Alaria marcianae

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Life History of Alaria marcianae (La Rue, 1917) Walton, 1949 (Trematoda: Diplostomatidae)

Author(s): Allen D. JohnsonSource: The Journal of Parasitology, Vol. 54, No. 2 (Apr., 1968), pp. 324-332Published by: The American Society of ParasitologistsStable URL: http://www.jstor.org/stable/3276944 .

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THE JOURNAL OF PARASITOLOGY

Vol. 54, No. 2, April 1968, p. 324-332

LIFEHISTORYOF ALARIAMARCIANAELARUE,1917) WALTON,1949 (TREMATODA:IPLOSTOMATIDAE)*

Allen D. Johnsont

Department of Zoology, University of Minnesota, Minneapolis

ABSTRACT: The experimentallife cycle of Alaria (A.) marcianae (La Rue, 1917) Walton, 1949, in-volves planorbid snails, Helisoma trivolvis and H. campanulatum,as first intermediatehosts; tadpolesof the leopardfrog, Rana pipiens, as second intermediatehosts; mice, rats, and chicks as paratenichosts;and the domestic cat as definitive host. The life cycle is similar to known cycles in the subgenusAlaria,where avian and mammalian ntermediatehosts of the mesocercariaeserve as paratenichosts; butit differs from the only known cycle in the subgenus Paralaria,where the mesocercariaedevelop intometacercariaein avian and mammalian intermediatehosts. This difference in mesocercarial behaviorrepresents a distinct biological difference between members of the two subgeneraand is an additionalsubgeneric character. Alaria (A.) minnesotaeChandler,1954, is a synonymof A. (A.) marcianae (new

synonymy).

Six Alaria spp. belonging to the subgenusAlaria Schrank, 1788, have been described

from indigenous North American carnivores:

A. americana Hall and Wigdor, 1918; A.

arisaemoides Augustine and Uribe, 1927; A.

oregonensis La Rue and Barone, 1927; A.

canis La Rue and Fallis, 1934; A. minnesotae

Chandler, 1954; and A. marcianae (La Rue,

1917) Walton, 1949. Of the first five species,

Dubois (1963) considered only A. americanaand A. arisaemoides valid. Alaria marcianae,the subject of this study, was not included in

his revision.

From 1960 to 1964, the writer collected

adults of an Alaria (A.) sp. from several dif-

ferent carnivore hosts in Minnesota. Additional

specimens collected during 1937 and 1938

were available for study. Morphological studies

were made of these worms, and the completelife history was studied in experimental hosts

beginning with eggs. These parasites werethen identified as A. marcianae.

HISTORICALREVIEW

La Rue (1917) described the mesocercaria

of A. marcianae from the garter snake, Tham-

nophis marcianus (Baird and Girard) (= T.

marciana), and named it Cercaria marcianae.

Cort (1918) redescribed this stage collected

from tadpoles of the leopard frog Rana pipiens

Received for publication25 September1967.* Portion of a thesis for the degree of Doctor of

Philosophy submitted to the Graduate School,University of Minnesota, 1965.

t Present address: Department of Zoology, Uni-versity of South Dakota, Vermillion, 57069.

324

Schreber and green frog R. clamitans Latreille,and from the garter snake, Thamnophis sirtalis

(L.). Cort demonstrated that snakes may

serve as paratenic hosts for the mesocercaria.

Cort and Brooks (1928) described the sporo-

cyst and cercarial stages from naturally in-

fected snails, Helisoma trivolvis (Say) and H.

campanulatum (Say), and recovered meso-

cercariae from tadpoles exposed to cercariae.

Cuckler (1941) fed mesocercariae obtainedfrom naturally infected leopard frogs to cats

from which A. marcianae adults were subse-

quently recovered. Thus he first established

that Alaria spp. require only three hosts instead

of four as reported by Bosma (1931) and

Odlaug (1940). In the definitive host a

tracheal migration occurs involving the transi-

tion of the mesocercariae to metacercariae in

the lungs before the adult stage is attained in

the small intestine. Cuckler also fed meso-

cercariae to mice and stated that they developto metacercariae. Although it is evident from

an abstract of Cuckler's study (1940) that he

was working with A. marcianae, Walton (1949)first formally proposed that Cercaria marcianae

be placed in the genus Alaria. The first pub-lished description of the adult was provided

by Burrows and Lillis (1965) who obtained

adults from a naturally infected cat. Theyidentified the adults by comparison with the

description in Cuckler's thesis.

MATERIALSAND METHODS

Colonies of four species of planorbid snails,Helisoma trivolvis, H. campanulatum,H. corpulen-tum (Say), and Gyraulus deflectus (Say), wereestablished from egg masses laid by field collected



JOHNSON-LIFE HISTORYOF ALARIAMARCIANAE LA RUE, 1917) (TREMATODA) 325

adults. The age of snails used in experimentswasestimated by comparing size with larger, labora-

tory-rearedadults.

