapted to the cat. J.
Parasit. 15: 209-215.