Life cycle studies were started with eggs col-lected by repeated sedimentation of the scrapedintestinal mucosa of two striped skunks, Mephitismephitis (Schreber). Eggs were incubated in dis-tilled water at room temperature. When miracidia

appearedfully developed (ca. 20 days), the eggswere put in small vials, covered with cheesecloth,and placed in 10-cm finger bowls containing thesnails.

Laboratory-reared adpoles and frogs were ex-

posed to cercariae singly or in groups of two tofour in 10-cm finger bowls. For the recovery of

large numbers of mesocercariaefrom infected tad-

poles or frogs, the tissues were teased apart and

placed on a screen in a funnel containing 0.7%saline. The larvae, free of debris, could be col-lected in a few ml of saline withdrawn from thefunnel.

Known numbers of mesocercariaefrom experi-mentally infected tadpoles were either force-fed to

laboratory-rearedmice and rats and to 1-day-oldunfed chicks, or injected intraperitoneally. Theywere fed to a laboratory-rearedcat in pieces ofraw liver and to a parasite-free raccoon in raw

eggs. After examination of the tissues of infected

mice, rats, and chicks for larvae, the remainingmaterial was ground up in a meat grinder and

either artificially digested (0.6% pepsinin

0.35%HC1 at 37 C) or placed on a screen in a funnel

containing 0.9% saline (extraction method) forthe recovery of additional larvae.

The writer collected adults of A. marcianaefrom the following carnivores examined: 3 of 6

cats; 5 of 10 stripedskunks;1 of 2 spotted skunks,

Spilogale putorius (L.); 1 of 10 red foxes, Vulpes

fulva (Desmarest); both of 2 gray foxes, Urocyoncinereoargenteus(Schreber); none of 8 raccoons,Procyonlotor (L.); and none of 3 badgers,Taxidea

taxus (Schreber). Collection specimenswere avail-

able from one striped skunk, three spotted skunks,and one badger. Adults used for measurements

were fixed without pressurein hot 10% formalin,cleared in methyl salicylate, and mounted in pic-

colyte. For fixation of cercariae an equal volumeof boiling 10% formalin was added to water con-

taining cercariae. Wet mounts of cercariae were

prepared for measurements. Sporocysts, meso-

cercariae,and metacercariaewere fixed in hot 10%formalin. Measurementsof sporocysts were fromstained and mounted specimens, while those of

mesocercariaeand metacercariaewere from glyc-erine-cleared specimens. Morphological studies of

larvae are based on both living and fixed material.Measurements are given in microns unless indi-

cated otherwise.

RESULTS

First intermediate hosts

Sporocysts developed in all three Helisoma

spp., but none of the H. corpulentum shed

TABLE I. Results of exposure of snails to eggs ofAlaria marcianae.

Snailspecies

Helisoma trivolvis

Helisoma campanulatum

Helisoma corpulentum

Gyraulus deflectus

Age of

snails

1/2 to 3/4

grown3?grown

% grown

12 grown

Numberexposed

30

7

7

17

Numberinfected

19

7

51

0

1 Sporocysts present but no cercariae shed.

cercariae (Table I). No sporocysts were found

in Gyraulus deflectus.

Although these results indicate that G. de-

flectus is not a suitable host for A. marcianae,the status of H. corpulentumr is not clear.

Sporocysts developed in five of seven H. cor-

pulentum but no developing cercariae were

present in daughter sporocysts even though

compared to the other two Helisoma spp.sufficient time was allowed for cercarial de-

velopment.

Second intermediate host

Seven young adult frogs and 93 tadpoleswere

exposedto cercariae shed

byH. trivolvis

and H. campanulatum. No larvae were found

in the adult frogs which were killed 10 to 22

days after infection. All tadpoles became in-

fected and fully developed mesocercariae were

recovered after 2 weeks. The larvae were

present in the thoracic, throat, back, and tail

muscles. Most were free in the tissues, al-

though a few larvae were individually en-

capsulated. After metamorphosis of the tad-

poles the mesocercariae in young frogs were

found primarily encapsulated in masses ven-tral to the mylohyoid muscles of the throat,

ventral to the sternum and between the mus-

cles of the thighs.

Paratenic hosts

Two rats, three mice, and three 1-day-oldunfed chicks were infected with mesocercariae.

The animals were killed 7 to 35 days after

infection and mesocercariae were recovered

from all (Table II). In rats and mice the

larvaewere observed in the

subscapular fat,thigh muscles, abdominal muscles, and the

fatty tissues and glands of the throat and jaw

region. The larvae in chicks were present in

the neck, back, breast, and leg muscles. The

larvae in all host species were individually



326 THEJOURNAL OF PARASITOLOGY, OL. 54, NO. 2, APRIL1968

TABLE II. Results of infection of paratenic hosts with mesocercariaeof Alaria marcianae.

No. ofHost No. of Method of Days after Method of larvae

species larvae given infection infection recovery recoveredrat 275 F 7 A 3

rat 375 F 35 A 24

mouse 280 I 30 A 2

mouse 280 I 31 E 53

mouse 400 I 31 E 50

chick 400 F 34 E 27

chick 290 I 32 E 64

chick 315 I 34 E 41

F = mesocercariae force-fed.

I = mesocercariae intraperitoneally injected.A = artificial digestion.E = extraction method.

encapsulated but readily escaped from the

cysts in saline.

None of the mesocercariae showed any ad-

vancement in development. Odlaug (1940)found that mesocercariae of A. mustelae Bosma,

1931, develop to metacercariae in 10 days in

mice and rats, so sufficient time was allowed

for possible further development.

Definitive host

Ayoung

cat was fed 150,100,

and 150

mesocercariae on 3 successive days and was

then fed 150 mesocercariae 30 days after the

initial feeding. Fluke eggs were first seen in

stool specimens 19 days after the initial feed-

ing. The cat was killed 41 days after the initial

feeding, and the lungs, trachea, esophagus,

stomach, and small intestine were removed

and examined separately. The lungs con-

tained 16 metacercariae, and more than 200

worms were recovered from the anterior third

of the small intestine.Except

for one imma-

ture worm, all intestinal forms were sexuallymature. It is considered that the adults re-

sulted from the first feedings, whereas the

metacercariae and the immature worm resulted

from the infection 30 days later. Metacercariae

were judged to be fully developed since theywere as large as the immature worm from the

intestine.

A raccoon kept in the laboratory for over

2 years was fed mesocercariae on four different

occasions over a period of 7 days with 350,

1,000, 250, and 125 larvae, respectively. Stool

specimens from this raccoon at the time it

was brought into the laboratory and again a

few days before infection were negative for

fluke eggs. The animal was killed 19 days

after the first feeding. No worms were found

in the lungs, esophagus, trachea, stomach, or

small intestine. Parts of the thigh muscle and

the diaphragm muscle were removed and arti-

ficially digested but no larvae were recovered.

Description of stages

Sporocysts

The sporocysts were only briefly described

by Cort and Brooks (1928) as elongate, un-

branchedsporocysts

in thedigestive gland

of

infected snails.

Description: Mother sporocysts in anterior re-

gion of snail hosts, exact location not determined;five specimens from H. trivolvis averaging 14.8

(14.1 to 16.4) mm long by 216 (109 to 306)wide. Birth pore and anterior spines not seen.Germinal masses and daughter sporocyst embryosin sporocyst lumen.

Daughter sporocysts (Fig. 5) in digestive glandof snail hosts, 10 specimensfrom H. trivolvis aver-

aging 1.82 (1.50 to 2.25) mm long by 69 (61 to82) wide. Spinespresentat anterior end and birth

pore near anterior end. Germinal masses and cer-cariae in various stages of development in sporo-cyst lumen.

Cercaria Fig. 1)

Cort and Brooks (1928) described the cer-

caria but important differences in the spina-tion and additional morphological characters

are noted here.

Description: (Measurements of 20 specimensfrom H. trivolvis) Furcocercous, longifurcous, di-stomate, and pharyngeate. Body, 143 (108 to 190)long by 41 (35 to 49) wide; tail stem, 217 (187

to 245) long by 22 (22 to 25) wide; furcae, 191(167 to 218) long; oral sucker, 37 (31 to 45)long by 26 (22 to 31) wide; pharynx, 11 (10 to

14) long by 13 (11 to 14) wide; ventral sucker,22 (20 to 24) long by 22 (20 to 25) wide.

Genital primordium midway between ventralsucker and bladder. Unpigmented eyespots mid-



JOHNSON-LIFEHISTORYF ALARIAMARCIANAELARUE,1917) (TREMATODA)

way between oral and ventral suckers laterally.About six pairs of caudal bodies in tail stem. Two

pairs of preacetabular penetration glands; ducts

opening into oral cavity.Oral hood composed of several rows of stag-

gered spines. Spines smaller and less dense pos-terior to oral hood, extending to posterior end of

body ventrally except for small spineless areas

posterior and anterior to ventral sucker; dorsalsurface spines extending to level slightly posteriorto pharynx, then scattered posterior to ventralsucker and in posterior one-fifth of body. One

pair of sensory hairs laterally on posterodorsalsurface. Two to four, usually three, rows of scat-tered spines around ventral sucker. Number of

long sensory hairs on lateral margin of tail stem.Two bands of small spines on ventral and dorsal

surfaces of tail stem; bands of spines continuingout along ventral and dorsal edges of furcae.

Flame cell formula: 2[(2+2+2)+(2+2)+(2)];bladder bicornuate and lacking an island of Cort.

Bladder arms convoluted at level of posteriorend

FIGURES 1-2. Alaria marcianae. Freehand toscale, ventral views. 1. Cercaria, from living and

preserved specimens. Spination shown on rightside and excretory system on left. 2. Adult, from

preserved specimen.Abbreviations: bat, blind anterior tubule; eip,

ejaculatorypouch; la, lappet.

3 4

dc bp

5

FIGURES 3-5. Alaria marcianae. Freehand to

scale, from living and preserved specimens. 3.

Metacercaria,ventral view.

Onlymajor branches

of reserve excretory system shown. 4. Mesocer-

caria, ventral view. Spinationshown on right sideand primaryexcretory system on left. 5. Daughtersporocyst.

Abbreviations: ac, anterior commissure; bp,birth pore; dc, developing cercaria; eb, excretorybladder; gb, germ ball; gr, genital rudiment;mlv,main lateral vessel; pac, postacetabular commis-

sure; pb, posterior branch; poc, postpharyngealcommissure.

of ceca; anterior blind tubule present. Caudal ex-

cretory tubule passes medially through tail stem;excretorypores located midfurcallyand dorsally.

Mesocercaria (Fig. 4; measurements of

15 specimens from tadpole)

The mesocercaria is essentially an enlargedcercarial body but it lacks the pair of sensory

hairs and possesses a more complex excretory

system.

The flame cell formula is: 2[(2-6+2-6+2-6)

+(2-6+2 6)]. The only variationseen from the

six flame cellsper group

was on two occasionswhen only five were seen. The mesocercaria

differs from the descriptiongiven by Cort (1918)

only in possessing anteriorand posteriorblind ex-

cretory tubules and pre- and postacetabularspine-less areas.

Body 413 (393 to 435) long by 161 (146 to

327



TABLE 3. Comparative measurements of adults of Alaria marcianae and A. americana in microns.

Species -* A. marcianae A. marcianae A. marcianae A. marcianae A. marcianae A. american

(after Cuckler, (after Burrows (after Chandler, (present study) (present study) (after Hall a1941) and Lillis, 1965) 1954) Wigdor, 191

Host -> cat, dog cat cat, Mephitis cat Mephitis dogmephitis mephitis

Total length 1.77 1.69 1.66

(in millimeters) (1.28-2.21) (1.210-1.600) (1.45-1.9) (1.57-1.75) (1.56-1.84) (1.16-2.32)

Oralsucker length 88 (75-102) (79-103) (105-114) 101 (88-122) 105 (95-122) (90-137)width 82 (66-99) (93-114) (diameter) 95 (82-109) 119 (102-136) (diamete

Ventralsucker length 77 (66-92) (74-100) 95 (average 78 (68-88) 90 (75-109) (70-176)width 81 (72-99) (diameter) diameter) 84 (78-95) 109 (88-122) (diameter

Pharynx length 118 (99-135) (114-150) (118-155) 126 (112-143) 165 (150-177) (120-196)width 85 (59-105) (78-96) (80-111) 84 (78-95) 116 (109-136) (80-137)

Holdfast organ length 535 (402-775) (330-473) (480-667) 590 (520-690) 620 (540-700)width 300 (144-434) (150-233) (248-310) 200 (160-240) 360 (280-570)

Ratio of lengths

pharynx:oral sucker 1:0.752 1:0.80 1:0.63

Ratio of lengthshindbody:forebody 1:1.592 1:1.64 1:1.62

Ratio of length to width

of holdfast organ 1:0.562 1:0.35 1:0.58

Eggs' length 125 (118-126) 120 (112-129) (90-120)

(uterine) width 70 (72-75) 72 (65-75) (80-86)

Position of ventral

sucker in forebody 30/100 31/100

1Eggs of A. marcianae in feces after Burrows and Lillis, 110 to 127 by 65 to 72, and in present study from the cat, 127 (119-140)

feces after Hall and Wigdor, 106 to 134 by 64 to 80, and after La Rue and Fallis, 125 (107-133) by 82 (77-99).2Determined here from average measurements.3 After Dubois, 1938.




190) wide; oral sucker,88 (81 to 95) long by 58

(53 to 67) wide; ventral sucker, 61 (57 to 64)long by 60 (56 to 66) wide.

Metacercoria (Fig. 3)

Cuckler (1941) did not describe the meta-

cercaria but did state that it was similar to

that of A. mustelae (see Bosma, 1934). How-

ever, of the metacercariae examined here the

body shape and also the reserve excretory

system were distinctly different from those of

A. mustelae.

Description: (Measurements of 10 specimens)Typical diplostomulum type metacercaria. Total

body length, 656 (593 to 731); forebody width,

363 (304 to 373); hindbody, small, conical, pro-jecting up to 50; oral sucker, 74 (67 to 81) longby 63 (56 to 73) wide; ventral sucker, 64 (59 to

73) long by 64 (59 to 70) wide; pharynx,50 (46to 56) long by 42 (36 to 48) wide; holdfast organ,209 (184 to 238) long by 99 (82 to 109) wide;lappets,maximum ength of 100. Genital rudimentnot well differentiated.

Bladder enlarged with prominent medial out-

growth extending anteriorly. Bladder arms turn-

ing laterad and becoming convoluted near level ofanterior end of holdfast organ. Primaryexcretorysystem not traced beyond this point. Main lateralvessels of reserve excretory system arising from

anteriorloop of each bladder arm extending for-ward to anterior end of body. Laterallyeach mainvessel giving rise to one posteriorbranch, one ortwo lateral branches, and one small anterolateralbranch. Main posterior branches giving rise lat-

erally to smaller divisions and medially to series ofat least six transverse commissures. Entire courseof individual commissures could not be followed.Main posteriorbranches continuingposteriorlybutunion not observed. Main lateral vessels givingrise medially to three branches forming, respec-tively, postacetabular commissure, postpharyngealcommissure,and anteriorcommissure. Median ves-sel

joiningthree commissuresand

apparentlyend-

ing blindly dorsal to holdfast organ. All abovebranches giving rise to smaller divisions endingblindly in excretory granules.

Adult (Fig. 2)

Burrows and Lillis (1965), and also Cuckler

(1941) in his thesis, adequately described the

adult, and my measurements of adults givenhere from a striped skunk and the experi-

mentally infected cat are similar to theirs

(Table III).

However, certain mensural differences are

evident between the adults from the skunk

and cat. The worms from both hosts were

fixed, and slides prepared, in the same manner,but those from the skunk were dead at the

time of fixation. As a result, the holdfast

organ of adults from the skunk was more

expanded, often covering part or all of the

ventral sucker; and the oral sucker, ventral

sucker, and pharynx were larger. Thus ratios

involving these structures are different for the

two groups of worms. This becomes importantwhen it is recognized that the actual and rela-

tive sizes of these structures have been used

in distinguishing Alaria spp. (Dubois, 1963).Measurements of adult worms from the dif-

ferent carnivore hosts were similar when the

method of fixation and the preparation of

whole mounts were the same. Thus the host

species did not appear to influence signifi-

cantly the size of the worms.

DISCUSSION

Although Cuckler (1940, 1941) stated that

mesocercariae of A. marcianae develop to

metacercariae in mice, it was definitely estab-

lished here that they do not advance in de-

velopment in mice, rats, or chicks. Thus avian

and mammalian intermediate host of the meso-

cercariae are paratenic hosts. The life cycle

of A. marcianae is then similar to other known

cycles in the subgenus Alaria (see Pearson,1956, for review of Alaria life cycles).

Since a description of the adult of A. mar-

cianae was not published until 1965, com-

parisons with this species were not included

in the descriptions and taxonomic revisions of

Alaria spp. Adults of A. marcianae are similar

to those of A. canis La Rue and Fallis, 1934;

A. americana Hall and Wigdor, 1918; and

A. minnesotae Chandler, 1954. All four species

possess prominent lappets, a bilobed posterior

testis, an ejaculatory pouch, the same anteriorextent of the vitellaria, eggs of the same size

(Table III), and were described from host

species in the same geographical area (north-

ern USA and Canada).

In fact, there is no doubt that A. minnesotae

is identical to A. marcianae. The adults are

similar in size (Table III) and they have been

reported from the same host species (cat and

striped skunk). Therefore, A. minnesotae is

regarded as a synonym of A. marcianae.

Dubois (1963) considered A. canis a syn-

onym of A. americana. Both species were

described from the dog and, as the brief de-

scription of A. americana along with the flat-

tened and contracted condition of the holotype



330 THEJOURNALOF PARASITOLOGY, OL. 54, NO. 2, APRIL1968

makes a critical comparison with closely related

species difficult, Dubois' opinion is acceptedhere.

A. marcianae is obviously closely related toA. americana, but differs in (1) its smaller size

and (2) its less well developed ejaculatory

pouch. The large, thick-walled pouch in A.

americana was noted by La Rue and Fallis

(1936), by Dubois and Rausch (1950), and

by Dubois (1963). I have also observed it

in adults from the red fox and the coyote,Canis latrans (Say). It extends almost to the

anterior border of the posterior testis and the

walls in whole mounts have been reported

from 35 to 55 , thick (Dubois and Rausch,1950; Dubois, 1963). In A. marcianae the

walls are about 15 / thick and the pouchextends only a short distance past the posteriorborder of the posterior testis.

The life histories of these two species arealike in that the snail hosts are the same, the

cercariae and mesocercariae are similar insize and morphology, and the sporocysts and

metacercariae are similar in morphology (seePearson, 1956, for complete life history of

A. americana). However, A. marcianae differsfrom A. americana in (1) the larger size ofthe mother sporocysts; (2) the marginal ratherthan submarginal location of the furcal excre-

tory pores of the cercariae; (3) the more re-

stricted distribution of body spines in the

cercariae and mesocercariae (spines cover the

entire dorsal surface of both larvae in A.

americana); and (4) the smaller size of the

metacercariae. Of these differences the spina-tion is probably the more significant, since it

is well established in digenetic trematodes

that specific morphological differences maybe found in larval stages when there is littleor no difference between the adults.

The division of the genus Alaria into the

subgenera Alaria and Paralaria was originallybased on the presence of lappets or of pseudo-suckers (Dubois, 1938). The diagnoses were

later extended to include host specificity

(Dubois, 1953). Because pseudosuckers maybe evaginated to resemble lappets and the

latter invaginated to simulate pseudosuckers,the reliability of these organs to distinguishbetween members of the two subgenera has

been doubted (Webster and Wolfgang, 1956;

Dubois, 1963). The basis for this criticism is

evident since these are homologous organs and

in certain strigeoids such as A. mustelae

Bosma, 1931, both forms have been observed

(Dubois, 1963).More recently two additional subgeneric

characters were introduced; namely, the shapeof the posterior testis and the location of the

openings of the forebody gland ducts (Dubois,

1963). This latter character is actually a

reflection of the difference in the shapeof lappets and evaginated pseudosuckers in

Alaria spp.

Notwithstanding some criticism, the two

subgenera have been retained, and the results

here on the behavior of A. marcianae meso-

cercariae in certain intermediate hosts providefurther support for this division. The life cycleof four of the five Alaria (A.) spp. are now

known and in all four species avian and mam-

malian intermediate hosts are paratenic hosts;

i.e., hosts in which no advancement in develop-ment occurs. Of the four species in the sub-

genus Paralaria, only the life history of A.

mustelae is known, but in this case avian

(chicks, personal observations)and mam-

malian intermediate host are auxiliary hosts;

i.e., nonessential hosts in which the meso-

cercariae develop to metacercariae. This dif-

ference in behavior of the mesocercariae rep-resents a distinct biological difference between

members of the two subgenera and is an addi-

tional subgeneric character.

In previous subgeneric diagnoses, members

of the subgenus Alaria were considered to be

common parasites of canids, but A. marcianae

is a common parasite of certain mustelids(skunks) and of cats as reported in this studyand also by Chandler (1954). Pearson (1956)

reported A. americana from a mustelid, the

fisher Martes pennanti (Erxleben), and from

certain felids, the lynx Lynx canadensis Kerr

and the bobcat L. rufus Schreber. However,since there is definitely an adaptation to the

Canidae in the case of the more highly evolved

forms in this subgenus (see Dubois, 1944,

1953), host specificity is retained as a sub-

generic character. Alaria alata (Goeze, 1782)

Krause, 1914, has been reported from canids

and a felid (see Sudarikov, 1960), whereas

A. arisaemoides Augustine and Uribe, 1927,has been reported only from canids.




Emended diagnosis of the subgenus Alaria

Schrank,1788 (after Dubois, 1963): Lappets pres-ent, openings of forebody gland ducts on lateral,

striated margin of lappets. Posterior testis multi-lobed or bilobed. Mesocercariae not advancing in

developmentin avian and mammalian ntermediatehosts (paratenic hosts). Parasites commonly of

Canidae, Felidae, and Mustelidae.

Type: Alaria alata (Goeze, 1782) Krause, 1914

(see Sudarikov,1960 for synonyms)Alaria marcianae (La Rue, 1917) Walton, 1949

Synonyms: CercariamarcianaeLa Rue, 1917;Agamodistomum marcianae (La Rue, 1917)Cort, 1918; Mesocercariamarcianae (La Rue,1917) Olivier and Odlaug, 1938; Alaria min-nesotae Chandler, 1954

Alaria americanaHall and Wigdor, 1918

Synonym: Alaria canis La Rue and Fallis,1934

Alaria arisaemoides Augustine and Uribe, 1927

Synonym: Alaria oregonensis La Rue andBarone, 1927

Alaria nasuae La Rue and Townsend, 1927Emended diagnosis of the subgenus Paralaria

Krause 1914: Pseudosuckerspresent, openings offorebody gland ducts on distal, striated margin ofevaginatedpseudosuckers. Posteriortestis trilobed,lateral lobes may be subdivided into a dorsal andventral lobe. Mesocercariaedeveloping to meta-cercariae in avian and mammalian intermediatehosts (auxiliary hosts). Parasites

commonlyof

Mustelidae.

Type: Alaria clathrata (Diesing, 1850) La Rue,1926

Synonyms: Hemistomum clathrata Diesing,1850 ex parte;Hemistoma clathratumDiesing,1850 ex parte Cobbold, 1860; Haemastomumclathratum Diesing, 1850 ex parte Rosseter,1909

Alaria pseudoclathrata(Krause, 1914) La Rue,1926

Synonym: Hemistomum pseudoclathratumKrause, 1914

Alaria mustelae Bosma, 1931

Synonyms: Alaria freundi Sprehn, 1932; A.intermedia (Olivier and Odlaug, 1938) Od-laug, 1940; A. dubia Chandler and Rausch,1946; A. minuta Chandler and Rausch, 1946

Alaria mustelae canadensis Webster and Wolf-gang, 1956

Synonym: Alaria canadensis Webster andWolfgang, 1956

Alaria taxidea Swanson and Erickson, 1946The host specificity of Alaria (A.) spp. is

not due to an ecological segregation of inter-

mediate hosts (see Pearson, 1956, for review

of intermediate hosts). One aspect of possible

importance may be a difference in the behavior

of mesocercariae in different carnivore hosts.

For example, certain mustelids may not become

infected with A. americana adults simply be-

cause the mesocercariae do not advance in

development. Thus, Pearson (1956) reportedadults of this species from the fisher and en-

cysted mesocercariae from the ferret, Mustela

puttorius (L.) and the otter, Lutra canadensis

(Schreber). In this study A. marcianae meso-

cercariae were fed to a raccoon to determine

their behavior in a carnivore in which the

adults have not been found, but no larvae

lere recovered.

ACKNOWLEDGMENT

I wish to express my appreciation to Dr.

Franklin G. Wallace, adviser for this research,

for his suggestions in the preparation of the

manuscript.

LITERATURE ITED

BOSMIA,N. J. 1931. Alaria mustelae sp. nov., atrematode requiring four hosts. Science 74:

521-522.1934. The life history of the trematode

Alaria mustelae, sp. nov. Tr. Am. Micr. Soc.

53: 116-153.

BURRows, R. B., AND W. G. LILLIS. 1965.

Trematodes of New Jersey dogs and cats.

J. Parasit. 51: 570-574.

CHANDLER, A. C. 1954. New strigeids from

Minnesota birds and mammals. Am. Midl.

Nat. 52: 133-141.

CORT, W. W. 1918. The excretory system of

Agamodistomum marcianae (La Rue), the

agamodistome stage of a fork-tailed cercaria.

J. Parasit. 4: 130-134., AND S. T. BROOKS. 1928. Studies on

the holostome cercariae from Douglas Lake,

Michigan. Tr. Am. Micr. Soc. 47: 179-221.

CUCKLER, A. C. 1940. Studies on the migrationand development of Alaria spp. (Trematoda:

Strigeata) in the definitive host. J. Parasit.

26 (Suppl.): 36.

1941. Morphological and biological

studies on certain strigeid trematodesof

mam-mals. Ph.D. thesis, Univ. of Minnesota,

Minneapolis, 102 p.DUBOIS, G. 1938. Monographie des Strigeida

(Trematoda). Mem. Soc. Neuch. Sci. Nat. 6:

1-535.1944. A propos de la specificite para-

sitaire des Strigeida. Bull. Soc. Neuch. Sci.

Nat. 69: 5-103.

1953. Systematique des Strigeida. Com-

plement de la monographie. Mem. Soc.Neuch. Sci. Nat. 8: 1-141.

.1963. Statut des Alariinae Hall et Wig-dor, 1918 (Trematoda: Diplostomatidae) et

revision de quelques alariens. Bull. Soc.Neuch. Sci. Nat. 86: 107-142.

, AND R. RAUSCH. 1950. Troisieme con-tribution a l'etude des strigeides (Trematoda)nord-americains. Bull. Soc. Neuch. Sci. Nat.73: 19-50.

HALL, M. C., AND M. WIGDOR. 1918. Two new



332 THEJOURNALOF PARASITOLOGY, OL. 54, NO. 2, APRIL196832 THEJOURNALOF PARASITOLOGY, OL. 54, NO. 2, APRIL1968

flukes from the dog. J. Am. Vet. Med. As.

53: 616-626.

LA RUE, G. R. 1917. Two new larval trema-

todes fromThamnophis

marciana and Tham-

nophis eques. Occas. Papers Mus. Zool., Univ.

Mich. No. 35: 1-12.

, AND A. M. FALLIS. 1936. Morpho-

logical study of Alaria canis n. sp. (Trema-toda: Alariidae), a trematode parasite of the

dog. Tr. Am. Micr. Soc. 55: 340-351.

ODLAUG, T. 0. 1940. Morphology and life his-

tory of the trematode, Alaria intermedia. Tr.

Am. Micr. Soc. 59: 490-510.

PEARSON, J. C. 1956. Studies on the life cyclesand morphology of the larval stages of Alariaarisaemoides Augustine and Uribe, 1927 and

flukes from the dog. J. Am. Vet. Med. As.

53: 616-626.

LA RUE, G. R. 1917. Two new larval trema-

todes fromThamnophis

marciana and Tham-

nophis eques. Occas. Papers Mus. Zool., Univ.

Mich. No. 35: 1-12.

, AND A. M. FALLIS. 1936. Morpho-

logical study of Alaria canis n. sp. (Trema-toda: Alariidae), a trematode parasite of the

dog. Tr. Am. Micr. Soc. 55: 340-351.

ODLAUG, T. 0. 1940. Morphology and life his-

tory of the trematode, Alaria intermedia. Tr.

Am. Micr. Soc. 59: 490-510.

PEARSON, J. C. 1956. Studies on the life cyclesand morphology of the larval stages of Alariaarisaemoides Augustine and Uribe, 1927 and

Alaria canis La Rue and Fallis, 1936 (Trema-toda: Diplostomidae). Can. J. Zool. 34:

295-387.

SUDARIKOV,V. E. 1960. Suborder

StrigeataLa

Rue, 1926. (In: Skrjabin, K. I. Trematodes

of animals and man. Moskova, 18: 453-694.

Translation: 1965. Israel Prog. Sci. Transl.

TT64-11055: 323-495.)

WALTON, A. C. 1949. Parasites of the Ranidae

(Amphibia). XIV. Tr. Ill. State Acad. Sci.

42: 161-164.

WEBSTER,G. A., AND R. W. WOLFGANG. 1956.Alaria canadensis sp. nov. and Euryhelmispyriformis sp. nov. from the skunk Mephitis

mephitis in Quebec. Can. J. Zool. 34: 595-601.

Alaria canis La Rue and Fallis, 1936 (Trema-toda: Diplostomidae). Can. J. Zool. 34:

295-387.

SUDARIKOV,V. E. 1960. Suborder

StrigeataLa

Rue, 1926. (In: Skrjabin, K. I. Trematodes

of animals and man. Moskova, 18: 453-694.

Translation: 1965. Israel Prog. Sci. Transl.

TT64-11055: 323-495.)

WALTON, A. C. 1949. Parasites of the Ranidae

(Amphibia). XIV. Tr. Ill. State Acad. Sci.

42: 161-164.

WEBSTER,G. A., AND R. W. WOLFGANG. 1956.Alaria canadensis sp. nov. and Euryhelmispyriformis sp. nov. from the skunk Mephitis

mephitis in Quebec. Can. J. Zool. 34: 595-601.

BOOK REVIEW . . .OOK REVIEW . . .

Animal Agents and Vectors of HlumanDisease byE. C. Faust, P. C. Beaver, and R. C. Jung. Lea

& Febiger, Philadelphia, Third Edition, 1968.ix + 461 p., 186 Figs., 10 Plates, 7 in color.

811.50.

This book is a revised edition of a widely used

textbook of medical parasitology for preclinicalmedical students and trainees in the field of publichealth. The authors state that this edition is

thoroughly revised, and enough significant items

have been added to justify an essentially new

volume. Superficially the third edition looks verymuch like the second. Upon comparison of the

two, however, it is evident that many parts of thetext have been revised or rewritten, and one ob-

tains the impression from an incomplete readingthat the authors have made every effort to bringthe text material up to date and to eliminate super-fluities. Remarkably, this has been done with a

reduction of the book size by 15 pages.This edition has the same table of contents and

general format as the second. Twenty-one chap-ters cover the subjects of general parasitology,protozoan, and helminth agents of human disease,

arthropods as agents and vectors, and technical

Animal Agents and Vectors of HlumanDisease byE. C. Faust, P. C. Beaver, and R. C. Jung. Lea

& Febiger, Philadelphia, Third Edition, 1968.ix + 461 p., 186 Figs., 10 Plates, 7 in color.

811.50.

This book is a revised edition of a widely used

textbook of medical parasitology for preclinicalmedical students and trainees in the field of publichealth. The authors state that this edition is

thoroughly revised, and enough significant items

have been added to justify an essentially new

volume. Superficially the third edition looks verymuch like the second. Upon comparison of the

two, however, it is evident that many parts of thetext have been revised or rewritten, and one ob-

tains the impression from an incomplete readingthat the authors have made every effort to bringthe text material up to date and to eliminate super-fluities. Remarkably, this has been done with a

reduction of the book size by 15 pages.This edition has the same table of contents and

general format as the second. Twenty-one chap-ters cover the subjects of general parasitology,protozoan, and helminth agents of human disease,

arthropods as agents and vectors, and technical

aids. Adequate author and subject indexes areprovided.

After a book has gone through three editions onewould expect that many technical and publicationdefects of previous editions have been found andeliminated. This is certainly true of this book. Afew minor defects, however, still appear. In the

copy for review the new, handsome color plate IVon parasitic amebae is misplaced in chapter 6; itshould be in chapter 4. On page ix a book byWhitlock (1960) is listed as a general reference,but a much more useful book on the same general

subject by Soulsby (1965) is not. In general mostof the illustrations are good to excellent in quality,

but a number of unsatisfactory ones remain, forexample, Fig. 112f, newly hatched Ascaris larva,and Fig. 124, copulatory bursa of male Tricho-

strongylus orientalis.This book gives a concise and accurate account

of animal agents and vectors of human disease,and provides up-to-date information on antipara-sitic medications, diagnostic techniques, and other

aspects of medical parasitology. It is a fine text-book on the subject for medical students.

K. C. Kates

aids. Adequate author and subject indexes areprovided.

After a book has gone through three editions onewould expect that many technical and publicationdefects of previous editions have been found andeliminated. This is certainly true of this book. Afew minor defects, however, still appear. In the

copy for review the new, handsome color plate IVon parasitic amebae is misplaced in chapter 6; itshould be in chapter 4. On page ix a book byWhitlock (1960) is listed as a general reference,but a much more useful book on the same general

subject by Soulsby (1965) is not. In general mostof the illustrations are good to excellent in quality,

but a number of unsatisfactory ones remain, forexample, Fig. 112f, newly hatched Ascaris larva,and Fig. 124, copulatory bursa of male Tricho-

strongylus orientalis.This book gives a concise and accurate account

of animal agents and vectors of human disease,and provides up-to-date information on antipara-sitic medications, diagnostic techniques, and other

aspects of medical parasitology. It is a fine text-book on the subject for medical students.

K. C. Kates

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Alaria marcianae